Modular Assembly of Biomaterials Using Polyphenols as Building Blocks

Review pubs.acs.org/journal/abseba

Cite This: ACS Biomater. Sci. Eng. XXXX, XXX, XXX−XXX

Modular Assembly of Biomaterials Using Polyphenols as Building Blocks Junling Guo,*,†,∥ Tomoya Suma,‡ Joseph J. Richardson,§,⊥ and Hirotaka Ejima*,§ †

Department of Biomass Chemistry and Engineering, Sichuan University, Chengdu 610065, China Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, Massachusetts 02115, United States ‡ Graduate School of Bio-Applications and Systems Engineering, Tokyo University of Agriculture and Technology, 2-24-16, Nakacho, Koganei-shi, Tokyo 184-8588, Japan § Department of Materials Engineering, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8656, Japan Downloaded via BUFFALO STATE on May 1, 2019 at 20:57:08 (UTC). See https://pubs.acs.org/sharingguidelines for options on how to legitimately share published articles.

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ABSTRACT: Polyphenols are building blocks with many advantages for engineering biomaterials because they are abundant in nature, biocompatible, biodegradable, and capable of assembly through different mechanisms. A variety of biomaterials across different length scales can be made with different physical/chemical properties and unique stimuli responses using modular and straightforward synthesis routes. We review the recent progress of biomaterials engineering based on polyphenols under three broad categories, namely, particles, films, and gels. The size and scale of the biomaterial along with the specific building blocks allow for a variety of biological applications including drug delivery and theranostics. The dynamic interactions, assembly processes, biological functions, and applications of a wide variety of representative polyphenol biomaterials are overviewed. KEYWORDS: metal-phenolic networks, drug delivery, theranostics, polyphenols, thin film

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INTRODUCTION Plant polyphenols were traditionally referred to as “vegetable tannins” due to their original use in the process of “tanning” to convert animal skin into leather and thereby impart thermal stability and antibacterial properties.1,2 The development of the leather industry and the corresponding scientific curiosity provided strong motivation for the continuous study of these natural products. Many fundamental and valuable insights about polyphenols were obtained by studies driven by leather chemists.3 The physicochemical properties of polyphenols have been historically linked with biological materials,4 which provides a broad knowledge-base on valuable pathways for the engineering of functional materials. The definition of polyphenols was established through the early understanding of their interactions with proteins, where protein-precipitation was recognized as the defining characteristic of polyphenols.2 With the development of modern analytical chemistry, we gradually gained deeper understanding on polyphenols. Haslam et al.5 further divided polyphenols into two basic categories, hydrolyzable and condensed families. This classification is well-recognized and still used today. The interest in natural polyphenols is attributable to their attractive biological properties, including antioxidant, antiallergic, antibacterial, anti-inflammatory, antitumor, antidiabetic, and antiviral activity.3 Based on these diverse biological functions, polyphenols have been widely used in pharmaceutical research, food industry, leather manufacturing, oil-field chemistry, wood science, water treatment, and so on.6 © XXXX American Chemical Society

In addition to their important roles in traditional applications, polyphenols have been enjoying an everincreasing recognition in multidisciplinary areas where they have been used as fundamental building blocks for the engineering of functional materials (Figure 1). In recent years, this interest in polyphenol-based materials has been growing dramatically especially for biomedicine and biotechnology. The connection between polyphenols and biological applications can be attributed to their generally biocompatible nature as well as their intriguing chemical and physical properties (e.g., metal chelation, hydrogen-bonding formation, and amphiphilic nature). Tea, fruits, and wine all contain an abundance of polyphenols and have been essential parts of human life for millennia.7 Polyphenols are also ubiquitous secondary metabolites in plants, where they play diverse roles in plant defense, including pigmentation, homeostatic mechanisms, metal sequestration, etc. Natural phenolics can be synthesized by two main pathways, namely, the shikimate/chorizmate or succinylbenzoate pathway and the acetate/malonate or polyketide pathway. The shikimate/ chorizmate or succinylbenzoate pathway produces the phenyl propanoid derivatives. This biosynthesis pathway also links Special Issue: Biomaterials Science and Engineering in Japan Received: November 30, 2018 Accepted: April 18, 2019

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DOI: 10.1021/acsbiomaterials.8b01507 ACS Biomater. Sci. Eng. XXXX, XXX, XXX−XXX

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ACS Biomaterials Science & Engineering

Figure 1. Polyphenols can be used as modular building blocks for the engineering of biomaterials. Physiochemical properties of polyphenols: properties commonly used for material engineering, including metal coordination, hydrogen bond formation, oxidation, etc. These diverse properties enable a wide range of interactions between polyphenols and biological systems and also strategies for designing and preparing materials. Material structures: mainly four types of materials are fabricated using polyphenol building blocks. Biological functions: due to the biocompatible properties of polyphenols, these biomaterials have great potentials in applications including drug delivery, diagnostics, cellular biohybrids, antibacterial, and antioxidant materials.

hydrophobic interactions with other aromatic rings through π−π stacking. Hydroxyl groups can act either as donors or as acceptors of hydrogen bonds which contribute to the interactions with proteins and a variety of other biological and synthetic molecules. When two or three adjacent hydroxyl groups appear on the same phenyl ring, these structures are named as dihydroxyphenyl (catechol) or trihydroxyphenyl (galloyl) groups, respectively. Catechol and galloyl groups bear an important function in forming five-sided-ring coordination bonds with different metal ions. Due to the need to deprotonate the hydroxyl groups, the pH of the chemical environment is important for metal complexation and thus higher pH is more favorable for binding metal ions.9 For galloyl groups, the additional third hydroxyl group can lower the pKa of the adjacent two hydroxyl groups, and therefore the metal binding ability of galloyl groups is usually higher than that of the catechol groups. This metal coordination property has been proven to play an important role in plant pigmentation and homeostatic mechanisms.10 Additionally, the presence of a hydroxyl group on aromatic rings can lead to the red shift of the maximum π−π* absorption of benzene (∼254 nm) to the phenol absorption (∼280 nm). Therefore, the phenolic compounds exhibit high UV absorption.11 One of the most important and well used properties of polyphenols is their sensitivity to oxidation processes.12 The relatively weak bond dissociation energy of phenolic O−H bonds leads to the production of highly reactive semiquinone or quinone free radicals.13−15 The free radicals induce further inter- or intramolecular reactions which form a series of complicated oxidative species. While in the presence of some metal ions, such as FeIII or CuII, and upon binding of a catecholate or gallate ligand to the metal, the polyphenol can reduce the metal (i.e., FeIII to FeII) while the polyphenol is

with the acetate/malonate or polyketide pathway to produce the side-chain-elongated phenyl propanoids, including the large group of flavonoids and some derived quinones. On the other hand, the precursor of shikimic acid, 3-dehydroshikimic acid (DHS), on the shikimate/chorizmate pathway can flow into the hydrolyzable tannin pathway to produce simple phenolics including gallic acid, gallotannins, and derivatives. Because of these properties, it has become more and more apparent that the rich scientific history and intriguing inherent properties of polyphenols can provide sources of inspiration for overcoming challenges in biomedicine and biotechnology. In the most recent decade, polyphenols have been widely used as “green” and low-cost building blocks for the engineering of biologically functional materials.8 Additionally, studies on the bionano interactions of polyphenol-based materials have attracted interest from a wide range of fields, especially in cell biology, oncology, and diagnostics. This review summarizes the recent advances in the use of polyphenols as modular building blocks for the engineering of functional materials focusing on the interface between materials science and biological systems. The related biomaterials engineered from polyphenols range from multifunctional particles to thin films, macroscopic gels, and even to living cell biohybrids.

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FUNDAMENTAL PROPERTIES OF POLYPHENOLS FOR BIOMATERIAL ENGINEERING Chemical and Physical Properties of Polyphenols. One of the most important properties of polyphenols is the inherent amphiphilicity, which arises from the combination of hydrophobic aromatic benzene groups and the hydrophilic hydroxyl groups. The aromatic benzene units of polyphenols enable hydrophobic interactions with other molecules such as solvents. Specifically, polyphenols are favorable to form B


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Figure 2. Polyphenol-based engineering of particle systems for drug delivery. (A) Metal library of metal-phenolic networks (MPNs). Lanthanides and transition metal ions as well as main-group elements can be used for the formation of supramolecular metal-phenolic coordination networks. Boronic acid can also be used to form a dynamic boronate-phenolic network for the engineering of particles. Reproduced with permission from ref 28. Copyright 2014 WILEY VCH Verlag GmbH & Co. (B) Optical, AFM, SEM, and TEM images of TA-FeIII capsules after the removal of PS templates. Reproduced with permission from ref 27. Copyright 2013 American Association for the Advancement of Science. (C) Porous templates (CaCO3, SiO2, etc.) can load therapeutic molecules (DOX, PTX, etc.) and then MPNs (e.g., TA-AlIII) can be formed on the loaded-templates. Drug-loaded capsules can be obtained after the removal of the loaded templates. The pH-responsive properties are commonly used for the controlled release from MPN-based particles systems for drug delivery. Reproduced with permission from ref 29. Copyright 2015 WILEY VCH Verlag GmbH & Co. (D) Mesoporous nanoparticles have large internal space with a high drug loading capacity. The TA-CuII network was used to seal the pores of the nanoparticles, and in acidic conditions, the TA-CuII network disassembles and the loaded molecules can be released. Reproduced with permission from ref 30. Copyright 2017 Wiley VCH Verlag GmbH & Co. (E) Due to the porous structure of MOF nanoparticles, they can be used as drug-loaded carriers. MPNs can be formed around the MOF temples and can control the release of the loaded drugs by external stimuli. Reproduced with permission from ref 31. Copyright 2018 Royal Society of Chemistry. (F) Hydrophobic drugs can form self-assembled nanosized crystals which can be used for the cores of drug-loaded MPN nanocapsules. Reproduced with permission from ref 32. Copyright 2016 American Chemical Society.

oxidized to a semiquinone during this process.13 Once the semiquinone radicals are generated, they are capable of reducing another metal ion (i.e., FeIII), in turn oxidizing itself to the quinone state. The oxidative pathways can be varied depending on the chemical environments.14 In alkaline conditions or with certain enzymes, dehydrogenation can occur and lead to the formation of quinones from catechol and galloyl groups, which at the same time behave as electron

donors. Numerous studies have therefore shown that polyphenols can act as scavengers of free radicals and ROS produced under oxidative stress conditions.3 Condensed tannins exhibit nucleophilic properties making them easy to react with electrophiles. There are two important reactions related to this property, namely, bromination and phenolicaldehyde reactions.16−18 C


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ACS Biomaterials Science & Engineering Interaction of Polyphenols with Biological Systems. The initial definition of polyphenols originated from their interactions with proteins. Historically, animal hide was immersed in plant extracts rich in tannins to produce leather.19 The interactions between polyphenols and salivary proteins result in the feeling of astringency.20 The astringent property of polyphenol protects plants from animals and insects, thus playing an important role in the plant’s natural defense systems.21 The polyphenol−protein interaction is attributed to the hydrophobic interaction−multiple hydrogen bonding theory, which is systematically proposed by Haslam and co-workers based on previous understanding.22 In the secondary structure of proteins, there are abundant aromatic, aliphatic, and other hydrophobic domains of amino acids, which together form hydrophobic pockets. The interactions between polyphenols and proteins are facilitated by hydrophobic interactions and multiple hydrogen bonds. In the initial stage, the catechol or galloyl groups that contain a hydrophobic moiety approaches into the hydrophobic pocket of proteins via hydrophobic interactions. In the final stage, the phenolic hydroxyl groups can interact with the polar groups, such as peptide linkages, hydroxyl groups, and carboxyl groups, to form two-pointpaired hydrogen bonds. These two driving forces (i.e., hydrophobic interactions and hydrogen bondings) work together to form stable polyphenol−protein complexes. This process is dependent on the molecular size of the interacting molecules and is therefore recognized as a typical example of a molecular reorganization process.4 Most of the interactions between polyphenols and proteins are dynamic and reversible; however, covalent bonding processes can occur under certain conditions, such as in the presence of oxygen, metal ions, and enzymes.2 In addition to the interactions with proteins, polyphenols can also interact with many other biological molecules, including alkaloids, polysaccharides, phosphatides, and nucleic acids.23−26 Based on experimental and simulation results, all of these interactions can be recognized as molecular recognition processes, depending on the molecular size and flexibility via hydrophobic interactions and hydrogen bonding in a dynamic reversible process. X-ray diffraction spectra of crystalline polyphenol−caffeine complexes revealed that both hydrophobic interaction and hydrogen bonding contributed to the complexation.22 Experimental results demonstrated that the aromatic rings of polyphenol and caffeine stack to form a “sandwich-like” layered structure. Hydrogen bonds between the hydroxyl groups of polyphenol molecules and nitrogen atoms in caffeine molecules further stabilize the layered structure. There is also extensive evidence supporting the conclusion that molecular polarization also contributes to the formation of these complexes.22 As for the interactions between polyphenols and polysaccharides, the molecular mechanism is more complicated. For example, in the case of β-cyclodextrin,2 association occurs highly selectively in the region of the hydrocarbon cage through hydrophobic interactions. After the insertion of the phenolic group or whole polyphenol molecule, hydrogen bonds are formed with the interior wall of β-cyclodextrin.2

multifunctional modular building blocks to assemble different types of particles through templating or template-free methods. Metal-phenolic coordination, self-oxidation, and hydrogen bonding provide driving forces for the assembly. These particulate systems have been demonstrated to apply in a wide range of applications including drug delivery, bioimaging, diagnostics, antibacterial function, and dental health care. Polyphenol-Based Hollow Capsules for Drug Delivery. The assembly of phenolic building blocks on sacrificial dissolvable particles (e.g., SiO2, PS, CaCO3) leads to the uniform construction of spherical and nanostructured film on these template particles. After the removal of the template particles, hollow microcapsules with a uniform size distribution can be obtained (Figure 2A−C). Ejima et al.27 demonstrated the formation of FeIII-TA networks on PS particles followed by dissolving PS templates to obtain FeIII-TA capsules. Due to the dynamic FeIII-TA coordination linkages, these capsules can be disassembled in acidic environments where disassembly occurs more rapidly at lower pH. Guo et al.28 further established a library of functional metal-phenolic network (MPN) capsules prepared from a ubiquitous natural polyphenol coordinated to 18 different metal ions, namely, AlIII, VIII, CrIII, MnII, FeIII, CoII, NiII, CuII, ZnII, ZrIV, MoII, RuIII, RhIII, CdII, CeIII, EuIII, GdIII, and TbIII (although other metal ions should also be usable), to generate robust MPN films capable of forming hollow structured capsules. The properties of the MPN capsules are determined by the coordinated metals, allowing for control over film thickness, disassembly characteristics, and fluorescence behavior, among other properties. DOX was first loaded in the AlIII-TA capsules and used as a pH-responsive carrier for intracellular drug delivery. The MPN capsules exhibited a high drug loading capacity (1.3 pg of DOX per capsule), which led to effective toxicity in HeLa cells with an IC50 value of 0.20 μg/ mL.29 The building blocks of metal ions were later expanded to titanium ions (TiIV), where the strong coordination bond between TA and TiIV enables the TA-TiIV capsules to retain high structural stability in the pH range of 3−11. Additionally, TA-TiIV capsules provide superior pH and thermal protection to loaded enzymes in the capsules. Metal-phenolic coordination provides pH-responsive properties to the MPN-based capsules, which is crucial for intracellular drug release due to the acidic microenvironment during endocytosis. However, such a singular biological trigger lacks the capacity to respond to complex microenvironments in the same, versatile way observed in nature, where dual or multiresponsiveness exists in complex biological environments. Guo et al.33 reported biologically relevant, dual responsive BPN capsules. The BPN capsules have a chemically defined mechanism for the pH and cis-diol responsiveness due to the dynamic nature of the reversible boronate ester bonds. The release of DOX from the capsules could be increased by decreasing the pH and/or adding cis-diols. This efficient combination of rapid complexation and dual stimuli responsive mechanisms provides a novel avenue for the design of “smart” capsules for a range of biological applications, including closed loop insulin delivery systems by glucose activation and anticancer drug delivery by an acidic pH trigger. Self-Assembled Polyphenol-Based Nanoparticles and Core-Shell Particles. Different template particles can be used for the engineering of polyphenol-based capsules, including MSNs,34 MOFs,35 drug molecule crystals,32 and emulsions,36 among which MSNs were demonstrated as well-studied templates (Figure 2D). DOX was used as model drug and

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POLYPHENOL-BASED MICROPARTICLE SYSTEMS Natural polyphenols and their synthetic derivatives have been used to construct a wide range of particulate functional materials or cell-integrated biohybrid systems. They are used as D


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ACS Biomaterials Science & Engineering loaded in the MSNs, followed by the coating of FeIII-TA to lock the DOX molecules inside the mesopores. Upon decreasing the pH, a burst release can be achieved and the MRI signal intensity was reduced due to the change of coordination stoichiometry of FeIII and TA.34 MPNs have also been used as controllable nanoscale gates for the stimuliresponsive release of guest molecules from MSNs.30 This work showed that the flexible structure of TA on the walls of the MSN pores provided open channels for cargo loading. However, when TA coordinated with Cu2+ ions, the pore channels closed, which prevented the release of cargo molecules. Interestingly, with the exposure of UV light, photolysis of photoacid generators, PAGs, led to the generation of acid, triggering the disassembly of the TA-CuII network, which opened the nanoscale gate for the release of the cargo molecules. A hydrophobic model drug, curcumin, showed sustainable drug release from MPN-coated MSNs under physiological conditions (pH 7.4), while a rapid drug release was observed by lowering the pH to 6.0 or 4.5. Interestingly, the release of curcumin could be controlled by adjusting the external glutathione concentration probably due to the accelerated disassembly of TA-FeIII complex by competitive liganding.37 Yao et al.38 used ZnII-TA and BPN networks as a gate-controller for the pH-responsive release of DOX from MSNs. Additionally, AlIII-TA coatings were applied to seal in siRNA and provided a pH-responsive controllable release in the cytoplasm of human osteosarcoma cancer cells.39 Supraparticles composed of MSNs and upconversion nanoparticles were engineered by the polyphenol-based interfacial assembly method. These supraparticles enabled kinetic monitoring of DOX release by FRET.40 MOF particles are often used as a template due to their highly porous structure and drug loading capacity (Figure 2E). ZIF-8 nanoparticles were used as templates on which dopamine-modified alginate and FeIII ions were complexed and deposited. These pH-responsive nanocapsules (∼120 nm) can load and release DOX in a controlled manner.35 ROSresponsive nanocapsules were engineered using MOF templates. DOX-doped ZIF-8 nanoparticles were coated with a EGCG-FeIII layer followed by ZIF-8 removal. The capsules eliminated the overproduced ROS of tumor cells.31 Drug molecules can form crystal particles which can be used as building blocks for the engineering of polyphenol-based drug delivery particles (Figure 2F). Hydrophobic drug (PTX) nanoparticles were stabilized by the interfacial assembly of TAFeIII coating on the surface. In vivo results indicate that these PTX@TA-FeIII nanoparticles have more effective antitumor activity and can be administered with higher dosage than the commercially approved Taxol.32 The PTX nanoparticles were generated by an aerosol spraying process and coated with MPNs.41 The in vivo results demonstrated that the nanoparticle formulation greatly improved antitumor activity (69.2% tumor growth inhibition rate), compared to free PTX drugs (14.7%). Moreover, the integration of MPN films on crystallized DOX nanoparticles can monitor the release of DOX. This is based on the mechanism that the fluorescence of DOX can be quenched when DOX is loaded on the TA-FeIII. The acidity of the lysosome triggered the release of DOX, and fluorescence recovery was observed, which enabled real-time monitoring of drug release in tumor cells. In vivo studies further indicated that this MPN-based DOX delivery system could significantly inhibit tumor growth with negligible heart toxicity.42

Polyphenol moieties, including catechol and galloyl groups, can be used as modular groups for the functionalization of other molecules (e.g., drugs or functional polymers).43 Dai et al.44 conjugated gallyol groups with a Pt prodrug to form a polyphenol-functionalized Pt prodrug. Template-free selfassembled PEG-modified Pt prodrug nanoparticles (∼100 nm) were synthesized through metal−polyphenol complexation combined with emulsification. These self-assembled nanoparticles exhibited high drug loading (0.15 fg Pt per nanoparticle) and low fouling properties due to the direct conjugation of polyphenols with PEG and prodrug molecules. The in vivo antitumor activity was four times better than either free prodrug or cisplatin. DOX and platinum drugs can both activate NADPH oxidases which generates superoxide radicals which synergize the chemotherapy by a cascade of bioreactions.45 The coassembly of Pt prodrug nanoparticles with hypochlorous acid can further improve the therapeutic efficacy of platinum drugs and effectively inhibit tumor growth in vivo.46 DEX and TA can form self-assembled nanoparticles with approximately 10% DEX loading. The TA-DEX nanoparticles showed responsive release behavior in the presence of esterase and scavenged radicals at the inflammation sites. These TA-DEX nanoparticles achieved remarkable treatment efficacy in colitis mice compared with the single building blocks individually. 47 Shin et al. 48 showed that the modification of protein and peptide therapeutic molecules with TA could improve their ability to specifically target heart tissue. Specifically, TA-modified proteins penetrated the endothelium and were bound to the myocardium extracellular matrix. In a rat model of myocardial ischemia-reperfusion injury, TA-modified fibroblast growth factor significantly reduced the infarct size and increased the cardiac function. Li et al. reported the engineering of self-assembled nanoparticles composed of Sm3+ ions, and small phenolic building blocks epigallocatechin-3-gallate (EGCG) and (−)-catechin (EC). The combination of lanthanide ions and phenolics provide remarkable selective cytotoxicity to colon cancer and metastatic melanoma.49,50 Nanoparticles, including Au nanoparticles, zein nanoparticles, and nanodiamonds, can be used as cores for the engineering of phenolic composite particle systems. EGCG and gelatin-DOX conjugates were used as building blocks to coat Au nanoparticles for fluorescence imaging and inhibition of prostate cancer cell growth.51 Oxidative self-polymerization of polyphenols formed polymeric coating on zein nanoparticles, which were degradable at acidic pH. The high level of intracellular glutathione concentration induced the biodegradation of the polyphenol coatings, resulting in a fast release of trapped anticancer drugs in the cells.52 Au nanorods were coated with GdIII-TA network to realize combination therapy for metastatic tumors. These nanocomposites could enhance antitumor therapeutic effects in vitro and in vivo with the combination of photothermal therapy and chemotherapy. The invasion and metastasis were inhibited due to the presence of polyphenol compounds.53 The encapsulation of exosomes with MPN layers protects exosomes from external aggressors and provided controllable degradation in cells.54 DOX-loaded MPN-coated exosomes could even selectively kill cancer cells. Bio-Nanointeractions of Polyphenol-Based Particles. Modulating protein corona can regulate the properties and functionalities of engineered particles. Ju et al.55 engineered MPN capsules with both high-targeting and low-nonspecific cell binding properties by coating catechol-functionalized HA E


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Figure 3. Polyphenol-based engineering of particle systems for theranostic applications. (A) Different metal ions coordinated in MPN systems for biomedical imaging functions. For example, EuIII and TbIII were complexed with coligands for fluorescence imaging; 64Cu can be used for PET imaging; FeIII, MnII, and GdIII based MPN capsules showed MRI relaxation. Reproduced with permission from ref 28. Copyright 2014 WILEY VCH Verlag GmbH & Co. (B) The incorporation of FeIII, VIII, and RuIII enables MPN-based nanoparticles to achieve high-performance photothermal efficiency. These MPN nanoparticles were used for tumor targeting NIR photothermal therapy coupled with photoacoustic imaging and MRI. Reproduced with permission from ref 66. Copyright 2018 American Chemical Society. (C) Catalytic activity of FeIII in MPN converts excess H2O2 to O2 microbubbles in the pathologic sites. These microbubbles can be detected by ultrasound imaging for diagnostics. Reproduced with permission from ref 67. Copyright 2015 WILEY VCH Verlag GmbH & Co. (D) Polyphenols extracted from blue honeysuckle were used to assemble MPN nanoparticles with theranostic properties (photoacoustic imaging, MRI, and high photothermal efficiency). Reproduced with permission from ref 68. Copyright 2018 American Chemical Society.

and PEG on calcium carbonate templates. The incorporation of HA significantly enhanced the association with a CD44 overexpressing (CD44+) cancer cell line, while the incorporation of PEG reduced nonspecific interactions with a CD44 minimal-expressing (CD44−) cell line. Moreover, the targeting specificity of HA-based MPN capsules was enhanced as a result of the formation of a protein corona.56 PEG-polyphenol ligands can be self-assembled on the liquid−liquid interface of oil-in-water emulsions. PEG provided a protective barrier on the emulsion phase and rendered the emulsion low fouling. The MPN-coated emulsions exhibited a low cell association in vitro and a blood circulation half-life of ∼50 min in vivo and are nontoxic to healthy mice. Furthermore, DOX can be encapsulated within the emulsion phase at a high loading capacity (∼5 fg of DOX per emulsion particle).57 Hydrogen Bonding as Driving Force for Particle Formation. The driving force for the assembly of phenolic building blocks is not limited to metal coordination. Hydrogen bonding and self-polymerization also serve as useful chemical strategy for synthesizing polyphenol-based particles. Liang et al.58,59 reported a novel versatile pH-responsive system based on hydrogen-bonded PEG/TA coatings on zein nanoparticles. These hydrogen bonding-based capsules could be used to load hydrophobic (e.g., vitamin D3) and unstable molecules

through interacting with zein by hydrophobic interaction. ARGET ATRP enabled the engineering of hybrid PDA/ PNIPAM nanocapsules with tunable morphologies, including core−shell, yolk−shell, and hollow capsules.60 Cubic manganese carbonate particles were used as sacrificial cores to form hydrogen-bonded TA/PVPON cubic capsules. The cubic shape could enhance the particle−cell interactions with breast cancer cells.61,62 PDA microcapsules were also developed as carriers for insulin delivery.63 The PDA capsules were stable for at least 60 days, making them promising for long-term storage and transportation of insulin for administration in diabetic patients. Complex capsules were fabricated by combining the polymerization of dopamine with hydrogenbonded LbL assembly of dopamine-modified PAA and PVPON. These complex capsules exhibited pH-responsive swelling−shrinking behavior.64 Polyphenol-Based Theranostics. The coordination of different metal ions and conjugated π electrons provide a broad platform for the engineering of phenolic particles with bioimaging functions (Figure 3). To impart fluorescence properties to the MPN capsules, Guo et al.28 incorporated lanthanides (EuIII and TbIII) with coligands into MPN capsules. The bioimaging function of MPN capsules was further extended by incorporating metals useful for PET and F


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ACS Biomaterials Science & Engineering MRI. Radioactive 64CuII-TA capsules were prepared by adding 5 MBq of 64Cu during MPN film assembly. When FeIII, MnII, and GdIII were incorporated into MPN capsules, the MPN capsules exhibited MRI imaging contrast. Among them, MnIITA capsules displayed the highest relaxivity r2 which was for in vivo use. Due to the ease of incorporating different metals, MPNs are promising for multimodal bioimaging. For example, (64CuII/EuIII-TTA)-TA capsules were used for both PET and fluorescence imaging. Zhu et al.65 engineered multimodal contrast agents by coating BaGdF5 nanoparticles with europium-based MPNs. The composite nanoparticles showed better cytocompatibility and lower cytotoxity than bare BaGdF5 nanoparticles and were promising for X-ray CT/ MRI/luminescence imaging. The coordinated metals can react with biological compounds and generate bioimaging signals. The nanoporous FeIII−TA replica particle was prepared by the replication of nanoporous CaCO3 particles infused with FeIII−TA complexes.67 Interestingly, the FeIII ions chelated by the phenolic ligands possess catalytic activity that converts H2O2 into O2 microbubbles under physiological pH. Under pathological conditions, tissues produce elevated levels of H2O2. The conversion of H2O2 to O2 microbubbles changed the acoustic impedance and could thereby be detected by ultrasound imaging in real time. The in vivo results based on glutathione peroxidase-1 knockout (GPx1−/−) mice demonstrated the potential of MPN particles for advanced ultrasound imaging in biomedical research. Alford et al.69 further used this catalytic activity of Mn and engineered manganoporphyrin-polyphenol capsules. These capsules exhibited enhanced radical-scavenging activity. Liu et al.70 reported ultrasmall coordination polymer nanodots by one-pot self-oxidation of TA and FeIII ions. These nanodots exhibited pH-activatable MRI contrast and outstanding photothermal performance. MRI-guided photothermal therapy completely suppressed tumor growth. Liu et al.66 reported a family of photothermal MPN-based materials by using FeIII, VIII, and RuIII as metal species. These assemblies were validated for tumor-specific photoactivated utilization, including NIR photothermal therapy with complete tumor elimination as well as photothermal and photoacoustic imaging in addition to T1-MRI imaging. Additional doping of MnII and a hydrophilic NIR fluoroprobe enabled T2-MRI and NIR fluorescence imaging, respectively. Natural anthocyanins extracted from blue honeysuckle (Lonicera caerulea L.) were used to engineer multifunctional nanoparticles possessing T1 relaxivity and strong absorption in the NIR region. The nanoparticles served as a contrast agent for MRI and photoacoustic imaging as well as a photothermal agent for photothermal therapy. MRI and photoacoustic contrast facilitated precise photothermal therapy by accurately locating tumor tissues. Furthermore, in vivo dynamic disassembly initiated by deferoxamine mesylate was demonstrated. The deferoxamine mesylate is an iron chelator that clinically reduces excess iron in the body.68 The integration of phenolic building blocks with inorganic nanoparticles provides additional avenues for accessing unique bioimaging functions. TA was used to integrate with magnetic Fe3O4 nanoparticles, and these Fe3O4@TA-PEG/ICG assemblies exhibited ATP-responsive and pH-facilitated disassembly due to the competitive binding of ATP to TA. A change of the transverse relaxivity and potent “turn-on” of fluorescence during the disassembly process enabled effective tumor dual-

modal imaging (MRI/fluorescence) and photothermal therapy.71 Magnetite/gold hybrid nanoparticles were synthesized from a single iron precursor (ferric chloride) through a polyphenol-based method using grape seed proanthocyanidin as the reducing and capping agents. CT imaging demonstrated high X-ray contrast, which can be attributed to the nanogold component in the hybrid. In vitro experiments demonstrated the potential application of this bimodal nanoconstruct for stem cell tracking and imaging.72 Fluorescent nanodiamonds are attracting major attention in the field of biosensing and biolabeling, and photoluminescence from single nitrogenvacancy defects in nanodiamonds was enhanced by MPN coating.73

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POLYPHENOL-BIOLOGICAL HYBRIDS Polyphenols can be used as coating agents for cells and enzymes to assemble polyphenol-biological hybrids. This provides a wide range of functions and potential applications, including decreasing the surface charge of cells,27 cytoprotective effects,74 enhanced cell activity, cell manipulability, and biosynthesis.75 Park et al.76 applied the MPN coating on yeast cells and demonstrated single-cell encapsulation. This system provided cytoprotection against multiple external aggressors, including UV irradiation, lytic enzymes, and silver nanoparticles. A cell-wall-like shell was constructed around proteinosomes by coordination complexes of TA and FeIII,77 which endowed the engineered proteinosomes with an enhanced Young’s modulus of the membrane, protease resistance, EDTA-mediated release of loaded DNA, electrostatic gated enzyme activity, as well as antioxidant capacity. Kim et al.78 reported a water−oil interfacial supramolecular self-assembly of FeIII ions and TA in biphasic systems. This versatile method allowed for cell encapsulation with various biphasic systems. The hollow microcapsules were loaded with yeast cells, Jurkat cells, and red blood cells. Pham-Hua et al.79 demonstrated that a novel cytoprotective multilayer coating for islet encapsulation consisting of TA/PVPON. The coating was efficacious in dampening in vitro immune responses involved in transplant rejection and preserving islet function, including decrease of chemokine synthesis and diabetogenic T cell migration. Moreover, PVPON/TA-encapsulated islets restored euglycemia after transplantation into diabetic mice. Polyphenols have been widely used for the synthesis of a range of nanoparticles, including gold, silver, iron oxides, etc. One of the distinct differences between polyphenol-based synthesis and other methods is the high biocompatibility. Different polyphenols, such as EGCG, resveratrol, fisetin, and high-molecular-weight tannins, can be used for the noble metal nanoparticle synthesis and a wide range of other applications has been studied, including cellular tracking, antioxidant, antitumor effect, antibacterial effect, etc. Debnath et al.80 reported a nanoparticle form of EGCG of ∼25 nm in diameter which is 10−100 times more efficient than molecular EGCG in inhibiting protein aggregation, like extracellular amyloid beta or intracellular mutant huntingtin protein aggregates. A largescale synthesis of autofluorescent tea polyphenol-based core− shell nanoparticles under microwave irradiation was also reported.81 These heterogeneous nanoparticles strongly inhibited E. coli growth with no obvious toxicity to normal cells. Polyphenols were also used as modular connecting materials for the engineering of yeast-semiconductor biohybrids.82 These polyphenol-linked biohybrids can harvest light and convert to reduction potential (e.g., NADPH) and G


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Figure 4. Polyphenol-based engineering of thin films. (A) Formation of adherent and free-standing MPN films of different shapes and geometries using a continuous growth process. (a) Schematic illustration of the thin film deposition process. (b−g) Different 2D and 3D freestanding MPN films. Reproduced with permission from ref 107. Copyright 2018 American Chemical Society. (B) Formation of MPN films at liquid−air interfaces through the oxidation of FeII to FeIII and the subsequent lift-off and stamping of the films. (a) Mechanism of MPN film formation at the liquid−air interface. (b) Stamping of MPNs onto different substrates. (c) Immersion of free-standing MPN films into different solvents. Reproduced with permission from ref 112 Copyright 2018 WILEY VCH Verlag GmbH & Co. (C) Deposition of PDA and subsequent metallization of the films on various substrates. Metallization of copper on PDA-coated (A) nitrocellulose, (B) dimes, and (C) plastic die. Note that parts B and C represent before and after images as left and right, respectively. (D) PDA coatings and metalization can also be combined with lithographic techniques to access unique thin film patterns. Reproduced with permission from ref 87. Copyright 2007 American Association for the Advancement of Science.

used (e.g., PEG−DOPA, HA−DOPA, TA-modified peptides).55,99,100 Moreover, the metal ions retain their functionality when incorporated into MPNs, allowing for a variety of applications and unique disassembly profiles, as described in the particle section.29 Substrates ranging from inorganic materials to organic materials to biological materials can all be coated with MPNs.27,76,84,101−104 Various techniques have been developed to deposit MPNs (Figure 4A,B) after the initial report on the near-instantaneous self-assembly of roughly 10 nm films,27 where the ionic strength used for assembly can increase the thickness and roughness marginally and high precursor concentrations can allow for sustained growth.105−107 Guo and Richardson et al.105 explored the influence of ionic strength on the conformation of MPN precursors in solution and how this determines the final thickness and morphology of MPN films. This work showed that the film thickness can increase ∼50%, from 10 nm in 0 M NaCl to 15 nm in 1 M NaCl, while at even high concentrations the films grow rougher rather than thicker. Small-angle X-ray scattering and molecular dynamics simulations suggested that at a higher ionic strength, Na+ ions shield the galloyl groups of TA, allowing extension away from the FeIII center. This then allows further interaction with other MPN complexes in solution to form thicker and rougher films. Spray assembly allows for the facile deposition of MPN films with a high-degree of control over thickness,108 and even gradient films can be assembled using spray-assembly and masks.109 Microfluidics can be used to continuously assemble MPN films around emulsions,78 while the use of solid metal sources (i.e., rust) can lead to the continuous generation of MPNs on substrates in solution.110 A more complex route for assembling MPNs is the oxidation of FeII into FeIII either using an electric current for the rapid assembly or the presence of

eventually facilitate the biosynthesis of drug precursor shikimic acid. This polyphenol-based modular biohybrid platform could be extended to the biosynthesis of a wide range of biomedical molecules through rational design of metabolic pathways.

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POLYPHENOL-BASED FILMS Thin films are useful materials capable of controlling the interaction between substrates and their environment and have been developed for biomedical, catalytic, and environmental applications.83−86 The various chemical functional groups displayed by phenolic molecules allow for physical and chemical attachment to diverse substrates, which has allowed for the formation of different classes of functional phenolic thin films.27,87,88 Not only do the physicochemical properties of phenolics allow them to adhere to various substrates, it also allows phenolics to self-assemble with other materials into thin films through a variety of chemical interactions.27,89 For example, thin films can be self-assembled through chelation with metals, hydrogen bonding, or electrostatics with metals, polymer, micelles, biomolecules, etc.90−92 Additionally, phenolics can often chemically react with themselves to form polymerized phenolic films.87,93 For example, dopamine can self-polymerize into phenolic thin films with various functionalities.87 This section introduces a variety of phenolic thin films assembled through self-assembly and polymerization but is not an exhaustive list. Self-Assembly of Phenolic Thin Films. MPNs are the most recently introduced class of self-assembled phenolic thin films where various metals (e.g., FeIII, AlIII, EuIII, CuII, GdIII, RhIII) and boron-containing metalloids cross-link phenolic molecules (e.g., TA, EGCG, GA, PG) via chelation.27,28,33,94−98 Often natural phenolics are used; however, synthetic catechol- and gallol-containing analogues can also be H


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Figure 5. Polyphenol-based engineering of gel systems based on different types of cross-linking chemistry. (A) Tissue adhesive catechol-modified hyaluronic acid hydrogel. (a) Adhesive HA-CA hydrogel immediately (left) and 2 weeks (right) after injection-free transplantation of hepatocytes to the liver. (b) Enhanced viability of hADSCs encapsulated in HA-catechol hydrogel was observed, compared to HA-methacrylate hydrogel (green, live; red, dead). Scale bar = 200 μm. Reproduced with permission from ref 168. Copyright 2015 WILEY VCH Verlag GmbH & Co. (B) Temperature-responsive shape memory PVA−TA hydrogel. (a) Mechanism of shape memory is through the temperature responsive formation and reformation of hydrogen bonding. (b) Shape memory behavior of a PVA−TA hydrogel prepared at 25 °C. Reproduced with permission from ref 181. Copyright 2016 American Chemical Society. (C) Metal-phenolic coordination for gelation. (a) Gelation of four-arm-PEG−catechol with FeIII based on pH-dependent metal-phenolic coordination. (b) Self-healing properties of the gels, compared to the covalently cross-linked gels. Reproduced with permission from ref 184. Copyright 2011 Niels Holten-Andersena, Matthew J. Harrington, Henrik Birkedal, Bruce P. Leed, Phillip B. Messersmith, Ka Yee C. Lee, and J. Herbert Waite. (D) Tunable gel mechanics with different dynamics of cross-linking. Schematics of the gel network and photo images of the gels formed by Fe3O4 nanoparticle-cross-linked hydrogel (NP gel), metal-ion coordination (FeIII gel), and covalent (CV gel) cross-linking are shown with a step strain (10%) relaxation curves at 20 °C. Reproduced with permission from ref 191. Copyright 2016 American Chemical Society.

films can be deposited onto nearly any macroscopic, microscopic, planar, or particulate substrate under mildly basic conditions (Figure 4C).87,125,128,132 Various external and internal parameters can be tuned to expedite and control PDA formation, including stirring, dopamine concentration, presence of oxygen and oxidizing agents, elevated temperature, and microwaves, where time is commonly the most used variable to control the film thickness.133−137 The resultant functional handles of PDA are more versatile than standard phenolics due to the presence of both amines and hydroxyls.138,139 Therefore, materials can be covalently attached to the PDA films including biomolecules,140 other large macromolecules like synthetic polymers,141−143 small molecules like drugs,144,145 and initiators.60,146−149 Noncovalently, the same driving forces used for the self-assembly of phenolic films described above can be used for postfunctionalizing PDA films including hydrogen bonding, chelation, and hydrophobic interactions.150−153 Moreover, PDA-polymer blends can be created by adding polymers into the dopamine solution prior to PDA formation.154 Other catechol- and gallol-containing phenolic materials can be induced to polymerize to form phenolic films.155 Similar to PDA, these films can be postmodified chemically156,157 and can be polymerized using routes other than high pH including UV radiation and small molecules such as trimesoyl chloride.158−160

oxygen for a more sustained assembly, where the films can be grown from hundreds to thousands of nanometers.111,112 TA has also been widely used to interact with various polymers for the formation of metal-free phenolic thin films, generally through hydrogen bonding and electrostatic interactions.89 For example, various biological and synthetic polymers, such as chitosan, PDDA, PVPON, PAH, PEI, PNIPAM, poly(N-vinylamide)s, and poly(2-ethyl-2-oxazoline), can all be used.64,89,91,113−115 As TA has multiple pHdependent protonation states, the pH of the polymer and TA solutions influence the resultant film properties.116 The exact physicochemical properties depend on whether the films were formed through electrostatics or hydrogen bonding, where high pH (deprotonated TA) favors electrostatics and low pH (protonated TA) favors hydrogen bonding and hydrophobic interactions.91,114 Additionally, more complex macromolecules115,117 and assemblies can be used to interact with phenolics and form thin films.118 For example, micelles119 and proteins, including enzymes, can interact with TA to form films,120 where TA does not necessarily inhibit the enzymatic activity or disrupt the micelles during film formation. Finally, the hydroxyl groups of TA can be chemically modified to yield self-assembling building blocks useful for forming films and particles.121,122 Polymerization of Phenolic Films. Dopamine is commonly polymerized into PDA, through a variety of routes 123−127 mimicking the adhesion of mussels to surfaces.87,93,128−131 Like self-assembled phenolic films, PDA I


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POLYPHENOL-BASED HYDROGELS The chemistry of phenolic network formation expands from nanoparticles and thin films to bulk materials. An important class of such bulk materials is “gel”, which is an insoluble threedimensional molecular network containing a large amount of solvent. The near universal adhesiveness of phenolic hydrogel to biological tissues has been a motivation for development of gel-based materials from phenolic building blocks. In contrast, recent studies leverage the ability of phenolic functional groups to form covalent and noncovalent chemical linkages for the development of functional materials, because the intermolecular interactions used for gelation is a critical factor for gel properties. Furthermore, the various phenolic building blocks can be readily obtained naturally, by conjugation of phenolic groups to presynthesized polymers161 and by synthesizing polymers from phenolic monomers.161−164 All of these advantages provide a great degree of freedom in designing gel-based materials with tailored functionalities. In this section, the recent advances in the assembly of gel-based biomaterials from phenolic derivatives are described. Hydrogels Based on Covalent Cross-Linking. Early studies focused on the oxidative coupling reaction between phenolic functional groups (e.g., catechol) or between phenolic functional groups and nucleophiles (e.g., amines and thiols) through Michael addition and Schiff base reaction, resulting in covalently linked hydrogels. Gelation of a variety of polymers was achieved by grafting phenolic functional groups in the side chain of the polymers, followed by chemical or enzymatic oxidation (e.g., tyrosinase, H2O2, NaIO4, and O2).165,166 The mechanical properties of the gels can be controlled by the degree of phenolic modification.167 The robustness of this approach is demonstrated by many examples of hydrogels prepared from biopolymers such as HA,168 alginate,169 poly(Llysine),165 and chitosan170 as well as synthetic polymers such as PEG166,167 and PS.171,172 Such hydrogels show excellent adhesiveness to biological tissues. For example, the four-armPEG-catechol hydrogel showed several times stronger adhesiveness, when compared to commercially available fibrin glue.173 On the other hand, the oxidative coupling is a simple yet advantageous approach for biological applications, because the gelation proceeds in mild conditions without the use of toxic photoinitiators or ultraviolet irradiation.166,168 For example, high viability of encapsulated cells and reduced inflammatory cytokine (TNF-a) secretion was observed in the gels from HA-catechol conjugate, when compared to the gels from the hyaluronic acid-methacrylate conjugate that needed photopolymerization for gelation (Figure 5A).168 In addition, the hyaluronic acid-catechol hydrogel remained attached to liver and heart tissue for at least 2 weeks after application, demonstrating the utility of phenolic hydrogels for tissue engineering and cell therapy applications (Figure 5A).168 The phenolic groups can form covalent linkages with nucleophiles through Michael addition and Schiff base reaction. In a recent example, the chitosan-catechol polymer film coated on the surface of injection needles undergoes in situ solid-gel transition (G″ > G′) after puncture, thereby effectively inhibiting bleeding.174 The hydrogels are crosslinked by the oxidative cross-linking between amino groups of chitosan and catechols. Notably, the elastic modulus of the hydrogel further increased upon contact with human plasma. This indicated that the human plasma proteins and/or other components can also participate in the network formation in

vivo after administration, as they are rich in amino and thiol groups. Meanwhile, such reactions with biological components can be used to tighten the network to change the permeability of the gels in vivo. The chitosan-catechol gel patch was placed to cover a drug-releasing fibrin gel that was applied to the cartilage. The exposed surface of the gel patch solidifies upon contact with blood, thereby achieving directional drug release to the cartilage by blocking isotropic drug release.175 Hydrogels Based on Hydrogen Bonding. The phenolic compounds interact noncovalently through hydrogen bonding, which can also be used as a driving force for gelation. For example, TA can hydrogen bond with the phosphodiester moiety of DNA, resulting in hydrogelation.176 The DNA/TA hydrogel was adhesive, extensible, and biodegradable and displayed hemostatic ability in vivo. The hydrogen bonding of phenolic groups is not limited to DNAs but includes other biomacromolecules such as proteins177,178 and synthetic polymers such as PVA.179−181 Among them, the hydrogel formation with a commercially available biocompatible polymer, PVA, has been extensively studied. For example, PVA−TA hydrogel was prepared by a freezing-thawing process179 or self-assembly at room temperature.180 A unique example of PVA−TA hydrogel is a temperature responsive shape memory gel (Figure 5B),181 comprised of strong hydrogen bonding between PVA and TA and weak hydrogen bonding between PVAs, which contribute to the fixation of permanent shape and temporal shape, respectively. The deformed/elongated gels can recover their original/permanent shape in a temperature responsive manner after immersion in hot water, due to the rearrangement of weak hydrogen bonding. Another interesting example is the hydrogel prepared from HA-galloyl conjugates and oligo-epigallocatechin gallate featuring a shear-thinning property that is suitable for injection.182 These studies illustrated that the hydrogels with various responsive behaviors can be engineered by taking advantage of hydrogen bonding as reversible cross-links. Hydrogels Based on Metal-Phenolic Coordination. In nature, the bis- and tris-complex of catechol−FeIII coordination play an important role in the function of the hard cuticle of the byssal theads,183 inspiring the idea that the metal-phenolic complexation can be a basis for design of advanced materials. In this context, pioneering work reported a metallogel comprising four-arm-PEG-catechols and multivalent transition metal ions (i.e., FeIII, TiIV) (Figure 5C).184 The metallogel is unique because it achieves both high mechanical strength and self-healing properties. The mechanical property of the metallogels is comparable to the covalently cross-linked gels because a FeIII−catechol coordination bond is almost as strong as a covalent bond. Meanwhile, in contrast to covalent bonds, the metal−phenolic coordination is reversible, imparting selfhealing properties to the metallogels. Alternatively, dynamic boronic acid esters can also be exploited to prepare self-healing hydrogels.185 In spite of the covalent nature, the boronic acid ester is analogous to the metal−phenolic coordination due to its reversibility. Moreover, the use of boronic acid esters imparts hydrophobicity and pH-sensitivity to the hydrogels that are different from the ones prepared using metal ions and make them potentially sugar-responsive. An important parameter in metal-phenolic complexation is the type of metal ions that participate in the cross-linking process. Metal-phenolic coordination is not limited to FeIII but can be extended to other metal ions as utilized by invertebrates in nature.186 For example, the metallogels from four-arm-PEGJ


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Figure 6. Advanced strategies to engineer functional polyphenol-based gel systems. (A) Injectable and ultratough hydrogels based on chitosan− catechol interactions. (a) Schematic representation of preparation of the DC and DN hydrogels. (b) Enhanced mechanical property of the DN gels against compression, compared to SN gels. (c) Double-syringe device allows combining the polymer solution with the FeIII ions on injection. Reproduced with permission from ref 196. Copyright 2017 WILEY-VCH Verlag GmbH & Co. (B) Functional materials based on nanoparticle composites. (a) Conductive and (b) magnetic hydrogels can be prepared by loading PDA-coated carbon black nanoparticles and Fe3O4 nanoparticles, respectively. Reproduced with permission from ref 203. Copyright 2017 Lu Han, Liwei Yan, Kefeng Wang, Liming Fang, Hongping Zhang, Youhong Tang, Yonghui Ding, Lu-Tao Weng, Jielong Xu, Jie Weng, Yujie Liu, Fuzeng Ren and Xiong Lu. (C) Oxidation resistant catecholinspired ligands. (a) Chemical structure of the four-arm-PEG cross-linker with terminal catechol, 4-nitrocatechol, and HOPO. Reproduced with permission from ref 205. Copyright 2013 Royal Society of Chemistry. (b) Complete disassembly of the hydrogels was observed for PAH-HOPO based hydrogels after disruption of coordination bonds with 150 mM EDTA but not for PAH-DOPA based hydrogels. Reproduced with permission from ref 207. Copyright 2017 American Chemical Society. (D) Gels directly obtained from a natural polyphenol, TA, and TiIV. The metal-phenolic supramolecular gels feature functions as broad as (a) shape persistence, (b) adhesiveness, (c) self-healing, and (d) injectability. The gel is capable of being loaded with functional nanoparticles. (e) Graphene oxide imparts conductivity to the gels. Reproduced with permission from ref 202. Copyright 2016 Wiley VCH Verlag GmbH & Co. (E) Crystallization of active pharmaceutical ingredient (API) molecules in the metal-phenolic supramolecular gels. (a) Schematic representation of gelation of the TA-TiIV gels, followed by the crystallization of API in the gels. (b) Morphology difference of the CBZ crystals grown in solution and in the gels. (c) Grown crystals can be readily collected by disassembling the gels. Reproduced with permission from ref 212. Copyright 2018 WILEY VCH Verlag GmbH & Co.

catechol can be prepared with TiIII, AlIII, and VIII, which feature distinct mechanical properties compared to the metallogels prepared with FeIII.184,187 In a different system, the mechanical properties of PAH-catechol/metal hydrogels were also affected by a type of metal ion (i.e., AlIII, InIII, GaIII),188 reflecting the stability of complexation. These studies indicated that the mechanical property of the metallogels prepared based on metal−ligand coordination can be tuned by the pair of transition metals and ligands or by a cocktail of metals as shown in elastomers.189 The HSAB theory can be a guide for this tuning.190 A further expansion of the metal ion-phenolic coordination approach is the use of metal nanoparticles as a cross-linker instead of metal ions (Figure 5D). Inspired by mussel adhesion to solid surfaces, Fe3O4 nanoparticles were used as crosslinking motifs instead of FeIII ions. The hydrogel prepared from four-arm-PEG−catechols and Fe3O4 nanoparticles showed reversible but more solidlike mechanical properties that are strikingly different from the ones prepared with FeIII. The

distinct mechanical property can be attributed to the multiple interfacial cross-linking between four-arm-PEG-catechols and Fe3O4 nanoparticles.191 This study illustrated a strategy to tune mechanical properties of the gels in a supramolecular crosslinking approach. Hydrogels Based on Dual Cross-Linking. Mechanically robust gels find broad applications in, for example, regenerative medicine, waste treatment, and so on. The ability of phenolic groups to form different types of chemical linkages is advantageous to prepare such tough gels in a strategy of DN192,193 and DC hydrogel formation.194 In addition, the hydrogen bonding or metal coordination by phenolic groups are reversible chemical linkages that allow for the preparation of tough and self-healing hydrogels. For example, the DC hydrogel system with high extensibility (∼10 times of original size) and a fast self-healing property was obtained by copolymerization of precoordinated catechol− FeIII cross-linkers and acrylamides.195 On the other hand, the DN hydrogel with high compressive strength (∼2.46 MPa), K


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adhesiveness as well as the functionality imparted by the nanoparticles.203 Hydrogels from Polyphenol-Inspired Ligands. The development of hydrogels with stable properties will be important for applications, such as implants, that need longterm stability. The metal-phenolic coordination and adhesiveness of phenolic groups will be diminished through oxidization and further reaction of the phenolic groups. Furthermore, the covalent networks formed through oxidation of phenolic groups generally results in tanned materials at the expense of transparency. Nevertheless, the presence of oxygen is unavoidable in most practical applications. In addition, metal-phenolic coordination usually requires alkaline pH,27,184 increasing the chance of polyphenol oxidization. Therefore, synthetic phenolic ligands that are oxidationresistant and capable of forming coordination at lower pH have been investigated to overcome the problems of naturally occurring phenolic ligands. Such ligands enable the engineering of functional materials with more stable and predictable properties by eliminating uncontrolled oxidative reactions. In this context, catechol derivatives with electron withdrawing substitution such as 4-nitrocatechol, 4-chlorocatechol, 4-cyanocatechol, and HOPO have been shown to be more resistant to oxidation (Figure 6C).205,206 Among them, HOPO showed a strong coordination ability to FeIII that is comparable to the one of catechol,206 while the hydrogel from four-armPEG-HOPO and FeIII showed remarkable resistance against oxidation. HOPO-metal coordination is fully reversible (Figure 6C). Furthermore, the lowered pKa of the hydroxyl group of HOPO allows metal complexation at lower pH, which not only reduces the chance of oxidation but also allows for formation of hydrogels at physiological pH. This is particularly advantageous for injectable drug delivery applications. Nevertheless, the lack of oxidative coupling may hinder the mechanical properties. In this context, tough and oxidation resistant DC gels were prepared using HOPO-PAH and TA, where metal-HOPO coordination works as noncovalent crosslinks and oxidative coupling of TA works as covalent crosslinks. The mechanical stiffness can be modulated solely by TA without sacrificing the self-healing property from the metalHOPO coordination. The hydrogels were formed by use of either FeIII or AlIII as a metal ion. In addition, the conjugation of the HOPO moiety onto PAH lowered the pKa of HOPO by a full pH unit, allowing more efficient hydrogelation at moderate pH. The HOPO-PAH/TA hydrogel showed high stiffness and self-healing properties as well as improved oxidation resitance.207 Hydrogels from Natural Sources. Although chemical conjugation is a relatively straightforward reaction, it is still time and energy consuming. Direct synthesis of functional materials from naturally available polyphenols are attractive, as it is simple, rapid, and low cost. In this context, a naturally available plant-sourced TA has been extensively used to prepare hydrogel materials. A few of the successful examples are TA/DNA hydrogels, TA/PVA hydrogels, and TA-PVA/ BSA hydrogels, which were already described in the previous sections.178−181 In contrast, it is difficult to obtain metallogels via metal-phenolic coordination from naturally available components, and thus the metallogels were typically prepared using synthetic components.184,208,209 Ternary gel systems represent a realistic solution for the preparation of metallogels from TA. The affinity of TA via ionic interactions, hydrogen bonding, and covalent bond

cell compatibility, adhesiveness, and injectability was obtained from chitosan-DOPA conjugates and FeIII (Figure 6A).196 The covalent linkage was formed between the amino groups of chitosan with the use of a cross-linker (i.e., genipin), while the noncovalent linkage was through metal-catechol coordination. The rapid gelation (∼8 s) via fast metal-phenolic coordination allows development of injectable formulation as shown in Figure 6A. The TA treatment of preformed hydrogels or aerogels is a robust strategy to prepare tough gels using a DC gel concept. An aerogel of PVA or PAAm was immersed in TA solution, resulting in the formation of hydrogen bonding between TA and the polymers. The obtained DC hydrogel showed high toughness, resistance to swelling, self-healing property, and adhesiveness.197 This is a generalizable transformation of a hydrogel into a mechanically strong DC gel. Similarly, the TAPVA/BSA hydrogel with ultrahigh tensile strength of ∼9.5 MPa was prepared by immersion of preformed PVA/BSA gels in the TA solution.178 Of note, the cross-linking by TA occurs more efficiently at the surface of the parent PVA/BSA gels, giving a hydrogel with the dense structure at the surface that prevent water inside hydrogel from evaporation. The hydrogel with a good water retention ability will be advantageous for practical applications, such as artificial skins. Composite Hydrogels. The mechanical properties of phenolic hydrogels can be enhanced by the addition of metal particles in the structure. For example, a composite hydrogel was prepared from a synthetic nanosilicate (i.e., laponite), acrylamide, and DMA via polymerization.198 The composite hydrogel is capable of being repeatedly deformed 10 times, while showing a compressive stress of over 1.1 MPa. Of note, the enhancement of the mechanical property was higher for the hydrogel containing DMA than the control hydrogel without DMA (i.e., PAAm hydrogel), suggesting that the fine-tuning of interfacial affinity between nanoparticles and phenolic components are important for enhancing the mechanical property of the composite hydrogels. Similarly, laponites were incorporated into the four-arm-PEG-catechol hydrogel systems, resulting in the reduction of curing time and enhancement of mechanical and adhesive properties.199 Composite hydrogels with nanomaterials also find importance in the development of functional hydrogels that have metal nanoparticle-derived functionalities (e.g., antibacterial, conductive, and magnetic).200−203 Among them, conductive hydrogels may find applications for bioelectronics and wearable devices. The phenolic hydrogels are quite advantageous as they are sticky and can be conductive by incorporating conductive nanomaterials, such as graphene, carbon nanotubes, and polypyrrole nanospheres.201−204 For example, paintable hydrogels containing dopamine and polypyrrole nanospheres were obtained, which showed conductivity as high as normal myocardium and stable adhesion to beating myocardial tissues over 4 weeks.204 Meanwhile, polyphenol chemistry also provides a powerful strategy for loading nanomaterials into hydrogels by improving dispersion via surface coating, as described in previous sections.201,203 For example, magnetic Fe3O4 nanoparticles and carbon black nanoparticles were successfully loaded into a polydopamine-PAAm hydrogel after coating by dopamine, resulting in magnetic and conductive hydrogels, respectively (Figure 6B). The composite gels showed high extensibility, toughness, self-healing property, cell affinity, and tissue L


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basic research that can be done on phenolics. Therefore, it is our belief that the study and utilization of phenolics in academia and industry will only continue to grow, and we envision this review as a short outline highlighting various phenolic materials and building blocks and their importance to biomedicine.

formation via Michael addition and Schiff base reactions allows phenolic modification of polymers just by mixing with TA in an aqueous solution. The multivalent transition metal species (e.g., FeIII) can then be added for cross-linking to the precursor solution, leading to metallogel formation. For example, a TA/ PAH/FeIII ternary metallogel was reported,210 although the binary mixture of TA/FeIII failed to form metallogels. The systematic study further demonstrated the versatility of this approach that are irrespective of polymer charges, which successfully obtained metallogels from PEG, PVPON, PDDA, and PSS.211 Recently, supramolecular phenolic metallogels were assembled solely from natural components, namely, TA and group IV transition metal species (i.e., TiIV, ZrIV) (Figure 6D), expanding the chemistry of MPN formation from thin films to bulk materials.202 The obtained metallogels showed a range of functionalities as broad as tunable gelation time, injectability, adhesiveness, metal ion capturing, and in situ crystallization of MOFs and pharmaceuticals. Of note, the in situ crystallization of pharmaceuticals enabled a control over size, morphology, and polymorphism of drug crystals (Figure 6E), which directly affects solubility and therefore efficacy of drug formulation.212 The metal-phenolic gels provide a platform to produce drug powders with desired crystal structures and can be also used as a sustained drug delivery system, because they are inexpensive, abundant, and low toxic materials.

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. ORCID

Junling Guo: 0000-0002-2948-880X Hirotaka Ejima: 0000-0002-4965-9493 Present Address ⊥

J.J.R.: Department of Chemical Engineering, The University of Melbourne, Parkville, Victoria 3010, Australia. Author Contributions

The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. Funding

J.G. is grateful for the Fellowships from National Youth Talents Program at Sichuan University and Wyss Institute at Harvard University. J.J.R. acknowledges Japan Society for the Promotion of Science (JSPS) for the postdoctoral fellowships for research in Japan (Short-term, Grant PE17019). H.E. acknowledges JSPS for the Grants-in-Aid for Scientific Research (Grants JP18K14000 and JP18K18802) and the Ministry of Education, Culture, Sports, Science and Technology (MEXT) for the Leading Initiative for Excellent Young Researchers (LEADER).

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OUTLOOK This review has highlighted that polyphenols are useful building blocks to assemble functional nanoparticles, films, and gels through the easy, cost-effective, and ecofriendly synthesis of materials with limited use of toxic chemicals. Currently, more attention has been devoted to the development of functional particles, while hybrid assemblies and films could emerge as new directions for the further development of polyphenol-based biomaterials. For example, polyphenol-based biohybrids could potentially biosynthesize more challenging biomolecules and drug molecules. Polyphenol films can be further explored for the coating of a wide range of implant devices and tissues. Materials constructed from synthetic polymers are from limited resources and typically not degradable, giving rise to severe environmental problems including marine pollution by microplastics.213,214 Microplastics are the most prevalent type of marine debris and ingested by diverse marine organisms. They can enter human food chains and thus have become a global environmental concern. This is a multidimensional issue and cannot be solved in a simple way, but this kind of global environmental concern drives materials scientists to engineer functional materials from highly abundant natural resources to realize a sustainable society.215 We expect that phenolic-based materials could be a better platform for engineering solutions to these social problems. Moreover, as many of the materials discussed herein utilize metal ions that theoretically could be recycled and reused, phenolic-based materials represent a unique class of potentially green and sustainable nanomaterials. Beyond the environmental implications, the natural abundance of phenolics in living organisms suggests that phenolics will increasingly be used in actual biomedical applications, ranging from wound healing to drug delivery to imaging, as discussed above. Although many mechanisms surrounding the formation and disassembly of phenolic materials still remain undefined or controversial, there is also an abundance of theoretical and

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank Gao Xiao and Yana Klyachina for helpful discussion. ABBREVIATIONS AFM, atomic force microscopy; API, active pharmaceutical ingredient; ARGET ATRP, activators regenerated by electron transfer atom transfer radical polymerization; ATP, adenosine triphosphate; BPN, boronate−phenolic network; BSA, bovine serum albumin; CBZ, carbamazepine; CT, computed tomography; DC, double cross-linked; DMA, dopamine methacrylate; DN, double network; DOPA, 3,4-dihydroxyphenyl-Lalanine; DOX, doxorubicin; DEX, dexamethasone; EGCG, epigallocatechin-3-gallate; FRET, fluorescence resonance energy transfer; GA, gallic acid; GRAS, generally recognized as safe; HA, hyaluronic acid; hADSCs, human adipose-derived stem cells; HSAB, hard and soft acids and bases; HOPO, 3hydroxy-4-pyridinone; ICG, indocyanine green; LbL, layer-bylayer; MOF, metal−organic framework; MPN, metal−phenolic network; MRI, magnetic resonance imaging; MSN, mesoporous silica nanoparticle; NADPH, nicotinamide adenine dinucleotide phosphate; NIR, near-infrared; PAA, poly(acrylic acid); PAAm, polyacrylamide; PAH, poly(allylamine hydrochloride); PDA, polydopamine; PDDA, poly(dimethyldiallylammonium chloride); PEG, poly(ethylene glycol); PEI, polyethylenimine; PET, positron emission tomography; PG, pyrogallol; PNIPAM, poly(N-isopropylacryM


Review


(22) Spencer, C. M.; Cai, Y.; Martin, R.; Gaffney, S. H.; Goulding, P. N.; Magnolato, D.; Lilley, T. H.; Haslam, E. Polyphenol ComplexationSome Thoughts and Observations. Phytochemistry 1988, 27 (8), 2397−2409. (23) Baxter, N. J.; Lilley, T. H.; Haslam, E.; Williamson, M. P. Multiple Interactions between Polyphenols and a Salivary ProlineRich Protein Repeat Result in Complexation and Precipitation. Biochemistry 1997, 36 (18), 5566−5577. (24) McManus, J. P.; Davis, K. G.; Beart, J. E.; Gaffney, S. H.; Lilley, T. H.; Haslam, E. Polyphenol Interactions. Part 1. Introduction; Some Observations on the Reversible Complexation of Polyphenols with Proteins and Polysaccharides. J. Chem. Soc., Perkin Trans. 2 1985, 9, 1429−1438. (25) Fang, M. Z.; Wang, Y.; Ai, N.; Hou, Z.; Sun, Y.; Lu, H.; Welsh, W.; Yang, C. S. Tea Polyphenol (−)-Epigallocatechin-3-Gallate Inhibits DNA Methyltransferase and Reactivates MethylationSilenced Genes in Cancer Cell Lines. Cancer Res. 2003, 63 (22), 7563−7570. (26) Labieniec, M.; Gabryelak, T. Interactions of Tannic Acid and Its Derivatives (Ellagic and Gallic Acid) with Calf Thymus DNA and Bovine Serum Albumin Using Spectroscopic Method. J. Photochem. Photobiol., B 2006, 82 (1), 72−78. (27) Ejima, H.; Richardson, J. J.; Liang, K.; Best, J. P.; Van Koeverden, M. P.; Such, G. K.; Cui, J.; Caruso, F. One-Step Assembly of Coordination Complexes for Versatile Film and Particle Engineering. Science 2013, 341, 154−157. (28) Guo, J.; Ping, Y.; Ejima, H.; Alt, K.; Meissner, M.; Richardson, J. J.; Yan, Y.; Peter, K.; Von Elverfeldt, D.; Hagemeyer, C. E.; Caruso, F. Engineering Multifunctional Capsules through the Assembly of Metal-Phenolic Networks. Angew. Chem., Int. Ed. 2014, 53, 5546− 5551. (29) Ping, Y.; Guo, J.; Ejima, H.; Chen, X.; Richardson, J. J.; Sun, H.; Caruso, F. PH-Responsive Capsules Engineered from Metal-Phenolic Networks for Anticancer Drug Delivery. Small 2015, 11 (17), 2032− 2036. (30) Park, C.; Yang, B. J.; Jeong, K. B.; Kim, C. B.; Lee, S.; Ku, B. Signal-Induced Release of Guests from a Photolatent Metal−Phenolic Supramolecular Cage and Its Hybrid Assemblies. Angew. Chem., Int. Ed. 2017, 56 (20), 5485−5489. (31) Wang, X.; Li, X.; Liang, X.; Liang, J.; Zhang, C.; Yang, J.; Wang, C.; Kong, D.; Sun, H. ROS-Responsive Capsules Engineered from Green Tea Polyphenol−Metal Networks for Anticancer Drug Delivery. J. Mater. Chem. B 2018, 6 (7), 1000−1010. (32) Shen, G.; Xing, R.; Zhang, N.; Chen, C.; Ma, G.; Yan, X. Interfacial Cohesion and Assembly of Bioadhesive Molecules for Design of Long-Term Stable Hydrophobic Nanodrugs toward Effective Anticancer Therapy. ACS Nano 2016, 10 (6), 5720−5729. (33) Guo, J.; Sun, H.; Alt, K.; Tardy, B. L.; Richardson, J. J.; Suma, T.; Ejima, H.; Cui, J.; Hagemeyer, C. E.; Caruso, F. BoronatePhenolic Network Capsules with Dual Response to Acidic PH and Cis-Diols. Adv. Healthcare Mater. 2015, 4 (12), 1796−1801. (34) Chen, Y.; Wang, J.; Liu, J.; Lu, L. Metal-Phenolic Encapsulated Mesoporous Silica Nanoparticles for PH-Responsive Drug Delivery and Magnetic Resonance Imaging. Z. Phys. Chem. 2018, 232 (9−11), 1733−1740. (35) Tang, L.; Shi, J.; Wang, X.; Zhang, S.; Wu, H.; Sun, H.; Jiang, Z. Coordination Polymer Nanocapsules Prepared Using Metal−Organic Framework Templates for PH-Responsive Drug Delivery. Nanotechnology 2017, 28 (27), 275601. (36) Bartzoka, E. D.; Lange, H.; Poce, G.; Crestini, C. Stimuli Responsive Tannin-Fe(III) Hybrid Microcapsules as Demonstrated by the Active Release of an Anti-Tuberculosos Agent. ChemSusChem 2018, 11 (22), 3975−3991. (37) Kim, S.; Philippot, S.; Fontanay, S.; Duval, R. E.; Lamouroux, E.; Canilho, N.; Pasc, A. PH-and Glutathione-Responsive Release of Curcumin from Mesoporous Silica Nanoparticles Coated Using Tannic Acid−Fe(III) Complex. RSC Adv. 2015, 5 (110), 90550− 90558.

lamide); PS, polystyrene; PSS, poly(sodium 4-styrenesulfonate); PVA, poly(vinyl alcohol); PVPON, poly(N-vinylpyrrolidone); PTX, paclitaxel; ROS, reactive oxygen species; SEM, scanning electron microscopy; TA, tannic acid; TEM, transmission electron microscopy; TTA, 2-thenoyltrifluoroacetone; ZIF-8, zeolitic imidazolate framework-8

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REFERENCES

(1) Bentley, W. E.; Payne, G. F. Nature’s Other Self-Assemblers. Science 2013, 341 (6142), 136−137. (2) Haslam, E. Plant Polyphenols: Vegetable Tannins Revisited; Cambridge University Press, 1989. (3) Quideau, S.; Deffieux, D.; Douat-Casassus, C.; Pouysegu, L. Plant Polyphenols: Chemical Properties, Biological Activities, and Synthesis. Angew. Chem., Int. Ed. 2011, 50 (3), 586−621. (4) Haslam, E. Polyphenol−Protein Interactions. Biochem. J. 1974, 139 (1), 285−288. (5) Haslam, E. Chemistry of Vegetable Tannins; Academic Press: London, 1966. (6) Singh, M.; Arseneault, M.; Sanderson, T.; Murthy, V.; Ramassamy, C. Challenges for Research on Polyphenols from Foods in Alzheimer’s Disease: Bioavailability, Metabolism, and Cellular and Molecular Mechanisms. J. Agric. Food Chem. 2008, 56 (13), 4855−4873. (7) Spanos, G. A.; Wrolstad, R. E. Phenolics of Apple, Pear, and White Grape Juices and Their Changes with Processing and Storage. A Review. J. Agric. Food Chem. 1992, 40 (9), 1478−1487. (8) Wei, Q.; Haag, R. Universal Polymer Coatings and Their Representative Biomedical Applications. Mater. Horiz. 2015, 2 (6), 567−577. (9) Guo, J.; Huang, X.; Wu, C.; Liao, X.; Shi, B. The Further Investigation of Tanning Machanisms of Typica Tannages by Ultraviolet-Visible and Near Infrared Diffused Reflectance Spectrophotometry. J. Am. Leather Chem. Assoc. 2011, 106 (7), 226−231. (10) Clemens, S. Molecular Mechanisms of Plant Metal Tolerance and Homeostasis. Planta 2001, 212 (4), 475−486. (11) Daayf, F.; Lattanzio, V. Recent Advances in Polyphenol Research; John Wiley & Sons, 2009. (12) Graham, H. N. Green Tea Composition, Consumption, and Polyphenol Chemistry. Prev. Med. 1992, 21 (3), 334−350. (13) Perron, N. R.; Brumaghim, J. L. A Review of the Antioxidant Mechanisms of Polyphenol Compounds Related to Iron Binding. Cell Biochem. Biophys. 2009, 53 (2), 75−100. (14) Hider, R. C.; Howlin, B.; Miller, J. R.; Mohd-Nor, A. R.; Silver, J. Model Compounds for Microbial Iron-Transport Compounds. Part IV. Further Solution Chemistry and Mössbauer Studies on Iron (II) and Iron (III) Catechol Complexes. Inorg. Chim. Acta 1983, 80, 51− 56. (15) Tanaka, T.; Matsuo, Y.; Kouno, I. Chemistry of Secondary Polyphenols Produced during Processing of Tea and Selected Foods. Int. J. Mol. Sci. 2010, 11 (1), 14−40. (16) Botha, J. J.; Viviers, P. M.; Ferreira, D.; Roux, D. G. Condensed Tannins: Competing Nucleophilic Centres in Biomimetic Condensation Reactions. Phytochemistry 1982, 21 (6), 1289−1294. (17) Ruderman, I. W. Bromination of Phenols and Phenol Alcohols. Ind. Eng. Chem., Anal. Ed. 1946, 18 (12), 753−759. (18) Luo, W.; Xiao, G.; Tian, F.; Richardson, J. J.; Wang, Y.; Zhou, J.; Guo, J.; Liao, X.; Shi, B. Engineering Robust Metal−Phenolic Network Membranes for Uranium Extraction from Seawater. Energy Environ. Sci. 2019, 12 (2), 607−614. (19) He, Q.; Yao, K.; Sun, D.; Shi, B. Biodegradability of TanninContaining Wastewater from Leather Industry. Biodegradation 2007, 18 (4), 465−472. (20) Bate-Smith, E. C. Haemanalysis of Tannins: The Concept of Relative Astringency. Phytochemistry 1973, 12 (4), 907−912. (21) Bennett, R. N.; Wallsgrove, R. M. Secondary Metabolites in Plant Defence Mechanisms. New Phytol. 1994, 127 (4), 617−633. N


Review

ACS Biomaterials Science & Engineering (38) Yao, X.; Zheng, X.; Zhang, J.; Cai, K. Oxidation-Induced Surface Deposition of Tannic Acid: Towards Molecular Gates on Porous Nanocarriers for Acid-Responsive Drug Delivery. RSC Adv. 2016, 6 (80), 76473−76481. (39) Xiong, L.; Bi, J.; Tang, Y.; Qiao, S. Magnetic Core−Shell Silica Nanoparticles with Large Radial Mesopores for SiRNA Delivery. Small 2016, 12 (34), 4735−4742. (40) Guo, J.; Tardy, B. L.; Christofferson, A. J.; Dai, Y.; Richardson, J. J.; Zhu, W.; Hu, M.; Ju, Y.; Cui, J.; Dagastine, R. R. Modular Assembly of Superstructures from Polyphenol-Functionalized Building Blocks. Nat. Nanotechnol. 2016, 11 (12), 1105−1111. (41) Huang, H.; Li, P.; Liu, C.; Ma, H.; Huang, H.; Lin, Y.; Wang, C.; Yang, Y. PH-Responsive Nanodrug Encapsulated by Tannic Acid Complex for Controlled Drug Delivery. RSC Adv. 2017, 7 (5), 2829− 2835. (42) Han, K.; Zhang, W.; Zhang, J.; Ma, Z.; Han, H. pH-Responsive Nanoscale Coordination Polymer for Efficient Drug Delivery and Real-Time Release Monitoring. Adv. Healthcare Mater. 2017, 6 (19), 1700470. (43) Yuan, C.; Chen, J.; Yu, S.; Chang, Y.; Mao, J.; Xu, Y.; Luo, W.; Zeng, B.; Dai, L. Protein-Responsive Assemblies from Catechol-Metal Ion Supramolecular Coordination. Soft Matter 2015, 11 (11), 2243− 2250. (44) Dai, Y.; Guo, J.; Wang, T.-Y.; Ju, Y.; Mitchell, A. J.; Bonnard, T.; Cui, J.; Richardson, J. J.; Hagemeyer, C. E.; Alt, K.; Caruso, F. SelfAssembled Nanoparticles from Phenolic Derivatives for Cancer Therapy. Adv. Healthcare Mater. 2017, 6 (16), 1700467. (45) Dai, Y.; Yang, Z.; Cheng, S.; Wang, Z.; Zhang, R.; Zhu, G.; Wang, Z.; Yung, B. C.; Tian, R.; Jacobson, O.; Xu, C.; Ni, Q.; Song, J.; Sun, X.; Niu, G.; Chen, X. Toxic Reactive Oxygen Species Enhanced Synergistic Combination Therapy by Self-Assembled Metal-Phenolic Network Nanoparticles. Adv. Mater. 2018, 30 (8), 1704877. (46) Dai, Y.; Cheng, S.; Wang, Z.; Zhang, R.; Yang, Z.; Wang, J.; Yung, B. C.; Wang, Z.; Jacobson, O.; Xu, C.; Ni, Q.; Yu, G.; Zhou, Z.; Chen, X. Hypochlorous Acid Promoted Platinum Drug Chemotherapy by Myeloperoxidase-Encapsulated Therapeutic Metal Phenolic Nanoparticles. ACS Nano 2018, 12 (1), 455−463. (47) Wang, X.; Yan, J.-J.; Wang, L.; Pan, D.; Yang, R.; Xu, Y.; Sheng, J.; Huang, Q.; Zhao, H.; Yang, M. Rational Design of PolyphenolPoloxamer Nanovesicles for Targeting Inflammatory Bowel Disease Therapy. Chem. Mater. 2018, 30 (12), 4073−4080. (48) Shin, M.; Lee, H.-A.; Lee, M.; Shin, Y.; Song, J.-J.; Kang, S.-W.; Nam, D.-H.; Jeon, E. J.; Cho, M.; Do, M.; Park, S.; Lee, M. S.; Jang, J. H.; Cho, S. W.; Kim, K. S.; Lee, H. Targeting Protein and Peptide Therapeutics to the Heart via Tannic Acid Modification. Nat. Biomed. Eng. 2018, 2 (5), 304−317. (49) Li, K.; Xiao, G.; Richardson, J. J.; Tardy, B. L.; Ejima, H.; Huang, W.; Guo, J.; Liao, X.; Shi, B. Targeted Therapy against Metastatic Melanoma Based on Self-Assembled Metal-Phenolic Nanocomplexes Comprised of Green Tea Catechin. Adv. Sci. 2019, 6, 1801688. (50) Li, K.; Dai, Y.; Chen, W.; Yu, K.; Xiao, G.; Richardson, J. J.; Huang, W.; Guo, J.; Liao, X.; Shi, B. Self-Assembled Metal-Phenolic Nanoparticles for Enhanced Synergistic Combination Therapy against Colon Cancer. Adv. Biosyst. 2019, 3, 1800241. (51) Tsai, L.-C.; Hsieh, H.-Y.; Lu, K.-Y.; Wang, S.-Y.; Mi, F.-L. EGCG/Gelatin-Doxorubicin Gold Nanoparticles Enhance Therapeutic Efficacy of Doxorubicin for Prostate Cancer Treatment. Nanomedicine 2016, 11 (1), 9−30. (52) Liang, H.; Zhou, B.; Li, J.; Liu, X.; Deng, Z.; Li, B. Engineering Multifunctional Coatings on Nanoparticles Based on Oxidative Coupling Assembly of Polyphenols for Stimuli-Responsive Drug Delivery. J. Agric. Food Chem. 2018, 66 (26), 6897−6905. (53) Fan, J.; Zheng, D.; Mei, W.; Chen, S.; Chen, S.; Cheng, S.; Zhang, X. A Metal−Polyphenol Network Coated Nanotheranostic System for Metastatic Tumor Treatments. Small 2017, 13 (48), 1702714.

(54) Kumar, S.; Michael, I. J.; Park, J.; Granick, S.; Cho, Y. Cloaked Exosomes: Biocompatible, Durable, and Degradable Encapsulation. Small 2018, 14 (34), 1802052. (55) Ju, Y.; Cui, J.; Sun, H.; Müllner, M.; Dai, Y.; Guo, J.; BertleffZieschang, N.; Suma, T.; Richardson, J. J.; Caruso, F. Engineered Metal-Phenolic Capsules Show Tunable Targeted Delivery to Cancer Cells. Biomacromolecules 2016, 17 (6), 2268−2276. (56) Ju, Y.; Dai, Q.; Cui, J.; Dai, Y.; Suma, T.; Richardson, J. J.; Caruso, F. Improving Targeting of Metal−Phenolic Capsules by the Presence of Protein Coronas. ACS Appl. Mater. Interfaces 2016, 8 (35), 22914−22922. (57) Besford, Q. A.; Ju, Y.; Wang, T.-Y.; Yun, G.; Cherepanov, P.; Hagemeyer, C. E.; Cavalieri, F.; Caruso, F. Self-Assembled MetalPhenolic Networks on Emulsions as Low-Fouling and PH-Responsive Particles. Small 2018, 14 (39), 1802342. (58) Liang, H.; Zhou, B.; Li, J.; Xu, W.; Liu, S.; Li, Y.; Chen, Y.; Li, B. Supramolecular Design of Coordination Bonding Architecture on Zein Nanoparticles for PH-Responsive Anticancer Drug Delivery. Colloids Surf., B 2015, 136, 1224−1233. (59) Liang, H.; Pei, Y.; Li, J.; Xiong, W.; He, Y.; Liu, S.; Li, Y.; Li, B. PH-Degradable Antioxidant Nanoparticles Based on HydrogenBonded Tannic Acid Assembly. RSC Adv. 2016, 6 (37), 31374− 31385. (60) Zeng, Z.; Wen, M.; Ye, G.; Huo, X.; Wu, F.; Wang, Z.; Yan, J.; Matyjaszewski, K.; Lu, Y.; Chen, J. Controlled Architecture of Hybrid Polymer Nanocapsules with Tunable Morphologies by Manipulating Surface-Initiated ARGET ATRP from Hydrothermally Modified Polydopamine. Chem. Mater. 2017, 29 (23), 10212−10219. (61) Alexander, J. F.; Kozlovskaya, V.; Chen, J.; Kuncewicz, T.; Kharlampieva, E.; Godin, B. Cubical Shape Enhances the Interaction of Layer-by-Layer Polymeric Particles with Breast Cancer Cells. Adv. Healthcare Mater. 2015, 4 (17), 2657−2666. (62) Liu, F.; Kozlovskaya, V.; Zavgorodnya, O.; Martinez-Lopez, C.; Catledge, S.; Kharlampieva, E. Encapsulation of Anticancer Drug by Hydrogen-Bonded Multilayers of Tannic Acid. Soft Matter 2014, 10 (46), 9237−9247. (63) Li, H.; Jia, Y.; Feng, X.; Li, J. Facile Fabrication of Robust Polydopamine Microcapsules for Insulin Delivery. J. Colloid Interface Sci. 2017, 487, 12−19. (64) Sun, J.; Su, C.; Zhang, X.; Li, J.; Zhang, W.-B.; Zhao, N.; Xu, J.; Yang, S. Responsive Complex Capsules Prepared with Polymerization of Dopamine, Hydrogen-Bonding Assembly, and Catechol Dismutation. J. Colloid Interface Sci. 2018, 513, 470−479. (65) Zhu, W.; Liang, S.; Wang, J.; Yang, Z.; Zhang, L.; Yuan, T.; Xu, Z.; Xu, H.; Li, P. Europium-Phenolic Network Coated BaGdF 5 Nanocomposites for Tri-Modal Computed Tomography/Magnetic Resonance/Luminescence Imaging. J. Mater. Sci.: Mater. Med. 2017, 28 (5), 74. (66) Liu, T.; Zhang, M.; Liu, W.; Zeng, X.; Song, X.; Yang, X.; Zhang, X.; Feng, J. Metal Ion/Tannic Acid Assembly as a Versatile Photothermal Platform in Engineering Multimodal Nanotheranostics for Advanced Applications. ACS Nano 2018, 12 (4), 3917−3927. (67) Guo, J.; Wang, X.; Henstridge, D. C.; Richardson, J. J.; Cui, J.; Sharma, A.; Febbraio, M. A.; Peter, K.; de Haan, J. B.; Hagemeyer, C. E. Nanoporous Metal−Phenolic Particles as Ultrasound Imaging Probes for Hydrogen Peroxide. Adv. Healthcare Mater. 2015, 4 (14), 2170−2175. (68) Xu, C.; Wang, Y.; Yu, H.; Tian, H.; Chen, X. Multifunctional Theranostic Nanoparticles Derived from Fruit-Extracted Anthocyanins with Dynamic Disassembly and Elimination Abilities. ACS Nano 2018, 12 (8), 8255−8265. (69) Alford, A.; Kozlovskaya, V.; Xue, B.; Gupta, N.; Higgins, W.; Pham-Hua, D.; He, L.; Urban, V. S.; Tse, H. M.; Kharlampieva, E. Manganoporphyrin-Polyphenol Multilayer Capsules as Radical and Reactive Oxygen Species (ROS) Scavengers. Chem. Mater. 2018, 30 (2), 344−357. (70) Liu, F.; He, X.; Chen, H.; Zhang, J.; Zhang, H.; Wang, Z. Gram-Scale Synthesis of Coordination Polymer Nanodots with Renal O


Review

ACS Biomaterials Science & Engineering Clearance Properties for Cancer Theranostic Applications. Nat. Commun. 2015, 6, 8003. (71) Song, X.; Li, S.; Dai, J.; Song, L.; Huang, G.; Lin, R.; Li, J.; Liu, G.; Yang, H. Polyphenol-Inspired Facile Construction of Smart Assemblies for ATP- and pH-Responsive Tumor MR/Optical Imaging and Photothermal Therapy. Small 2017, 13 (20), 1603997. (72) Narayanan, S.; Sathy, B. N.; Mony, U.; Koyakutty, M.; Nair, S. V.; Menon, D. Biocompatible Magnetite/Gold Nanohybrid Contrast Agents via Green Chemistry for MRI and CT Bioimaging. ACS Appl. Mater. Interfaces 2012, 4 (1), 251−260. (73) Bray, K.; Previdi, R.; Gibson, B. C.; Shimoni, O.; Aharonovich, I. Enhanced Photoluminescence from Single Nitrogen-Vacancy Defects in Nanodiamonds Coated with Phenol-Ionic Complexes. Nanoscale 2015, 7 (11), 4869−4874. (74) Li, W.; Bing, W.; Huang, S.; Ren, J.; Qu, X. Mussel Byssus-Like Reversible Metal-Chelated Supramolecular Complex Used for Dynamic Cellular Surface Engineering and Imaging. Adv. Funct. Mater. 2015, 25 (24), 3775−3784. (75) Kozlovskaya, V.; Xue, B.; Lei, W.; Padgett, L. E.; Tse, H. M.; Kharlampieva, E. Hydrogen-Bonded Multilayers of Tannic Acid as Mediators of T-Cell Immunity. Adv. Healthcare Mater. 2015, 4 (5), 686−694. (76) Park, J. H.; Kim, K.; Lee, J.; Choi, J. Y.; Hong, D.; Yang, S. H.; Caruso, F.; Lee, Y.; Choi, I. S. A Cytoprotective and Degradable Metal−Polyphenol Nanoshell for Single-Cell Encapsulation. Angew. Chem. 2014, 126 (46), 12628−12633. (77) Su, D.; Liu, X.; Wang, L.; Ma, C.; Xie, H.; Zhang, H.; Meng, X.; Huang, Y.; Huang, X. Bio-Inspired Engineering Proteinosomes with a Cell-Wall-like Protective Shell by Self-Assembly of a Metal-Chelated Complex. Chem. Commun. 2016, 52 (95), 13803−13806. (78) Kim, B. J.; Han, S.; Lee, K.; Choi, I. S. Biphasic Supramolecular Self-Assembly of Ferric Ions and Tannic Acid across Interfaces for Nanofilm Formation. Adv. Mater. 2017, 29 (28), 1700784. (79) Pham-Hua, D.; Padgett, L. E.; Xue, B.; Anderson, B.; Zeiger, M.; Barra, J. M.; Bethea, M.; Hunter, C. S.; Kozlovskaya, V.; Kharlampieva, E. Islet Encapsulation with Polyphenol Coatings Decreases Pro-Inflammatory Chemokine Synthesis and T Cell Trafficking. Biomaterials 2017, 128, 19−32. (80) Debnath, K.; Shekhar, S.; Kumar, V.; Jana, N. R.; Jana, N. R. Efficient Inhibition of Protein Aggregation, Disintegration of Aggregates, and Lowering of Cytotoxicity by Green Tea Polyphenol-Based Self-Assembled Polymer Nanoparticles. ACS Appl. Mater. Interfaces 2016, 8 (31), 20309−20318. (81) Fei, J.; Zhao, J.; Du, C.; Wang, A.; Zhang, H.; Dai, L.; Li, J. One-Pot Ultrafast Self-Assembly of Autofluorescent PolyphenolBased Core@ Shell Nanostructures and Their Selective Antibacterial Applications. ACS Nano 2014, 8, 8529−8536. (82) Guo, J.; Suástegui, M.; Sakimoto, K. K.; Moody, V. M.; Xiao, G.; Nocera, D. G.; Joshi, N. S. Light-Driven Fine Chemical Production in Yeast Biohybrids. Science 2018, 362 (6416), 813−816. (83) Richardson, J. J.; Björnmalm, M.; Caruso, F. TechnologyDriven Layer-by-Layer Assembly of Nanofilms. Science 2015, 348 (6233), No. aaa2491. (84) Richardson, J. J.; Cui, J.; Björnmalm, M.; Braunger, J. A.; Ejima, H.; Caruso, F. Innovation in Layer-by-Layer Assembly. Chem. Rev. 2016, 116 (23), 14828−14867. (85) Ariga, K.; Hill, J. P.; Ji, Q. Layer-by-Layer Assembly as a Versatile Bottom-up Nanofabrication Technique for Exploratory Research and Realistic Application. Phys. Chem. Chem. Phys. 2007, 9 (19), 2319−2340. (86) Ariga, K.; Yamauchi, Y.; Rydzek, G.; Ji, Q.; Yonamine, Y.; Wu, K. C.-W.; Hill, J. P. Layer-by-Layer Nanoarchitectonics: Invention, Innovation, and Evolution. Chem. Lett. 2014, 43 (1), 36−68. (87) Lee, H.; Dellatore, S. M.; Miller, W. M.; Messersmith, P. B. Mussel-Inspired Surface Chemistry for Multifunctional Coatings. Science 2007, 318, 426−430. (88) Rahim, M. A.; Kristufek, S. L.; Pan, S.; Richardson, J. J.; Caruso, F. Phenolic Building Blocks for the Assembly of Functional Materials. Angew. Chem., Int. Ed. 2019, 58 (7), 1904−1927.

(89) Shutava, T.; Prouty, M.; Kommireddy, D.; Lvov, Y. PH Responsive Decomposable Layer-by-Layer Nanofilms and Capsules on the Basis of Tannic Acid. Macromolecules 2005, 38 (7), 2850− 2858. (90) Rahim, M. A.; Ejima, H.; Cho, K. L.; Kempe, K.; Müllner, M.; Best, J. P.; Caruso, F. Coordination-Driven Multistep Assembly of Metal-Polyphenol Films and Capsules. Chem. Mater. 2014, 26 (4), 1645−1653. (91) Takemoto, Y.; Ajiro, H.; Akashi, M. Hydrogen-Bonded Multilayer Films Based on Poly (N-Vinylamide) Derivatives and Tannic Acid. Langmuir 2015, 31 (24), 6863−6869. (92) Kim, S.; Kim, D. S.; Kang, S. M. Reversible Layer-by-Layer Deposition on Solid Substrates Inspired by Mussel Byssus Cuticle. Chem. - Asian J. 2014, 9 (1), 63−66. (93) Lee, B. P.; Messersmith, P. B.; Israelachvili, J. N.; Waite, J. H. Mussel-Inspired Adhesives and Coatings. Annu. Rev. Mater. Res. 2011, 41, 99−132. (94) Ejima, H.; Richardson, J. J.; Caruso, F. Phenolic Film Engineering for Template-Mediated Microcapsule Preparation. Polym. J. 2014, 46 (8), 452−459. (95) Ejima, H.; Richardson, J. J.; Caruso, F. Metal-Phenolic Networks as a Versatile Platform to Engineer Nanomaterials and Biointerfaces. Nano Today 2017, 12, 136−148. (96) Bertleff-Zieschang, N.; Rahim, M. A.; Ju, Y.; Braunger, J. A.; Suma, T.; Dai, Y.; Pan, S.; Cavalieri, F.; Caruso, F. Biofunctional Metal−Phenolic Films from Dietary Flavonoids. Chem. Commun. 2017, 53 (6), 1068−1071. (97) Rahim, M. A.; Björnmalm, M.; Bertleff-Zieschang, N.; Ju, Y.; Mettu, S.; Leeming, M. G.; Caruso, F. Multiligand Metal−Phenolic Assembly from Green Tea Infusions. ACS Appl. Mater. Interfaces 2018, 10 (9), 7632−7639. (98) Rahim, M. A.; Kempe, K.; Müllner, M.; Ejima, H.; Ju, Y.; Van Koeverden, M. P.; Suma, T.; Braunger, J. A.; Leeming, M. G.; Abrahams, B. F.; Caruso, F. Surface-Confined Amorphous Films from Metal-Coordinated Simple Phenolic Ligands. Chem. Mater. 2015, 27 (16), 5825−5832. (99) Ju, Y.; Cui, J.; Müllner, M.; Suma, T.; Hu, M.; Caruso, F. Engineering Low-Fouling and PH-Degradable Capsules through the Assembly of Metal-Phenolic Networks. Biomacromolecules 2015, 16 (3), 807−814. (100) Yang, X.; Yang, B.; He, L.; Li, R.; Liao, Y.; Zhang, S.; Yang, Y.; Xu, X.; Zhang, D.; Tan, H. Bioinspired Peptide-Decorated Tannic Acid for in Situ Remineralization of Tooth Enamel: In Vitro and in Vivo Evaluation. ACS Biomater. Sci. Eng. 2017, 3 (12), 3553−3562. (101) Tardy, B. L.; Richardson, J. J.; Guo, J.; Lehtonen, J.; Ago, M.; Rojas, O. J. Lignin Nano-and Microparticles as Template for Nanostructured Materials: Formation of Hollow Metal-Phenolic Capsules. Green Chem. 2018, 20 (6), 1335−1344. (102) Xiao, G.; Chen, W.; Tian, F.; Richardson, J. J.; Tardy, B. L.; Liu, M.; Joshi, N. S.; Guo, J. Thermal Transition of Bimetallic Metal− Phenolic Networks to Biomass-Derived Hierarchically Porous Nanofibers. Chem. - Asian J. 2018, 13 (8), 972−976. (103) Yang, S. H.; Hong, D.; Lee, J.; Ko, E. H.; Choi, I. S. Artificial Spores: Cytocompatible Encapsulation of Individual Living Cells within Thin, Tough Artificial Shells. Small 2013, 9 (2), 178−186. (104) Park, T.; Kim, J. Y.; Cho, H.; Moon, H. C.; Kim, B. J.; Park, J. H.; Hong, D.; Park, J.; Choi, I. S. Artificial Spores: Immunoprotective Nanocoating of Red Blood Cells with Supramolecular Ferric IonTannic Acid Complex. Polymers (Basel, Switz.) 2017, 9 (4), 140. (105) Guo, J.; Richardson, J. J.; Besford, Q. A.; Christofferson, A. J.; Dai, Y.; Ong, C. W.; Tardy, B. L.; Liang, K.; Choi, G. H.; Cui, J. Influence of Ionic Strength on the Deposition of Metal−Phenolic Networks. Langmuir 2017, 33 (40), 10616−10622. (106) Park, T.; Kim, W. Il; Kim, B. J.; Lee, H.; Choi, I. S.; Park, J. H.; Cho, W. K. Salt-Induced, Continuous Deposition of Supramolecular Iron (III)−Tannic Acid Complex. Langmuir 2018, 34 (41), 12318−12323. P


Review


Technique to Prepare Polymer Capsules. Chem. Mater. 2009, 21 (14), 3042−3044. (126) Hong, S.; Na, Y. S.; Choi, S.; Song, I. T.; Kim, W. Y.; Lee, H. Non-covalent Self-assembly and Covalent Polymerization Cocontribute to Polydopamine Formation. Adv. Funct. Mater. 2012, 22 (22), 4711−4717. (127) Dreyer, D. R.; Miller, D. J.; Freeman, B. D.; Paul, D. R.; Bielawski, C. W. Elucidating the Structure of Poly (Dopamine). Langmuir 2012, 28 (15), 6428−6435. (128) Waite, J. H. Surface Chemistry: Mussel Power. Nat. Mater. 2008, 7 (1), 8. (129) Waite, J. H.; Andersen, N. H.; Jewhurst, S.; Sun, C. Mussel Adhesion: Finding the Tricks Worth Mimicking. J. Adhes. 2005, 81 (3−4), 297−317. (130) Liu, M.; Zeng, G.; Wang, K.; Wan, Q.; Tao, L.; Zhang, X.; Wei, Y. Recent Developments in Polydopamine: An Emerging Soft Matter for Surface Modification and Biomedical Applications. Nanoscale 2016, 8 (38), 16819−16840. (131) Mrówczyński, R. Polydopamine-Based Multifunctional (Nano) Materials for Cancer Therapy. ACS Appl. Mater. Interfaces 2018, 10 (9), 7541−7561. (132) Chen, X.; Yan, Y.; Müllner, M.; van Koeverden, M. P.; Noi, K. F.; Zhu, W.; Caruso, F. Engineering Fluorescent Poly (Dopamine) Capsules. Langmuir 2014, 30 (10), 2921−2925. (133) Hong, S. H.; Hong, S.; Ryou, M.; Choi, J. W.; Kang, S. M.; Lee, H. Sprayable Ultrafast Polydopamine Surface Modifications. Adv. Mater. Interfaces 2016, 3 (11), 1500857. (134) Zhou, P.; Deng, Y.; Lyu, B.; Zhang, R.; Zhang, H.; Ma, H.; Lyu, Y.; Wei, S. Rapidly-Deposited Polydopamine Coating via High Temperature and Vigorous Stirring: Formation, Characterization and Biofunctional Evaluation. PLoS One 2014, 9 (11), No. e113087. (135) Kasemset, S.; Lee, A.; Miller, D. J.; Freeman, B. D.; Sharma, M. M. Effect of Polydopamine Deposition Conditions on Fouling Resistance, Physical Properties, and Permeation Properties of Reverse Osmosis Membranes in Oil/Water Separation. J. Membr. Sci. 2013, 425, 208−216. (136) Lee, M.; Lee, S.; Oh, I.; Lee, H. Microwave-Accelerated Rapid, Chemical Oxidant-Free, Material-Independent Surface Chemistry of Poly (Dopamine). Small 2017, 13 (4), 1600443. (137) Wei, Q.; Zhang, F.; Li, J.; Li, B.; Zhao, C. Oxidant-Induced Dopamine Polymerization for Multifunctional Coatings. Polym. Chem. 2010, 1 (9), 1430−1433. (138) Lee, M.; Kim, J. U.; Lee, J. S.; Lee, B. Il; Shin, J.; Park, C. B. Mussel-Inspired Plasmonic Nanohybrids for Light Harvesting. Adv. Mater. 2014, 26 (26), 4463−4468. (139) Yang, J.; Cohen Stuart, M. A.; Kamperman, M. Jack of All Trades: Versatile Catechol Crosslinking Mechanisms. Chem. Soc. Rev. 2014, 43 (24), 8271−8298. (140) Cui, J.; Ju, Y.; Liang, K.; Ejima, H.; Lörcher, S.; Gause, K. T.; Richardson, J. J.; Caruso, F. Nanoscale Engineering of Low-Fouling Surfaces through Polydopamine Immobilisation of Zwitterionic Peptides. Soft Matter 2014, 10 (15), 2656−2663. (141) Teo, B. M.; van der Westen, R.; Hosta-Rigau, L.; Städler, B. Cell Response to PEGylated Poly (Dopamine) Coated Liposomes Considering Shear Stress. Biochim. Biophys. Acta, Gen. Subj. 2013, 1830 (10), 4838−4847. (142) Zhang, X.; Zeng, G.; Tian, J.; Wan, Q.; Huang, Q.; Wang, K.; Zhang, Q.; Liu, M.; Deng, F.; Wei, Y. PEGylation of Carbon Nanotubes via Mussel Inspired Chemistry: Preparation, Characterization and Biocompatibility Evaluation. Appl. Surf. Sci. 2015, 351, 425−432. (143) Lynge, M. E.; Schattling, P.; Städler, B. Recent Developments in Poly (Dopamine)-Based Coatings for Biomedical Applications. Nanomedicine 2015, 10 (17), 2725−2742. (144) Cui, J.; Yan, Y.; Such, G. K.; Liang, K.; Ochs, C. J.; Postma, A.; Caruso, F. Immobilization and Intracellular Delivery of an Anticancer Drug Using Mussel-Inspired Polydopamine Capsules. Biomacromolecules 2012, 13 (8), 2225−2228.

(107) Yun, G.; Besford, Q. A.; Johnston, S. T.; Richardson, J. J.; Pan, S.; Biviano, M.; Caruso, F. Self-Assembly of Nano-to Macroscopic Metal−Phenolic Materials. Chem. Mater. 2018, 30 (16), 5750−5758. (108) Park, J.; Choi, S.; Moon, H.; Seo, H.; Kim, J.; Hong, S.-P.; Lee, B.; Kang, E.; Lee, J.; Ryu, D. Antimicrobial Spray Nanocoating of Supramolecular Fe (III)-Tannic Acid Metal-Organic Coordination Complex: Applications to Shoe Insoles and Fruits. Sci. Rep. 2017, 7, 6980. (109) Zhong, Q.-Z.; Pan, S.; Rahim, M. A.; Yun, G.; Li, J.; Ju, Y.; Lin, Z.; Han, Y.; Ma, Y.; Richardson, J. J. Spray Assembly of Metal− Phenolic Networks: Formation, Growth, and Applications. ACS Appl. Mater. Interfaces 2018, 10 (39), 33721−33729. (110) Rahim, M. A.; Björnmalm, M.; Bertleff-Zieschang, N.; Besford, Q.; Mettu, S.; Suma, T.; Faria, M.; Caruso, F. Rust-Mediated Continuous Assembly of Metal−Phenolic Networks. Adv. Mater. 2017, 29 (22), 1606717. (111) Maerten, C.; Lopez, L.; Lupattelli, P.; Rydzek, G.; Pronkin, S.; Schaaf, P.; Jierry, L.; Boulmedais, F. Electrotriggered Confined SelfAssembly of Metal−Polyphenol Nanocoatings Using a Morphogenic Approach. Chem. Mater. 2017, 29 (22), 9668−9679. (112) Lee, H.; Kim, W. Il; Youn, W.; Park, T.; Lee, S.; Kim, T.; Mano, J. F.; Choi, I. S. Iron Gall Ink Revisited: In Situ Oxidation of Fe (II)−Tannin Complex for Fluidic-Interface Engineering. Adv. Mater. 2018, 30, 1805091. (113) Adatoz, E. B.; Hendessi, S.; Ow-Yang, C. W.; Demirel, A. L. Restructuring of Poly (2-Ethyl-2-Oxazoline)/Tannic Acid Multilayers into Fibers. Soft Matter 2018, 14 (19), 3849−3857. (114) Kozlovskaya, V.; Kharlampieva, E.; Drachuk, I.; Cheng, D.; Tsukruk, V. V. Responsive Microcapsule Reactors Based on Hydrogen-Bonded Tannic Acid Layer-by-Layer Assemblies. Soft Matter 2010, 6 (15), 3596−3608. (115) Ball, V. High Loading Capacity of Fe3+ Cations in LBL Films Made from Poly (Ethyleneimine) and Tannic Acid: An Alternative to Coordination Driven Multistep Assembly Using Polyphenols and Fe3+. Colloid Interface Sci. Commun. 2014, 3, 1−4. (116) Shutava, T. G.; Lvov, Y. M. Nano-Engineered Microcapsules of Tannic Acid and Chitosan for Protein Encapsulation. J. Nanosci. Nanotechnol. 2006, 6 (6), 1655−1661. (117) Allais, M.; Meyer, F.; Ball, V. Multilayered Films Made from Tannic Acid and Alkaline Phosphatase with Enzymatic Activity and Electrochemical Behavior. J. Colloid Interface Sci. 2018, 512, 722−729. (118) Hammond, P. T. Building Biomedical Materials Layer-byLayer. Mater. Today 2012, 15 (5), 196−206. (119) Kim, B.-S.; Lee, H.; Min, Y.; Poon, Z.; Hammond, P. T. Hydrogen-Bonded Multilayer of PH-Responsive Polymeric Micelles with Tannic Acid for Surface Drug Delivery. Chem. Commun. 2009, 28, 4194−4196. (120) Lomova, M. V.; Brichkina, A. I.; Kiryukhin, M. V.; Vasina, E. N.; Pavlov, A. M.; Gorin, D. A.; Sukhorukov, G. B.; Antipina, M. N. Multilayer Capsules of Bovine Serum Albumin and Tannic Acid for Controlled Release by Enzymatic Degradation. ACS Appl. Mater. Interfaces 2015, 7 (22), 11732−11740. (121) Payra, D.; Yamauchi, Y.; Samitsu, S.; Naito, M. Natural Polyphenol Surfactants: Solvent-Mediated Spherical Nano-Containers and Its Stimuli-Responsive Release of Molecular Payloads. Chem. Mater. 2018, 30, 8025−8033. (122) Payra, D.; Naito, M.; Fujii, Y.; Nagao, Y. Hydrophobized Plant Polyphenols: Self-Assembly and Promising Antibacterial, Adhesive, and Anticorrosion Coatings. Chem. Commun. 2016, 52 (2), 312−315. (123) d’Ischia, M.; Napolitano, A.; Ball, V.; Chen, C.-T.; Buehler, M. J. Polydopamine and Eumelanin: From Structure−Property Relationships to a Unified Tailoring Strategy. Acc. Chem. Res. 2014, 47 (12), 3541−3550. (124) Chen, C.-T.; Martin-Martinez, F. J.; Jung, G. S.; Buehler, M. J. Polydopamine and Eumelanin Molecular Structures Investigated with Ab Initio Calculations. Chem. Sci. 2017, 8 (2), 1631−1641. (125) Postma, A.; Yan, Y.; Wang, Y.; Zelikin, A. N.; Tjipto, E.; Caruso, F. Self-Polymerization of Dopamine as a Versatile and Robust Q


Review

ACS Biomaterials Science & Engineering (145) Zhang, D.; Wu, M.; Zeng, Y.; Wu, L.; Wang, Q.; Han, X.; Liu, X.; Liu, J. Chlorin E6 Conjugated Poly (Dopamine) Nanospheres as PDT/PTT Dual-Modal Therapeutic Agents for Enhanced Cancer Therapy. ACS Appl. Mater. Interfaces 2015, 7 (15), 8176−8187. (146) Song, Y.; Ye, G.; Lu, Y.; Chen, J.; Wang, J.; Matyjaszewski, K. Surface-Initiated ARGET ATRP of Poly (Glycidyl Methacrylate) from Carbon Nanotubes via Bioinspired Catechol Chemistry for Efficient Adsorption of Uranium Ions. ACS Macro Lett. 2016, 5 (3), 382−386. (147) Yang, Y.; Liu, X.; Ye, G.; Zhu, S.; Wang, Z.; Huo, X.; Matyjaszewski, K.; Lu, Y.; Chen, J. Metal-Free Photoinduced Electron Transfer−Atom Transfer Radical Polymerization Integrated with Bioinspired Polydopamine Chemistry as a Green Strategy for Surface Engineering of Magnetic Nanoparticles. ACS Appl. Mater. Interfaces 2017, 9 (15), 13637−13646. (148) Song, Y.; Ye, G.; Wu, F.; Wang, Z.; Liu, S.; Kopeć, M.; Wang, Z.; Chen, J.; Wang, J.; Matyjaszewski, K. Bioinspired Polydopamine (PDA) Chemistry Meets Ordered Mesoporous Carbons (OMCs): A Benign Surface Modification Strategy for Versatile Functionalization. Chem. Mater. 2016, 28 (14), 5013−5021. (149) Le-Masurier, S. P.; Gody, G.; Perrier, S.; Granville, A. M. OnePot Polymer Brush Synthesis via Simultaneous Isocyanate Coupling Chemistry and “Grafting from” RAFT Polymerization. Polym. Chem. 2014, 5 (8), 2816−2823. (150) Jiang, J.; Zhu, L.; Zhu, L.; Zhang, H.; Zhu, B.; Xu, Y. Antifouling and Antimicrobial Polymer Membranes Based on Bioinspired Polydopamine and Strong Hydrogen-Bonded Poly (NVinyl Pyrrolidone). ACS Appl. Mater. Interfaces 2013, 5 (24), 12895− 12904. (151) Zhang, P.; He, M.; Zeng, Y. Ultrasensitive Microfluidic Analysis of Circulating Exosomes Using a Nanostructured Graphene Oxide/Polydopamine Coating. Lab Chip 2016, 16, 3033−3042. (152) Miao, Z.-H.; Wang, H.; Yang, H.; Li, Z.-L.; Zhen, L.; Xu, C.-Y. Intrinsically Mn2+-Chelated Polydopamine Nanoparticles for Simultaneous Magnetic Resonance Imaging and Photothermal Ablation of Cancer Cells. ACS Appl. Mater. Interfaces 2015, 7 (31), 16946−16952. (153) Liu, Y.; Ai, K.; Lu, L. Polydopamine and Its Derivative Materials: Synthesis and Promising Applications in Energy, Environmental, and Biomedical Fields. Chem. Rev. 2014, 114 (9), 5057− 5115. (154) Zhang, Y.; Thingholm, B.; Goldie, K. N.; Ogaki, R.; Städler, B. Assembly of Poly (Dopamine) Films Mixed with a Nonionic Polymer. Langmuir 2012, 28 (51), 17585−17592. (155) Sileika, T. S.; Barrett, D. G.; Zhang, R.; Lau, K. H. A.; Messersmith, P. B. Colorless Multifunctional Coatings Inspired by Polyphenols Found in Tea, Chocolate, and Wine. Angew. Chem. 2013, 125 (41), 10966−10970. (156) Lee, J. S.; Lee, J. S.; Lee, M. S.; An, S.; Yang, K.; Lee, K.; Yang, H. S.; Lee, H.; Cho, S.-W. Plant Flavonoid-Mediated Multifunctional Surface Modification Chemistry: Catechin Coating for Enhanced Osteogenesis of Human Stem Cells. Chem. Mater. 2017, 29 (10), 4375−4384. (157) Watanabe, H.; Fujimoto, A.; Nishida, J.; Ohishi, T.; Takahara, A. Biobased Polymer Coating Using Catechol Derivative Urushiol. Langmuir 2016, 32 (18), 4619−4623. (158) Behboodi-Sadabad, F.; Zhang, H.; Trouillet, V.; Welle, A.; Plumeré, N.; Levkin, P. A. UV-Triggered Polymerization, Deposition, and Patterning of Plant Phenolic Compounds. Adv. Funct. Mater. 2017, 27 (22), 1700127. (159) Zhang, Y.; Su, Y.; Peng, J.; Zhao, X.; Liu, J.; Zhao, J.; Jiang, Z. Composite Nanofiltration Membranes Prepared by Interfacial Polymerization with Natural Material Tannic Acid and Trimesoyl Chloride. J. Membr. Sci. 2013, 429, 235−242. (160) Behboodi-Sadabad, F.; Zhang, H.; Trouillet, V.; Welle, A.; Plumeré, N.; Levkin, P. A. Bioinspired Strategy for Controlled Polymerization and Photopatterning of Plant Polyphenols. Chem. Mater. 2018, 30 (6), 1937−1946.

(161) Krogsgaard, M.; Nue, V.; Birkedal, H. Mussel-Inspired Materials: Self-Healing through Coordination Chemistry. Chem. Eur. J. 2016, 22 (3), 844−857. (162) Zhan, K.; Ejima, H.; Yoshie, N. Antioxidant and Adsorption Properties of Bioinspired Phenolic Polymers: A Comparative Study of Catechol and Gallol. ACS Sustainable Chem. Eng. 2016, 4 (7), 3857− 3863. (163) Zhan, K.; Kim, C.; Sung, K.; Ejima, H.; Yoshie, N. TunicateInspired Gallol Polymers for Underwater Adhesive: A Comparative Study of Catechol and Gallol. Biomacromolecules 2017, 18 (9), 2959. (164) Liu, F.; Long, Y.; Zhao, Q.; Liu, X.; Qiu, G.; Zhang, L.; Ling, Q.; Gu, H. Gallol-Containing Homopolymers and Block Copolymers: ROMP Synthesis and Gelation Properties by Metal-Coordination and Oxidation. Polymer 2018, 143, 212−227. (165) Yu, M.; Deming, T. J. Synthetic Polypeptide Mimics of Marine Adhesives. Macromolecules 1998, 31 (15), 4739−4745. (166) Lee, B. P.; Dalsin, J. L.; Messersmith, P. B. Synthesis and Gelation of DOPA-Modified Poly (Ethylene Glycol) Hydrogels. Biomacromolecules 2002, 3 (5), 1038−1047. (167) Barrett, D. G.; Fullenkamp, D. E.; He, L.; Holten-Andersen, N.; Lee, K. Y. C.; Messersmith, P. B. pH-Based Regulation of Hydrogel Mechanical Properties Through Mussel-Inspired Chemistry and Processing. Adv. Funct. Mater. 2013, 23 (9), 1111−1119. (168) Shin, J.; Lee, J. S.; Lee, C.; Park, H.; Yang, K.; Jin, Y.; Ryu, J. H.; Hong, K. S.; Moon, S.; Chung, H. Tissue Adhesive Catecholmodified Hyaluronic Acid Hydrogel for Effective, Minimally Invasive Cell Therapy. Adv. Funct. Mater. 2015, 25 (25), 3814−3824. (169) Kastrup, C. J.; Nahrendorf, M.; Figueiredo, J. L.; Lee, H.; Kambhampati, S.; Lee, T.; Cho, S.-W.; Gorbatov, R.; Iwamoto, Y.; Dang, T. T. Painting Blood Vessels and Atherosclerotic Plaques with an Adhesive Drug Depot. Proc. Natl. Acad. Sci. U. S. A. 2012, 109 (52), 21444−21449. (170) Ryu, J. H.; Hong, S.; Lee, H. Bio-Inspired Adhesive CatecholConjugated Chitosan for Biomedical Applications: A Mini Review. Acta Biomater. 2015, 27, 101−115. (171) Westwood, G.; Horton, T. N.; Wilker, J. J. Simplified Polymer Mimics of Cross-Linking Adhesive Proteins. Macromolecules 2007, 40 (11), 3960−3964. (172) Matos-Pérez, C. R.; White, J. D.; Wilker, J. J. Polymer Composition and Substrate Influences on the Adhesive Bonding of a Biomimetic, Cross-Linking Polymer. J. Am. Chem. Soc. 2012, 134 (22), 9498−9505. (173) Burke, S. A.; Ritter-Jones, M.; Lee, B. P.; Messersmith, P. B. Thermal Gelation and Tissue Adhesion of Biomimetic Hydrogels. Biomed. Mater. 2007, 2 (4), 203−210. (174) Shin, M.; Park, S.-G.; Oh, B.-C.; Kim, K.; Jo, S.; Lee, M. S.; Oh, S. S.; Hong, S.-H.; Shin, E.-C.; Kim, K.-S. Complete Prevention of Blood Loss with Self-Sealing Haemostatic Needles. Nat. Mater. 2017, 16 (1), 147−152. (175) Lee, J. M.; Ryu, J. H.; Kim, E. A.; Jo, S.; Kim, B.-S.; Lee, H.; Im, G.-I. Adhesive Barrier/Directional Controlled Release for Cartilage Repair by Endogenous Progenitor Cell Recruitment. Biomaterials 2015, 39, 173−181. (176) Shin, M.; Ryu, J. H.; Park, J. P.; Kim, K.; Yang, J. W.; Lee, H. DNA/Tannic Acid Hybrid Gel Exhibiting Biodegradability, Extensibility, Tissue Adhesiveness, and Hemostatic Ability. Adv. Funct. Mater. 2015, 25 (8), 1270−1278. (177) Van Buren, J. P.; Robinson, W. B. Formation of Complexes between Protein and Tannic Acid. J. Agric. Food Chem. 1969, 17 (4), 772−777. (178) Xu, R.; Ma, S.; Lin, P.; Yu, B.; Zhou, F.; Liu, W. High Strength Astringent Hydrogels Using Protein as the Building Block for Physically Cross-Linked Multi-Network. ACS Appl. Mater. Interfaces 2018, 10 (9), 7593−7601. (179) Hong, K. H. Polyvinyl Alcohol/Tannic Acid Hydrogel Prepared by a Freeze-Thawing Process for Wound Dressing Applications. Polym. Bull. 2017, 74 (7), 2861−2872. (180) Chen, Y.-N.; Jiao, C.; Zhao, Y.; Zhang, J.; Wang, H. SelfAssembled Polyvinyl Alcohol−Tannic Acid Hydrogels with Diverse R


Review

ACS Biomaterials Science & Engineering Microstructures and Good Mechanical Properties. ACS Omega. 2018, 3 (9), 11788−11795. (181) Chen, Y.-N.; Peng, L.; Liu, T.; Wang, Y.; Shi, S.; Wang, H. Poly (Vinyl Alcohol)−Tannic Acid Hydrogels with Excellent Mechanical Properties and Shape Memory Behaviors. ACS Appl. Mater. Interfaces 2016, 8 (40), 27199−27206. (182) Shin, M.; Lee, H. Gallol-Rich Hyaluronic Acid Hydrogels: Shear-Thinning, Protein Accumulation against Concentration Gradients, and Degradation-Resistant Properties. Chem. Mater. 2017, 29 (19), 8211−8220. (183) Harrington, M. J.; Masic, A.; Holten-Andersen, N.; Waite, J. H.; Fratzl, P. Iron-Clad Fibers: A Metal-Based Biological Strategy for Hard Flexible Coatings. Science 2010, 328 (5975), 216−220. (184) Holten-Andersen, N.; Harrington, M. J.; Birkedal, H.; Lee, B. P.; Messersmith, P. B.; Lee, K. Y. C.; Waite, J. H. PH-Induced MetalLigand Cross-Links Inspired by Mussel Yield Self-Healing Polymer Networks with near-Covalent Elastic Moduli. Proc. Natl. Acad. Sci. U. S. A. 2011, 108 (7), 2651−2655. (185) He, L.; Fullenkamp, D. E.; Rivera, J. G.; Messersmith, P. B. PH Responsive Self-Healing Hydrogels Formed by Boronate− Catechol Complexation. Chem. Commun. 2011, 47 (26), 7497−7499. (186) Werneke, S. W.; Swann, C.; Farquharson, L. A.; Hamilton, K. S.; Smith, A. M. The Role of Metals in Molluscan Adhesive Gels. J. Exp. Biol. 2007, 210 (12), 2137−2145. (187) Holten-Andersen, N.; Jaishankar, A.; Harrington, M. J.; Fullenkamp, D. E.; DiMarco, G.; He, L.; McKinley, G. H.; Messersmith, P. B.; Lee, K. Y. C. Metal-Coordination: Using One of Nature’s Tricks to Control Soft Material Mechanics. J. Mater. Chem. B 2014, 2 (17), 2467−2472. (188) Krogsgaard, M.; Hansen, M. R.; Birkedal, H. Metals & Polymers in the Mix: Fine-Tuning the Mechanical Properties & Color of Self-Healing Mussel-Inspired Hydrogels. J. Mater. Chem. B 2014, 2 (47), 8292−8297. (189) Ejima, H.; Oba, A.; Yoshie, N. Tuning the Mechanical Properties of Bioinspired Catechol Polymers by Incorporating Dual Coordination Bonds. J. Photopolym. Sci. Technol. 2018, 31 (1), 75−80. (190) Pearson, R. G. The HSAB PrincipleMore Quantitative Aspects. Inorg. Chim. Acta 1995, 240 (1−2), 93−98. (191) Li, Q.; Barrett, D. G.; Messersmith, P. B.; Holten-Andersen, N. Controlling Hydrogel Mechanics via Bio-Inspired Polymer− Nanoparticle Bond Dynamics. ACS Nano 2016, 10 (1), 1317−1324. (192) Gong, J. P.; Katsuyama, Y.; Kurokawa, T.; Osada, Y. Doublenetwork Hydrogels with Extremely High Mechanical Strength. Adv. Mater. 2003, 15 (14), 1155−1158. (193) Gong, J. P. Why Are Double Network Hydrogels so Tough? Soft Matter 2010, 6 (12), 2583−2590. (194) Lin, P.; Ma, S.; Wang, X.; Zhou, F. Molecularly Engineered Dual-Crosslinked Hydrogel with Ultrahigh Mechanical Strength, Toughness, and Good Self-Recovery. Adv. Mater. 2015, 27 (12), 2054−2059. (195) Hou, S.; Ma, P. X. Stimuli-Responsive Supramolecular Hydrogels with High Extensibility and Fast Self-Healing via Precoordinated Mussel-Inspired Chemistry. Chem. Mater. 2015, 27 (22), 7627−7635. (196) Azevedo, S.; Costa, A. M. S.; Andersen, A.; Choi, I. S.; Birkedal, H.; Mano, J. F. Bioinspired Ultratough Hydrogel with Fast Recovery, Self-Healing, Injectability and Cytocompatibility. Adv. Mater. 2017, 29 (28), 1700759. (197) Fan, H.; Wang, J.; Jin, Z. Tough, Swelling-Resistant, SelfHealing, and Adhesive Dual-Cross-Linked Hydrogels Based on Polymer−Tannic Acid Multiple Hydrogen Bonds. Macromolecules 2018, 51 (5), 1696−1705. (198) Skelton, S.; Bostwick, M.; O’Connor, K.; Konst, S.; Casey, S.; Lee, B. P. Biomimetic Adhesive Containing Nanocomposite Hydrogel with Enhanced Materials Properties. Soft Matter 2013, 9 (14), 3825− 3833. (199) Liu, Y.; Meng, H.; Konst, S.; Sarmiento, R.; Rajachar, R.; Lee, B. P. Injectable Dopamine-Modified Poly (Ethylene Glycol) Nano-

composite Hydrogel with Enhanced Adhesive Property and Bioactivity. ACS Appl. Mater. Interfaces 2014, 6 (19), 16982−16992. (200) GhavamiNejad, A.; Park, C. H.; Kim, C. S. In Situ Synthesis of Antimicrobial Silver Nanoparticles within Antifouling Zwitterionic Hydrogels by Catecholic Redox Chemistry for Wound Healing Application. Biomacromolecules 2016, 17 (3), 1213−1223. (201) Han, L.; Liu, K.; Wang, M.; Wang, K.; Fang, L.; Chen, H.; Zhou, J.; Lu, X. Mussel-Inspired Adhesive and Conductive Hydrogel with Long-Lasting Moisture and Extreme Temperature Tolerance. Adv. Funct. Mater. 2018, 28 (3), 1704195. (202) Rahim, M. A.; Björnmalm, M.; Suma, T.; Faria, M.; Ju, Y.; Kempe, K.; Müllner, M.; Ejima, H.; Stickland, A. D.; Caruso, F. Metal−Phenolic Supramolecular Gelation. Angew. Chem., Int. Ed. 2016, 55 (44), 13803−13807. (203) Han, L.; Yan, L.; Wang, K.; Fang, L.; Zhang, H.; Tang, Y.; Ding, Y.; Weng, L.-T.; Xu, J.; Weng, J. Tough, Self-Healable and Tissue-Adhesive Hydrogel with Tunable Multifunctionality. NPG Asia Mater. 2017, 9 (4), No. e372. (204) Liang, S.; Zhang, Y.; Wang, H.; Xu, Z.; Chen, J.; Bao, R.; Tan, B.; Cui, Y.; Fan, G.; Wang, W. Paintable and Rapidly Bondable Conductive Hydrogels as Therapeutic Cardiac Patches. Adv. Mater. 2018, 30 (23), 1704235. (205) Menyo, M. S.; Hawker, C. J.; Waite, J. H. Versatile Tuning of Supramolecular Hydrogels through Metal Complexation of Oxidation-Resistant Catechol-Inspired Ligands. Soft Matter 2013, 9 (43), 10314−10323. (206) Cui, J.; Iturri, J.; Paez, J.; Shafiq, Z.; Serrano, C.; d’Ischia, M.; del Campo, A. Dopamine-Based Coatings and Hydrogels: Toward Substitution-Related Structure−Property Relationships. Macromol. Chem. Phys. 2014, 215 (24), 2403−2413. (207) Andersen, A.; Krogsgaard, M.; Birkedal, H. Mussel-Inspired Self-Healing Double-Cross-Linked Hydrogels by Controlled Combination of Metal Coordination and Covalent Cross-Linking. Biomacromolecules 2018, 19 (5), 1402−1409. (208) Ceylan, H.; Urel, M.; Erkal, T. S.; Tekinay, A. B.; Dana, A.; Guler, M. O. Mussel Inspired Dynamic Cross-linking of Self-healing Peptide Nanofiber Network. Adv. Funct. Mater. 2013, 23 (16), 2081− 2090. (209) Grindy, S. C.; Learsch, R.; Mozhdehi, D.; Cheng, J.; Barrett, D. G.; Guan, Z.; Messersmith, P. B.; Holten-Andersen, N. Control of Hierarchical Polymer Mechanics with Bioinspired Metal-Coordination Dynamics. Nat. Mater. 2015, 14 (12), 1210−1216. (210) Krogsgaard, M.; Andersen, A.; Birkedal, H. Gels and Threads: Mussel-Inspired One-Pot Route to Advanced Responsive Materials. Chem. Commun. 2014, 50 (87), 13278−13281. (211) Fan, H.; Wang, L.; Feng, X.; Bu, Y.; Wu, D.; Jin, Z. Supramolecular Hydrogel Formation Based on Tannic Acid. Macromolecules 2017, 50 (2), 666−676. (212) Rahim, M. A.; Hata, Y.; Björnmalm, M.; Ju, Y.; Caruso, F. Supramolecular Metal−Phenolic Gels for the Crystallization of Active Pharmaceutical Ingredients. Small 2018, 14, 1801202. (213) Haward, M. Plastic Pollution of the World’s Seas and Oceans as a Contemporary Challenge in Ocean Governance. Nat. Commun. 2018, 9 (1), 667. (214) Rochman, C. M. Microplastics Researchfrom Sink to Source. Science 2018, 360 (6384), 28−29. (215) Hillmyer, M. A. The Promise of Plastics from Plants. Science 2017, 358 (6365), 868−870.

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