Article Cite This: Acc. Chem. Res. XXXX, XXX, XXX−XXX
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Material-Independent Surface Chemistry beyond Polydopamine Coating Haesung A. Lee,† Yanfei Ma,‡,§ Feng Zhou,*,‡,∥ Seonki Hong,*,⊥ and Haeshin Lee*,†
Acc. Chem. Res. Downloaded from pubs.acs.org by WASHINGTON UNIV on 03/05/19. For personal use only.
†
Department of Chemistry, Korea Advanced Institute of Science and Technology (KAIST), 291 University Road, Daejeon 34141, South Korea ‡ State Key Laboratory of Solid Lubrication, Lanzhou Institute of Chemical Physics, Chinese Academy of Sciences, Lanzhou 730000, China § University of Chinese Academy of Sciences, Beijing 100049, China ∥ State Key Laboratory of Solidification Processing, College of Materials Science and Technology, Northwestern Polytechnical University, 127 YouyiXi Road, Xi’an 710072, China ⊥ Department of Emerging Materials Science, Daegu Gyeongbuk Institute of Science and Technology (DGIST), 333 Techno Jungang-daero, Daegu 42988, South Korea
CONSPECTUS: Various methods have been developed in surface chemistry to control interface properties of a solid material. A selection rule among surface chemistries is compatibility between a surface functionalization tool and a target material. For example, alkanethiol deposition on noble metal surfaces, widely known as the formation of a self-assembled monolayer (SAM), cannot be performed on oxide material surfaces. One must choose organosilane molecules to functionalize oxide surfaces. Thus, the surface chemistry strictly depends on the properties of the surface. Polydopamine coating is now generally accepted as the first toolbox for functionalization of virtually any material surface. Layer-by-layer (LbL) assembly is a widely used method to modify properties of versatile surfaces, including organic materials, metal oxides, and noble metals, along with polydopamine coating. On flat solid substrates, the two chemistries of polydopamine coating and LbL assembly provide similar levels of surface modifications. However, there are additional distinct features in polydopamine. First, polydopamine coating is effective for two- or three-dimensional porous materials such as metal−organic frameworks (MOFs), synthetic polyolefin membranes, and others because small-sized dopamine (MW = 153.18 u) and its oxidized oligomers are readily attached onto narrow-spaced surfaces without exhibiting steric hindrance. In contrast, polymers used in LbL assembly are slow in diffusion because of steric hindrance due to their high molecular weight. Second, it is applicable to structurally nonflat surfaces showing special wettability such as superhydrophobicity or superoleophobicity. Third, a nonconducting, insulating polydopamine layer can be converted to be a conducting layer by pyrolysis. The product after pyrolysis is a N-doped graphene-like material that is useful for graphene or carbon nanotube-containing composites. Fourth, it is a suitable method for engineering the surface properties of various composite materials. The surface properties of participating components in composite materials can be unified by polydopamine coating with a simple one-step process. Fifth, a polydopamine layer exhibits intrinsic chemical reactivity by the presence of catecholquinone moieties and catechol radical species on surfaces. Nucleophiles such as amine and thiolate spontaneously react with the functionalized layer. Applications of polydopamine coating are exponentially growing and include cell culture/patterning, microfluidics, antimicrobial surfaces, tissue engineering, drug delivery systems, photothermal therapy, immobilization of photocatalysts, Li-ion battery membranes, Li−sulfur battery cathode materials, oil/water separation, water detoxification, organocatalysts, membrane separation technologies, carbonization, and others. In this Account, we describe various polydopamine coating methods and then introduce a number of chemical derivatives of dopamine that will open further development of material-independent surface chemistry.
1. ADVANCES IN POLYDOPAMINE COATING TECHNIQUES
because of its chemical diversity and heterogeneity. A consensus in polydopamine chemistry begins with spontaneous oxidation of dopamine to dopamine quinone followed by further oxidative
1.1. Understanding the Formation of Polydopamine
Understanding the chemistry of polydopamine formation is a challenging subject despite the extensive studies over a decade © XXXX American Chemical Society
Received: November 20, 2018
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DOI: 10.1021/acs.accounts.8b00583 Acc. Chem. Res. XXXX, XXX, XXX−XXX
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Accounts of Chemical Research
Figure 1. Programmable disassembly and reassembly of polydopamine coatings by alternating non-covalent and cation−π interactions between oligomers. Adapted from ref 7.
insufficient to explain the material independence shown in polydopamine coating because amine-free catechol analogues often fail to show such versatile surface modifications.10 A recent study performed using a surface force apparatus subsequently emphasized the synergistic effect of amine and catechol. Amine groups play an important role in displacing hydrated salts on the surface and then bring catechols near the surface to form strong molecular bonds.11 1.1.2. Non-covalent Interactions in Polydopamine. The identification of a physical trimer, (dopamine)2/DHI, in polydopamine suggested that non-covalent interactions between low-molecular-weight intermediates could be strong enough to generate a three-dimensional molecular assembly.2 Subsequent studies have suggested various types of noncovalent interactions, such as π effects, electrostatic forces, and van der Waals forces.12,13 Recently, Hong and co-workers7 suggested a new type of non-covalent interactions, cation−π interactions, upon revealing the important role of protonated amine groups in polydopamine. It was found that polydopamine disassembled from the surface under strongly basic conditions (pH > 10) as a result of loss of cation−π interactions because the amine cationic species of dopamine became deprotonated. However, under the same pH conditions in the presence of additional cations, it can mediate strong non-covalent interactions. For the first time, the authors demonstrated the pH-sensitive disassembly and subsequent reassembly of a polydopamine coating by re-establishing cation−π interactions using additional cations (Figure 1). Because catechol in DHI is not a strongly π-conjugated system, the coexistence of protonated uncyclized amines is a critical factor in the formation of polydopamine. However, recent studies have raised new questions about the origin of the material-independent coating
conversion to 3,4-dihydroxyindole (DHI), which is considered as an acceptable pathway for a polydopamine monomer since 2007.1 However, recent studies have proposed the existence of other intermediates in polydopamine formation: (1) there is always found to be a detectable level of uncyclized dopamine monomer (i.e., the presence of −NH2) in polydopamine chains,2,3 which indicates that the conversion yield from dopamine to DHI is not 100% (various reactions are discussed in sections 1.2 and 1.3); (2) DHI alone is insufficient for coating;4 (3) degradation of a catechol ring generates pyrroles with carboxylic acid in polydopamine;5,6 (4) DHI−dopamine oligomer intermediates participate in diverse non-covalent interactions (details are provided in section 1.1.2).2,7 Therefore, supramolecular assembly of various combinations of DHI-, dopamine-, and pyrrole-containing oligomers is a current structural insight for polydopamine. Thus, further understanding of the chemical diversity of oligomers that constitute polydopamine is critical in the future. Questions related to the topic include identifications of major repeating units in oligomers and molecular weight distributions. Finally, mechanisms to drive assembly of the oligomers should be address. In sections 1.1.1 and 1.1.2 we introduce a few very recent studies that address these questions related to polydopamine formation. 1.1.1. Synergistic Effect of Amine and Catechol in Material Independence. Polydopamine coating is the first reported material-independent surface chemistry that can be applicable to virtually all kinds of substrates, regardless of surface properties.1 Catechol can interact with substrates via various types of molecular interactions: coordination bonding to metals,8 Michael-type addition and Schiff base formation with amine groups,8 hydrogen bonding on metal oxides,9 and so on. However, this dynamic bonding to various substrates is B
DOI: 10.1021/acs.accounts.8b00583 Acc. Chem. Res. XXXX, XXX, XXX−XXX
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Accounts of Chemical Research
Figure 2. Nature-derived catechol/gallol families. (a−g) Representative plant-derived polyphenol molecules (section 2.1): (a) tannic acid; (b) catechin; (c) epigallocatechin (EGC); (d) epicatechin gallate (ECG); (e) epigallocatechin gallate (EGCG); (f) hydroxyhydroquinol; (g) morin. (h− j) Polymerization pathway of norepinephrine, a catecholic neurotransmitter (section 2.2): (h) norepinephrine; (i) dihydroxybenzaldehyde (DHBA); (j) norepinephrine−DHBA conjugate.
tilting in the solution resulted in a similarly graded polydopamine coating that possessed gradient antibacterial properties.20
properties of polydopamine, as systems of catecholic compounds and diamines have also succeeded in generating material-independent coating capabilities similar to those of polydopamine even though DHI is not generated during the process.14,15
1.3. Various Polydopamine Coating Methods
1.3.1. Polydopamine Coating at Acidic/Neutral pH. The pKa1 of the catechol group in dopamine is approximately 9; at this pH, dissolved oxygen can uptake an electron from the deprotonated catechol anion, producing an oxidized species called catechol quinone. However, a decrease in pH to neutral or acidic does not produce deprotonated catechol anions. Thus, chemical oxidants can be an option for oxidants to trigger polydopamine coating at acidic pH. The chemical structure of polydopamine can be altered depending on the oxidant used: it is noteworthy that the DHI subunits were partially degraded by the action of the oxidants during the oxidant coating, causing the surface to become more hydrophilic.21 A hydrothermal process in an autoclave can trigger polydopamine synthesis without oxidants.22 Also, plasma-activated water can initiate dopamine polymerization even in the absence of oxygen.23 1.3.2. Polydopamine Coating with Rapid Kinetics. The combination of basic pH and chemical oxidants provides a dramatic increase in coating rate. The addition of 2 molar equiv of sodium periodate to dopamine at pH 9.5 resulted in an approximately 200-fold increase in the coating rate.24 The coating could be applied to a large surface via a simple spray approach.24 Microwaves are another emerging trigger for catechol oxidation. Lee et al.25 reported that microwaves successfully reduced the coating time from 6 h to 15 min. They suggested that microwave-assisted rapid polydopamine coating can be achieved by the synergistic action of thermal acceleration followed by radical generation.25
1.2. Importance of Oxygen in Polydopamine Growth
1.2.1. Thin-Film Formation at the Air−Water Interface. Ball and co-workers observed that the growth of a polydopamine film at the air−water interface was twice as fast as that in solution and that the film was able to be transferred to a solid support.16 Independently, Hong et al.17 showed that amine-rich polymers such as polyethylenimine (PEI) dramatically enhanced interfacial film growth, allowing the film to be free-standable. Whereas the air-exposed side of the film was composed largely of nonswellable nonporous catechols resulting from oxidation, the solution side exhibited micropillar-rich water-swellable porous structures that displayed a Janus-type morphology.17 Interfacial free-standing films can also be produced by phenolic compounds called pyrogallols.18 The formation of films containing pyrogallol and PEI was rapid and occurred in a few minutes. In addition, the damaged area in the film was rapidly resealed by film regeneration because of re-exposure of the solution to the air−water interface.18 1.2.2. Gradient Polydopamine Coating. Limited oxygen diffusion naturally generates an oxygen gradient from the top air−water interface to the deep bulk solution. Xu and co-workers utilized the natural oxygen gradient to achieve a polydopamine coating showing gradients in thickness and hydrophilicity simply by tilting the surface in the solution during the coating process.19 Repeated draining and replenishing of the surface by cyclic C
DOI: 10.1021/acs.accounts.8b00583 Acc. Chem. Res. XXXX, XXX, XXX−XXX
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Accounts of Chemical Research 1.3.3. Polydopamine Coating in Organic Solvents. Poor access of water molecules to hydrophobic surfaces is a major drawback of aqueous-based polydopamine coating methods despite the unique material-independent applicability. However, it has been reported that polydopamine coating of hydrophobic surfaces can be performed in the presence of watermiscible solvents such as alcohols.26 Furthermore, by the addition of an organic base such as piperidine, organic solvents that cannot be mixed with water can also be used as solvents for hydrophobic surface coating.27 1.3.4. Phototriggered Polydopamine Coating. Photoillumination followed by photoreaction is a facile method that can be turned on and off in a spatiotemporally controllable manner. This approach has been useful in the fabrication of twodimensional patterns on surfaces. Levkin’s group reported the photo-cross-linking reaction of catechol and gallol derivatives. UV irradiation at 260 nm triggered the oxidation of both dopamine28 and plant polyphenols29 and generated a coating in a few hours. 1.3.5. Dopamine One-Pot Coating with Desired Molecules. Polydopamine-coated surfaces can be further functionalized via various chemical modes of surface-decorated catechols. However, this two-step process is time-consuming and labor-intensive. In 2012, Kang and co-workers developed a single-step surface functionalization method, denoted as “onepot” coating, which introduces the desired molecule to the surface during polydopamine coating. It was found that biopolymers inserted in the one-pot polydopamine coating retained their biological activity.30
consumption of hydroxyl groups of tannic acid to anchor and mask the lubricating oligo/polysaccharides of mucin results in exposure of the phenolic moieties of tannic acid to the outermost layer. Thus, an increased feeling of friction is produced within the oral cavity, and this phenomenon is described as the unique taste called “astringency”.33 In addition to interactions with proteins, tannic acid is able to bind with a zwitterionic polymer, poly(sulfobetaine methacrylate) (PSBMA). This zwitterionic hydrophilic surface exhibits protein adsorption resistance (i.e., antifouling) properties.34 Similar to the material-independent surface chemistry of polydopamine, tannic acid also shows versatility in surface modifications. Surfaces of metal oxides and even hydrophobic polymers have been functionalized with a thickness of 20 nm.35 The surface wettability is controlled by tannic acid. Dense coating onto a polypropylene membrane with tannic acid-functionalized carbon nanotubes generates superoleophobicity upon vacuum filtration of the carbon nanotube solution.36 An additional important ability of tannic acid is the formation of metal−gallol coordination bonds, which are the basis of a second materialindependent surface chemistry.37,38 Metal ion/tannic acid coordination complexes result in the formation of thin adherent films on virtually any type of substrate. This surface chemistry is known as a metal−phenolic network (MPN). Beyond the thinfilm form adhered on surfaces, MPNs can be combined with polymer scaffolds such as polysaccharides to make freestandable hydrogel or fiber forms.39,40 Compared with polydopamine coating, an advantage of MPN surface chemistry is its rapid kinetics. Thus, MPN is suitable to functionalize “living” cell surfaces. Choi and co-workers reported the single-cell encapsulation of individual Saccharomyces cerevisiae by artificial shells (or spores).41 The yeast surfaces protected by MPN layers showed resistance to external stimuli such as UV radiation, lytic enzymes, and toxic silver nanoparticles. 2.1.2. Catechin Derivatives. Catechin (Figure 2b) is a nondegradable phenolic molecule that is a plant secondary metabolite. Similar to tannic acid, catechin also exhibits surface modification and intermolecular interaction capabilities. Catechin does functionalize various surfaces, such as polycarbonate (PC), nylon, poly(dimethylsiloxane) (PDMS), poly(tetrafluoroethylene) (PTFE), polystyrene (PS), Au, and SiO2.42 Interestingly, functionalized surfaces triggered the photografting of polymer brushes of PSBMA and poly(2((methacryloyloxy)ethyl)trimethylammonium chloride).43 The antioxidative and calcium-binding properties of surface-coated catechin resulted in the osteogenic differentiation of human adipose-derived stem cells (hADSCs).44 This was the first study to demonstrate the effectiveness of a polyphenol coating in stem cell culture. Catechin is poorly water-soluble. However, it can form complexes with poly(ethylene glycol) (PEG) by lyophilization processes. After freeze-drying, catechin/PEG complexes became highly water-soluble, demonstrating therapeutic effects for dry eye.45 2.1.3. Urushiol and Alkanecatechol. Beginning prior to the fifth century B.C., a series of catechol derivatives with unsaturated hydrocarbons, collectively called “urushiols”, have been used. Urushiols form protective and polishing coating layers on the surfaces of various wooden furniture. Oxidative cross-linking between catechol in urushiol coatings has similar aspects to polydopamine and other aforementioned polyphenol coatings. However, this cross-linking is largely mediated by the enzyme copper-containing laccase.46 Recently, saturated (i.e., hydrogenated) urushiol (h-urushiol) was prepared in a synthetic
2. NATURE-DERIVED CATECHOL/GALLOL FAMILIES 2.1. Plant Polyphenol Family
2.1.1. Tannic Acid. In nature there exist a number of catechol/gallol chemical derivatives in addition to dopamine. Gallol is trihydroxyphenol, which is biochemically synthesized by hydroxylation of catechol. Gallol-containing molecules are generally superior in intermolecular binding, particularly for proteins. A representative gallol-containing small molecule is tannic acid (Figure 2a). In 1969 it was reported that tannic acid binds to proteins, producing complexes instantaneously.31 At neutral pH, the gallol moieties in tannic acid are not fully protonated, and parts of the hydroxyl groups are deprotonated to form galloquinone. The hydrogen-bond configuration of the gallol moieties in complexes shows the alternating presence of hydrogen-bond donors and acceptors. The coexistence of donors and acceptors is closely related to cytosine base pairing in DNA as well as α-helix and β-sheet formation in proteins. In this developing hypothesis, tannic acid is superior in the formation of protein/tannic acid complexes. A recently published study in 2018 demonstrated that proteins and peptides are complexed with tannic acid to form soluble nanoparticles in particular stoichiometric ranges. For example, nanoparticles are stably formed in aqueous solutions with a [tannic acid]/[green fluorescent protein] stoichiometry between 70 and 140. Surprisingly, when the nanocomplexes are injected via an intravenous route, they effectively target the myocardium. In addition to the extracellular matrix (ECM) proteins in the myocardium, mucin, found in the oral cavity as well as the gastrointestinal tract, is readily complexed with tannic acid.32 Although the exact binding sites in mucin are not known, the abundant hydroxyl groups of tannic acid could interact with surface-exposed oligo/polysaccharides via hydrogen bonds. The D
DOI: 10.1021/acs.accounts.8b00583 Acc. Chem. Res. XXXX, XXX, XXX−XXX
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Accounts of Chemical Research
Figure 3. Small-molecule dopamine conjugates. (a, b) Catecholic derivatives. (c) Catechol-containing acrylate. (d) Diels−Alder (DA) reaction. (e) Cycloaddition reactions for click chemistry. (f) Catecholic liquid lubricant. (g) Zwitterionic polymers in biosurface formation and resistance to fouling. (h) Polydopamine gradient.
2h,i). DHBA acts as the key molecule in reducing surface roughness by preventing the intermolecular aggregation of norepinephrine intermediates. The smooth poly(norepinephrine) nanolayer allows the functionalization of surfaces with micro/nanoscale structures without increasing surface roughness. Furthermore, the secondary alkylamine in DHBA provides a suitable platform for NONO-ate surface immobilization as a nitric oxide (NO) depot. The alkyl hydroxyl group of norepinephrine is effective in initiating surface-initiated ring-opening metathesis polymerization (SI-ROMP) on surfaces.49 In the cited study, the authors demonstrated the surfaceinitiated polymerization of β-caprolactone in a materialindependent manner. Later, the same group also showed surface-initiated atomic transfer radical polymerization (SIATRP) by a catechol-conjugated bromine initiator.51 As the redox activity of polydopamine layers originates from catechol oxidation and reduction, poly(norepinephrine) layers also show redox-active properties. Graphene oxide (GO) spontaneously receives electrons from poly(norepinephrine) layers to create reduced GO (rGO) by simple mixing.52 The advantage of using poly(norepinephrine) reduction is that the surfaces of rGO are simultaneously functionalized and used in additional metal ion doping or SI-ROMP. Biomedical applications of poly(norepinephrine) coatings have been published. Compared with polydopamine, surfaces coated by poly(norepinephrine) show increased hydrophilicity and provide versatile platforms
manner to investigate the physicochemical contributions of the saturated hydrocarbon in natural urushiols.47 Curing with hurushiol takes a long time (∼12 h) compared with the time required for natural urushiol (
