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Biological and Medical Applications of Materials and Interfaces

Mimicking Dynamic Adhesiveness and Strain Stiffening Behavior of Biological Tissues in Tough and SelfHealable Cellulose Nanocomposite Hydrogels Changyou Shao, Lei Meng, Meng Wang, Chen Cui, Bo Wang, Chun-rui Han, Feng Xu, and Jun Yang ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.8b21588 • Publication Date (Web): 17 Jan 2019 Downloaded from http://pubs.acs.org on January 17, 2019

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ACS Applied Materials & Interfaces

Mimicking Dynamic Adhesiveness and Strain Stiffening Behavior of Biological

Tissues

in

Tough

and

Self-Healable

Cellulose

Nanocomposite Hydrogels Changyou Shao, Lei Meng, Meng Wang, Chen Cui, Bo Wang, ChunRui Han, Feng Xu, Jun Yang* Beijing Key Laboratory of Lignocellulosic Chemistry, Beijing Forestry University, No 35, Tsinghua East Road, Haidian District, Beijing, 100083, China

ABSTRACT: Despite self-healing gels with structural resemblance to biological tissues attract great attention in biomedical field, it remains a dilemma for combination between fast selfhealing properties and high mechanical toughness. Based on the design of dynamic reversible cross-links, we incorporate rigid tannic acid-coated cellulose nanocrystal (TA@CNC) motifs into the poly(vinyl alcohol) (PVA)-borax dynamic networks for the fabrication of a high toughness and rapidly self-healing nanocomposite (NC) hydrogel, together with dynamically adhesive and strain stiffening properties that are particularly indispensable for practical application in soft tissues substitutes. The results demonstrate that the obtained NC gels present a highly interconnected network, where flexible PVA chains wrap onto the rigid TA@CNC motifs and form the dynamic TA@CNC-PVA clusters associated by hydrogen bonds, affording the critical mechanical toughness. The synergetic interactions between borate-diol bonds and hydrogen bonds impart typical self-healing behavior into the NC gels, allowing the dynamic cross-linked networks undergo fast rearrangement in the time scale of seconds. Moreover, the obtained NC hydrogels not only mimic the main feature of biological tissue with the unique strain stiffening behavior, but also display unique dynamic adhesiveness to nonporous and porous substrates. It is expected that this versatile approach opens up a new prospect for the rational design of multifunctional cellulosic hydrogels with remarkable performance to expand their applications. 1

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KEYWORDS: cellulose nanocrystal, tannic acid, self-healable hydrogels, tough, adhesive, strain stiffening

INTRODUCTION Autonomous self-healing behaviors are inherent to biological soft tissues in response to accidental damage, which is a particularly advantageous strategy to assist the restoration of their original structures and physiological function.1-4 Inspired by biological systems, self-healing hydrogels with a typical soft-and-wet feature have been increasingly investigated due to their structural resemblances to biological soft tissue, such as good nutrition permeability, high biocompatibility as well as low friction coefficient, which is viewed as a promising candidate for applications in substitutes of soft tissues.5-7 According to various healing mechanisms, self-healing gels can be classified into physical self-healing gels and chemical self-healing gels.8 Compared to the chemical self-healing gels that are generally reform their networks with assistance of external stimuli (e.g., pH,9 UV light,10 or temperature11, 12), physical self-healing gels with dynamic noncovalent interactions (such as hydrophobic interactions,13 host-guest interactions,14 hydrogen bonds,15 and metal coordination bonds16,

17)

are especially

preferred considering their autonomous self-healing features under mild conditions. While elegant and promising, most physical self-healing gels suffer from notoriously poor mechanical performances since there seems an inherent compromise between these two properties. Highly effective healing capacity of hydrogels requires reversible cleavage and formation of dynamic noncovalent interactions and the mobile polymer chains, whereas the high mechanical strength usually benefits from strong and stable crosslinking interactions which would restrict the mobility of polymer chains and decrease the healing capacity of the hydrogels.18,

19

For example, Vlassak et al.20

reported a fast self-healing hydrogel based on the hydrophobic association and multiple hydrogen bonds in micellar copolymerization, which exhibited completely healing within 30 s but low fracture strength of 3.92 kPa. Xie et al.21 developed a self-healable, super tough graphene oxide (GO)-poly(acrylic acid) (PAA) nanocomposite gels by 2


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using Fe3+ ions as cross-linkers, while the optimal healing efficiency can only reach up 70% after a long healing time of 48 h. Despite these previous efforts have been achieved in the creation of self-healing robust gels, it still struggles to create a rapid self-healing (i.e. in the time scale of seconds) hydrogel material without sacrificing mechanical robustness. Fast self-healing efficiency is urgently desirable to restore their original structures and functions as soon as possible from a damage event, which enables to avoid failures caused by the accumulation of cracks, leading to increases in the durability, reliability, and safety of the material in certain practical applications, especially in soft tissues substitute.5, 8, 20, 22 Meanwhile, with the inspiration of the biological soft tissues that not only firmly bonded to bones (i.e. self-adhesive) but also become stiffer as applied strain (i.e. strain stiffening) to counteract large deformation and thereby sustain their structural integrity, biomimetic synthetic physical gel materials imparted with self-adhesive and strain stiffening properties are extremely necessary for potential application in soft tissues substitutes.23-25 However, most synthetic physical gels usually exhibit relatively poor adhesion to bone mainly ascribed to their high water contents and low sliding frictions,26-28 and tend to soften under deformation without the rational structure design.29-32 Hence, a substantial need exists for fabrication of the integrated hydrogels with mechanical toughness, fast self-healing, dynamical adhesiveness, and strain stiffening to be an ideal candidate for replacement and restoration of biological tissue. To address this need, many mussel-inspired adhesive hydrogels, such as polydopamine (PDA) gels systems, have been developed with effective bonding to various solid surfaces.33, 34 These adhesive PDA gels, however, typically struggle to be imparted outstanding mechanical properties without sacrificing other desired properties. 35, 36

Moreover, the high costs of dopamine and the characteristically dark color of PDA

gels may impede the practical applications. Given their analogous structure to dopamine, tannic acid (TA) featured with colorless and low-cost is recognized as a better alternative plant phenolic to PDA for the design of biocompatible adhesive materials or functional surfaces engineering.37-42 3



Inspired by mussel-inspired adhesive mechanism, we propose a cellulose nanocomposite (NC) hydrogel with simultaneous enhancement of mechanical performances as well as self-healing properties by incorporating rigid tannic acidcoated cellulose nanocrystal (TA@CNC) motifs into the polyvinyl alcohol (PVA)borax dynamic networks. Particularly, the promotion in the self-healing efficiency of NC gels based on the synergy of reversible borate-diol bonds and hydrogen bonds is remarkable where their mechanical recovery exceeds 90% within 60 s without sacrificing other properties. Intriguingly, microscopic network structures of NC gels present a unique “hard and soft” core-shell structure consisting of rigid TA@CNC skeleton (hard core) and surface wrapped flexible PVA polymer chains (soft shell) via hydrogen bonds, endowing NC gels with general feature of strain-stiffening behavior that is notably sought after in the bioinspired materials design strategy to mimic biological tissue. Indeed, PVA-borate hydrogels have been widely investigated as a model system to study their nonlinear rheology properties (e.g. strain stiffening) of physical gels,43 while there is not distinct strain stiffening behavior in the tensile properties (large deformation) of PVA-borax gels, inferring that the dynamic TA@CNC plays a significant role in the nonlinear mechanical properties of NC gels. Moreover, the obtained NC gels display dynamic adhesiveness to nonporous and porous substrates as well as unique tissue-adhesive, which is a particular advantage for fixing on bones in tissue substitute filed. This elegant strategy by incorporating sacrificial bonds associated CNC motifs offers a new perspective for the design and development of multifunctional cellulosic hydrogels with remarkable properties, expanding their applications where mechanically robust, rapidly self-healing, dynamically adhesive, and strain stiffening properties are required, such as tissue substitutes.

MATERIALS AND METHODS Materials. The never-dried bleached softwood Kraft pulp obtained from DongHua Pulp Factory was applied to prepare cellulose nanocrystal (CNC) suspensions. Tannic 4


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acid (TA), poly(vinyl alcohol) (PVA, Mw=1750 ± 50 Da) and borax (Na2B4O7·10H2O) were purchased from Beijing Lanyi Co. Ltd., China. Tris(hydroxymethyl)aminomethane (Tris) was purchased from Sigma-Aldrich. All other chemicals were reagent grade and used without further purification. Extraction of Cellulose Nanocrystals. Extraction of cellulose nanocrystals (CNCs) was described in our previous work.44 In brief, 4 g of pulp was added into 200 mL of 55 wt % sulfuric acid under vigorous mechanical stirring (350 rpm) in an ice-water bath, then the suspension was heated to 50 °C under continually stirring for 90 min. The obtained suspension was diluted with deionized water and concentrated by centrifugation, followed by dialysis against water until pH neutrality. Then the highpressure homogenization was performed to increase dispersity and stability of the suspension, and finally the homogenized CNC suspension (1 wt%) was sonicated for 10 min (300 W) and cryopreserved (4 °C) before usage. The average dimensions of CNCs were measured to be 200 ± 10 nm long × 20 ± 5 nm wide (Figure S1). Preparation of Tannic Acid Coated Cellulose Nanocrystals. The TA@CNC suspension was prepared via a one-pot water-based process. The above obtained CNC suspension (100 g) was adjusted to pH = 8.0 by dropwise adding Tris buffer solution (1 M). Then 3 g of tannic acid (TA) was added and the resultant suspension was magnetically stirred for 6 h at room temperature, the collected TA@CNC suspension (~3.5 wt%; CNC:TA=1:3, wt%) was sonicated (300 W, 10 min) and stored at 4 °C before usage. The average dimensions of TA@CNC were measured to be 210 ± 15 nm long × 40 ± 5 nm wide (Figure S1). Nanocomposite (NC) Hydrogels Preparation. Deionized water (24 g), PVA powder (6 g), and TA@CNC suspension (1-3 wt%) were added into a 50 mL beaker, then heated at 98 °C under continually stirring for 2 h until the PVA powder was completely dissolved to form a homogeneous mixture solution. Subsequently, borax solution (0.04 mol/L, 30mL) was added into the obtained mixture solution (water bath at 90 °C) for 1 h until the gels were attained. The sample codes for NC gels (TA@CNC-x) are marked by the weight ratio of the 5



TA@CNC against water (constant at 24 g). For example, 1.0% TA@CNC ionic gel referred to a gel loaded with 240 mg of TA@CNC is designated as [email protected], and the detail compositions of NC gels are summarized in Table S2. For neat PVA-borate cross-linked hydrogels (TA@CNC-0), they were prepared by the same procedures without incorporation of TA@CNCs. Mechanical Tests. The mechanical properties of the NC gels were measured at room temperature using a Universal Material Testing machine (Zwell/Roell) equipped with a 200 N load cell. The uniaxial tensile test was performed on the rectangular-shape sample (10 mm in width, 6 mm in depth, and 35 mm in length). Both ends of the sample were clamped and stretched at a constant rate of 60 mm/min. A layer of silicone oil was coated on the sample surface during the testing and storage time to minimize water evaporation. The fracture stress and strain were determined from the stress-strain curves at the breaking points. For each sample, three strips were tested and the average values were present. The tensile hysteresis was analyzed under the same conditions in which the sample was initially stretched to a predefined strain and immediately unloaded at the same velocity. Stress relaxation measurements were performed by keeping a constant strain over a period of time (600 s), and the time dependent stress was recorded. The unconfined compression tests of the cylindrical sample (15 mm in diameter and 10 mm in height) were conducted at a crosshead speed of 10 mm/min. Morphological Observation. Microscopic observation via transmission electron microscopy (TEM) was performed using a Hitachi H7600 instrument at an acceleration voltage of 100 kV. The frozen samples were cryo-microtomed (Leica EM UC6) to obtain the thin section (∼100 nm) and stained with uranyl acetate for 10 s before TEM observation. Self-Healing Experiments. (1) The macroscopic self-healing behavior of hydrogels was examined by the direct visual inspection. Briefly, two pieces of NC gel disks (15 mm in diameter and 10 mm in height) stained by rhodamine B and methyl green were cut into equal 4 pieces, respectively. Then the pieces of alternate colors were combined into the blended integral hydrogel disks. (2) The strip-like specimens (80 mm length 6


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and 10 mm width) were cut into halves using blades, and then the two separate halves were brought into contact immediately without applied stress in air and were stored in a sealed vessel to minimize the water evaporation. After a certain self-healing period (10-600 s), the uniaxial tensile test was measured to evaluate the tensile healing efficiency (HE) that defined as the tensile strength ratio between the healed gel and original gel. (3) To compare the role of hydrogen bonds and borate-diol bonds in selfhealing process, the fracture interfaces of cut gel pieces were immersed dipped in urea and glucose solution (1 M) for 10 min before healing, respectively, then the tensile strength was measured to evaluate the tensile healing efficiency. Rheological Measurements. (1) The storage moduli (G′) of the NC gel disks (15 mm in diameter) with different TA@CNC contents were tested by rheometer (TA AR2000) fitted with parallel plates (both upper and underside plates are 15 mm in diameter). Under a fixed strain level (1.0%), the angular frequency was swept from 0.01 to 100 rad/s. (2) The gel disks were measured under strain amplitude sweep (10%1000%) at a fixed angular frequency (10 rad/s). (3) The alternate step strain sweep of gel disk was measured at a fixed angular frequency (6.28 rad/s). Amplitude oscillatory strains were switched from small strain (1.0%) to subsequent large strain (160%, 250%, and 400%) with 200 s for every strain interval. (4) The step strain sweep tests were also performed for a fixed large strain (400%) with loading period changed from 200 to 400 s for each strain level. Adhesion Tests. Lab shear strength tests were performed with different substrates (glasses, aluminum (Al), polytetrafluoroethylene (PTFE), bone, and wood). The specimens were prepared according to M. A. Zadeh’s work by gluing two identical plates (length × width × thickness = 75 × 20 × 1 mm3) with a junction contact area of 4 cm2 using 0.2 g NC gels.45 The lap joint was compressed under a 300 g weight for 10 min, and then the two ends of the substrates were mechanically clamped to prevent undesired changes of the junction contact area. Subsequently, the adhesion test was immediately conducted using a universal Zwell/Roell mechanical tester at a crosshead speed of 2 mm/min until the occurrence of separation. The adhesion strength was 7



calculated by the maximum load divided by the initial bonded area. Each sample was tested a minimum of 3 times and averaged.

RESULTS AND DISCUSSION Our products consisted of four components: water, tannic acid-coated cellulose nanocrystals (TA@CNCs), poly(vinyl alcohol) (PVA), and borax. The cellulose nanocrystals (CNCs) were extracted from pulp paper by the sulfuric acid hydrolysis and high-pressure homogenization, resulting the well-dispersed rod-like CNCs particles. The subsequent surface coating of CNCs was achieved by adding tannic acid (TA) under alkaline conditions (Figure 1a), where TA can form the higher molecular weight species due to the self-oxidation of plant polyphenol, leading to the decreased solubility.46 Presumably, this decreased solubility of tannic acid and its inherent affinity toward cellulose generate the TA coated CNCs (TA@CNCs), which remain in colloidal stability but with a slightly yellow discoloration (Figure 1b). To prepare TA@CNC nanocomposite (NC) gels, PVA initially dissolved in hot water (98 °C) and subsequently mixed with TA@CNCs, the obtained fluidic mixture transformed into elastic hydrogel via homogeneously mixing with borax solution (0.04 M) under stirring (90 °C). According to the proposed preparation scheme in Figure 1c, the resultant NC gels are primarily constructed by dynamic borate-diol complexation between borate ions and the adjacent hydroxyl of PVA (Figure 1d), which impart the hydrogels with the self-healing property to dynamically restructure and autonomously self-heal after mechanical disruption. The incorporation of TA@CNCs motifs into the PVA−borax networks enables to further interact with the surrounding polymer phase by the formation of hydrogen bonds derived from the extensive hydroxyl groups between TA@CNCs and PVA (Figure S2), and thereby simultaneously improve the mechanical and self-healing properties of NC gels. In this system, the borate-diol bonds primarily serve as strong cross-links to construct the primary structure and maintaining the integrity of gels, whereas the weaker hydrogen bonds acting as sacrificial bonds 8


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preferentially break and reform, synergistically resulting in good mechanical performances. Intriguingly, both of borate-diol bonds and hydrogen bonds are dynamically reversible, which collectively contribute to the rapid and effective selfhealing networks while affording elasticity as the same time.

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Figure 1. (a) The self-assembly coating process from well-dispersed CNC particles to tannic acid-coated CNC (TA@CNC), and (b) the corresponding AFM images (bar = 100 nm). (c) Schematic illustration of the NC gel networks with TA@CNC and PVAborate. (d) Reversible borate-diol complexation between PVA and borax. (e) The pictures of NC gels with different TA@CNC contents and the corresponding TEM images (bar = 500 nm), the inset shows the core-shell structure that TA@CNC nanofiber core with surface wrapped PVA shell (bar = 50 nm).

As visualized in Figure 1e, with the increased contents of TA@CNCs, NC gels turn into opaque along with the darker color, and transmission electron microscopy (TEM) images reveal their distinction of interconnected structure (Figure S3). In contrast to pristine PVA-borax gels with well-defined and loose porous networks, NC gels with TA@CNC motifs exhibit the denser networks with thicker wall and smaller pores, inferring a continuous polymer layer (soft shell) wrapped on the rigid TA@CNC skeleton (hard core) and the formation of interconnected TA@CNC-PVA clusters. Notably, no obvious aggregates were found within the examined length scale, indicating the excellent phase miscibility and well-dispersed hybrid network, which may facilitate the stress transfer and energy dissipation.47 Indeed, this uniformly distributed core-shell hierarchical structure could remarkably improve the mechanical properties of NC gels, since the typical “hard-and-soft” components (TA@CNC-PVA clusters) throughout the matrix enables a large contact area with polymer chains and leads to efficient stress transfer.48, 49 The uniaxial tensile tests were conducted to corroborate the enhancement of TA@CNCs on mechanical property. As shown in Figure 2a, a pronounced increase in the fracture stress associated with increasing fracture strain is exhibited, revealing the significant reinforcement role of TA@CNCs. A summary of mechanical properties including Young's modulus, fracture stress, fracture strain, and toughness is listed in Table S1. It is worthy to note that the increase in both stiffness and toughness are coupled without sacrificing extensibility, which may be attributed to the stiffness of 10


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individual TA@CNCs and strong synergetic interactions between adjacent rigid nanoparticles and the flexible polymer phase, leading to synergistic effects on the dramatic reinforcement.50

Figure 2. (a) Tensile stress-strain curves of NC gels as a function of TA@CNC contents. (b) Tensile stress-strain curve and the corresponding first derivative line of TA@CNC3 gels. (c) Stress relaxation curves for NC gels over time. (d) Loading–unloading cycle up to a strain of 600%.

Contrast to the counterpart PVA-borax gels, the NC gels incorporating with TA@CNC motifs show the unique strain stiffening behavior as shown in Figure 2b. After the yield point A, the NC gels initially displays a typical J-shaped strain-stiffening behavior (the slope of the stress–strain curves increases with strain) until point H, followed by the so-called strain-softening behavior (the slope of stress–strain curves decreases with strain) until the fracture point. The NC gels with various TA@CNC contents follow the similar stress-strain profiles, indicating that strain-stiffening behaviors could be a general feature in NC gels. 11



Stress relaxation was conducted to gain insights into the dynamically structural rearrangement for the strain-stiffening behavior of NC gels (Figure 2c). After holding the prestrain (400% for NC gels, 300% for PVA-borax gels), the stress relaxation process reveals that the NC gels released the stress faster than that of pristine PVAborax gels and the relaxation dynamics is positively correlated with TA@CNC contents, convincing the superior ability of the NC gel network to undergo rearrangement by dynamic non-covalent interactions (hydrogen bonds) between TA@CNC skeleton and surface wrapped polymer chains. The dynamic interactions can also be justified by the result that the hysteresis of the NC gel network is more pronounced than the neat PVAborax counterparts (Figure 2d), indicating the TA@CNC skeleton provides significant energy dissipation by reversible association and dissociation of hydrogen bonding.

Figure 3. Schematic illustration of the proposed mechanism for the strain-stiffening behavior of the TA@CNC NC gels. The initial hydrogen bond-associated TA@CNCPVA clusters are stretched, coiled polymer chains wrapped on the TA@CNC surface start to elongate and slide, releasing significant hidden lengths accompanied by preferential sacrificial rupture of hydrogen bonds before borate-diol bonds (borax-PVA complexation), which lead to the strain-stiffening. With the increase in stress, the gels undergo dynamic network disruption under a larger strain.

We hypothesized the following mechanism for the strain-stiffening behaviors of NC 12


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gel networks by their dynamically structural rearrangement at different stretched levels. As illustrated in Figure 3, NC gels present a highly porous and interconnected network with a thick wall on the TA@CNC surface at the initial “relaxed” state (strain = 0%). Notably, PVA segments have high affinity to TA@CNC surfaces,51 which promotes the formation of hydrogen bond-associated TA@CNC-PVA cluster with a unique coreshell structure consisting of rigid TA@CNC skeleton (hard core) and surface wrapped flexible PVA polymer chains (soft shell). Meesorn et al.51 demonstrated that PVA would lead to better dispersion of CNCs and support the formation of a hydrogenbonded percolating network within the polymer/CNC nanocomposites. Herein, the existence of TA@CNC-PVA cluster leads to the higher density of polymer chains around the TA@CNCs than that in the bulk matrix, and the PVA segments may extend to neighboring clusters to generate a more stable structure on account of hydrogen bonding between TA@CNC and PVA chains. Tong et al.52 found that strain stiffening behaviors of polymer-clay nanocomposite hydrogels were caused by the orientation of both network chains and clay platelets under large deformation of uniaxial elongation. Similarly in this work, with increase in strain (small strain), PVA polymer chains gradually elongate along the stress direction and thereby lead to the pore walls become thinner. During elongation, TA@CNC-PVA clusters are oriented considering that the rigid and straight cellulose backbone has a strong tendency to rearrange to their parallel conformations with stress.49 After the yield point, coiled polymer chains wrapped on the TA@CNC surface start to elongate and slide, releasing significant hidden lengths of coiled polymer chains accompanied by preferential sacrificial rupture of hydrogen bonds. This process would dissipate a large number of energy and thus increase the resistance against crack propagation, leading to the sequential increase in stiffness with applied strain (strain stiffening). As the network is subjected to an even larger deformation (916%), the initially interconnected clusters become isolated and the crosslinked network undergo disruption and collapse because of the dissociation of complexation between PVA and borax. Fortunately, reversible nature of borate-diol bonds and hydrogen bonds allows to self-heal from an event of damage (discussion 13



below).

Figure 4. (a) Temperature sweep by 6.28 rad/s with 0.1% strain, the inset shows heating-cooling cycles. (b) The free-shapeable properties of NC gels (stained with methylene blue).

Since the NC gels engineered by the transient physical cross-links (borate-diol bonds and hydrogen bonds), their rheological properties are expect to be temperature dependent. According to Figure 4a, the value of storage modulus (G′) is constantly higher than that of loss modulus (G″), indicating elasticity of NC gels within the entire temperature range (25-100 °C). The value of loss factor (tan δ = G″/G′) levels off at relative low temperature (25-60 ºC) and then increases with further increasing of temperature (>60 ºC) due to the more significant decrease in G′. In fact, this decrease in G′ is ascribed to the disruption of dynamic physical interactions throughout gel network as the temperature is raised, rather than relying on the irreversible degradation or hydrolysis of the systems, which can be corroborated through the reversible transition back to original elastic state (inset images). Intriguingly, this reversible transition endows NC gels display the free-shapeable properties under heating-cooling cycles, enabling the gels readily adapt many complex geometrical shapes (Figure 4b) to satisfy certain demands in the practical applications.

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Figure 5. (a) Images of self-healing process with disc-shaped gel samples (one stained with rhodamine B and the other stained with methyl green). (b) The tensile stress- strain curves of the NC hydrogels with different TA@CNC contents before and after healing for 60 s, and (c) the corresponding healing efficiency. (d) The time-dependent selfhealing behaviors of the TA@CNC-3 NC gels. (e) Effect of urea and glucose treatments on the mechanical properties of the healed TA@CNC-3 gels (healing 10 min). (f) Synergistically self-healing mechanism of NC gels by dynamic borate-diol bonds and hydrogen bonds.

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The reversible interactions involving borate-diol bonds and hydrogen bonds in the gel networks ensure fast self-healing property to the NC gels. Self-healing behaviors of NC gels can be visualized directly as illustrated in Figure 5a. In details, the two discshaped gel samples with red (stained with rhodamine B) and green colors (stained with methyl green) were cut into equal four pieces by a razor blade, respectively (Figure 5a1, a2). Subsequently, the exposed fresh incisions of cut gels pieces were brought into contact, integrating a new gel disk with alternate colors. After a prescribed healing time without any external intervention, the healed gel disks could stand up by themselves (Figure 5a3) and even load the weights of 200 g (Figure 5a4), revealing the self-healing behavior of the NC gel networks, which is related to the dynamic interactions rather than the simple adhesion. Moreover, we investigated the tensile properties of self-healed gels with different TA@CNC contents to evaluate their self-healing efficiency. The healing efficiency (HE) is defined as the fracture strength ratio between the healed sample and the pristine sample. After healing for 10 s at 25 °C, the HE increased from 60.5% to 92.0% with TA@CNC content increasing from 0% to 3% (Figure 5b and 5c), demonstrating that the dynamic hydrogen bonds-associated TA@CNC-PVA cluster motifs can effectively facilitate the reversible rearrangement in the self-healing process of NC gel. The TA@CNC-3 gels with optimized healing efficiency are chose to further investigate the effect of the healing time on healing efficiency via tensile tests. Figure 5d indicates that HE can further increase from 89.5% up to 98.2% as the time elongated to 600 s. This result can be explained that the self-healing process is a time dependent process, where more borate-diol complexation and hydrogen bonds are achieved at the neighboring fracture surface and promotes the self-healing level. Especially noteworthy is that contrast to other self-healing gels that require external stimuli such as pH, temperature, and UV light,9-11 the self-healing behavior of the current NC gel occurs autonomously, which can be viewed as most advantageous of self-healing gels for applications in biomedical fields. To demystify the role of borate-diol bonds and hydrogen bonds in self-healing 16


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process, the cut gel pieces were treated by dipping the fracture interfaces into urea and glucose solution (1 M) for 10 min, respectively, and then the tensile strength was measured after healing. As shown in Figure 5e, the healed gel treated with urea displays a lower tensile fracture strength of 79.5 kPa than that of the pristine gel (99.2 kPa), which is attributed to the disruption of hydrogen bonding across the fracture interfaces after the urea treatment.53, 54 Similarly, for the pieces treated with glucose, the tensile strength decreased more significantly to 21.8 kPa, revealing that glucose significantly hindered the self-healing process. In glucose solution, borax preferentially complexes with the cis-diol groups of glucose due to the high complexation constant.55,

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Consequently, glucose molecules act as competitive diols to hinder the formation of dynamic borate-diol bonds between the cut pieces. The above results collectively demonstrate that the dynamic borate-diol interactions play a dominant role in selfhealing behavior of NC gels compared to hydrogen bonding. Based on the above results, the proposed self-healing process is illustrated in Figure 5f. When the NC gels are cut into pieces, the dynamic borate-diol bonds and hydrogen bonds are disrupted, resulting in the exposing freely reactive groups at fracture interfaces. These disassociated reactive groups have a strong tendency to proceed conformational rearrangement, and thereby dynamic borate-diol bonds and hydrogen bonds undergo reformation after the cut surfaces contact again, which synergistically contribute to the rapid and effective self-healing networks.57

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Figure 6. The rheological measurements of NC gels. (a) The storage moduli (G′) of NC gels with different TA@CNC contents by 6.28 rad/s with 1.0 % strain. (b) The G′ and G″ of TA@CNC-3 gels from strain amplitude sweep (10%-1000%) at a fixed angular frequency (6.28 rad/s). (c) The G′ and G″ of TA@CNC-3 gels by alternate step strain switching from small strain (1.0 %) to large strain (160 %, 250 %, and 400 %) at a fixed angular frequency (6.28 rad/s). Each strain interval was kept constant as 200 s. (d) Cyclic G′ and G″ values of the hydrogel for a large strain level (400 %) and different loading period from 200 to 400 s with 100 s interval.

To elucidate the effect of TA@CNCs on the viscoelastic properties of the NC gels, the storage moduli (G′) were recorded for the gels with variable loading of TA@CNC at a fixed strain (1 %). The results show a substantial increase in elastic response, inferring the reinforcement role of TA@CNC motifs (Figure 6a). Therefore, the mechanical properties of the NC gels can be facilely tailored by TA@CNC content. Besides, the strain amplitude sweep shows that the G′ and the loss moduli (G″) curve intersect at the strain of 160% (Figure 6b), signifying the transition from elastic gel to 18


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viscous sol at a higher strain due to the collapse of the dynamic cross-linked networks. Additionally, the dynamic reversible behavior of the NC gel was assessed by the alternate step strain test with aim to study the disruption and reformation of the NC gel network. When the gel was subjected to a small amplitude oscillatory shear (strain = 1%), G′ was greater than G″ and both moduli keep almost constant with time, indicating the stable elastic gel (G′ > G″) under small oscillatory strain. As the oscillatory shear strain stepped from 1% to 160% and maintained for 200 s, the G′ and G″ overlapped (G′ = G″), while they immediately recovered their original values after the strain returned to 1% (Figure 6c). Subsequently, when the hydrogel was subjected to an even larger amplitude oscillatory shear (strain = 250% or 400%), the G′ and G″ were inverted immediately (G′ < G″) and accompanied by a drastic decrease in G′, which indicated that the gel was converted into the sol state due to the disruption of gel network. When the applied strains (250% and 400%) was decreased to the initial small strain (1%) again, the G′ almost restored the initial value without any evident decrease, suggesting that the gel-like character (G′ > G″) was recovered. Thus, this rapid sol−gel transition with the complete recovery of the gel network after shear induced disruption corroborated the excellent self-healing capability of the NC gel. Moreover, we fixed step strain to 400 % and varied the loading period from 200 to 400 s with a constant 100 s interval to investigate the influence of loading period on rheological recovery behavior. The results in Figure 6d showed that the G′ immediately recovered after switching from a large strain of 400 % to a small strain of 1% regardless of loading period, implying the independency of rheological recovery with loading period. These results further corroborate that polymer networks of NC gels exhibit rapid self-healing behaviors when subject to oscillatory shear strain, which may be ascribed to the reversible reconstruction of synergetic interactions between dynamic borate-diol complexation and hydrogen bonds in the cross-linked network.

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Figure 7. (a) Schematic representation of lap shear test geometry. (b) Tensile-strain curves of the glass slides samples bonded with NC gel with variable TA@CNC contents. (c) Evaluation of glass lap joints over time bonded with TA@CNC gels. (d) Repeatable adhesion behavior of TA@CNC-3 NC gels via lap-shear tests. (e) Shear stress for different

nonporous

substrates

(including

glass,

aluminum

(Al),

polytetrafluoroethylene (PTFE)), porous substrates (using bone and wood as typical samples), as well as biological soft tissue (using hogskin as a typical example) bonded with TA@CNC-3 NC gels. (f) Pictures of NC gels bonded with bone samples. (g) NC gels can directly adhere to fingers and withstand the stretch. (h) Tensile strength versus tissue-adhesive strength charts for comparison with previous mussel-inspired adhesive hydrogels.

The NC gels were found to be highly adhesive on a wide of substrates, which was attributed to the catechol groups of oxidized polyphenols mimicking the mussel 20


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adhesion mechanism.33,

58, 59

The adhesion strength of the NC gels bonded with

substrate surfaces was quantified by the lap-shear tests and the experimental scheme was depicted in Figure 7a. The lap joints were prepared by bonding a quantitative amount of NC gels between two substrates, resulting an overlap area 400 mm2 with gel density of ≈10 mg cm−2 and estimated thickness of ≈30 μm. Figure 7b revealed that the shear stress of NC gels bonded with glass increased significantly in contrast to the neat PVA-borate gels, further corroborates that the substantial promotion for interfacial adhesion mainly stems from the incorporation of the TA@CNCs as the promoter. To evaluate the adhesive durability of NC gels, the glass lap joints bonded with NC gels were subjected to a constant stress (20, 40, and 60 kPa, respectively) and the evolution of stress was recorded in Figure 7c. One can note that the bonded glass lapjoints did not show any remarkable creep or failure within a time scale of 8 min under a stress of 20 kPa, whereas the creep of hydrogel adhesive layer could be gradually activated with the applied stress increased to 40 kPa. When the applied stress was further enhanced up to 60 kPa, close to the fracture stress, an immediate creep and failure of the lap-joint appeared. Interestingly, the shear stress of the re-bonded glass lap joints was essentially comparable to their initial values (Figure 7d) after eight cycles. Whereas for the increased adhesion stress during the initial five cycles over the repeated cycles is most likely due to the increased viscosity involving unavoidable loss of water during bonding, which is in good agreement with the previous reports that the shear stress for lap joints increased with decreased water content.60 While excessive loss of water would lead to a slight decrease in shear strength after five cycles, it still exceeds 75% of original adhesion strength after eight cycles, this result is quite distinct from the traditional adhesive hydrogels that could not be reactivated after curing.34, 61 To explore the application of NC gels as adhesive tissue substitutes in biomedical fields, the adhesion affinity of NC gels to substrates with smooth (glass, Al, and PTFE) as well as nonporous surfaces (wood and bone) was examined (Figure 7e), which widely exist in our daily life. The hydrogen bonding is probably the primary interaction in the adhesion interfaces between NC gels and smooth substrates (glasses and PTFE), 21



whereas the NC gels demonstrated the higher adhesion on Al due to the synergy of metal complexation and hydrogen bonding. Compared with these smooth surfaces, the affinity between the NC gels and porous substrate substantially increased especially for bone materials (Figure 7f), inferring that the NC gels are promising candidates for regenerated natural bone-tissue junction including artificial articular cartilage or meniscus tissues.25 In addition, the NC gels display impressive tissue-adhesive behavior, which can directly adhere to human fingers without any skin tissue irritation or inflammatory response and withstand the stretch (Figure 7g), benefiting its further application in wound dressing. In contrast to previous reported mussel-inspired adhesive hydrogels,33, 58, 59, 62-64 this new NC gel demonstrates integrated remarkable tensile strength and tissue-adhesive strength as shown in Figure 7h, showing their distinct advantages in promising biomedical applications. The tensile strength of this NC gel is 1.2-3.6 times higher than that of polydopamine-based nanocomposite hydrogels,58, 59, 62, 64 indicating the significant mechanical reinforcement derived from resistance against crack propagation of rigid TA@CNCs and the synergistic interfacial interactions of borate-diol bonds and hydrogen bonds. Although the tensile strength is lower than PDA-pGO-PAM hydrogels,33 however, the tissue-adhesive strength is far superior to PDA-pGO-PAM hydrogels (2.5 times). The tissue-adhesive strength of this NC gels is also 1.4-5.7 times higher than that of polydopamine-based adhesive hydrogels with covalent or noncovalent cross-linking,33, 58, 59, 62-64 which affords a better alternative than dopamine to design mussel-inspired adhesive hydrogels with the lowcost and biocompatible plant polyphenol.

CONCLUSIONS In this work, we have reported a cellulose nanocomposite (NC) hydrogel with simultaneous enhancement between mechanical performances and self-healing properties by incorporating rigid TA@CNC into the PVA-borax dynamic networks. The resultant NC gels are found to be strain-stiffen and highly adhesive that are notably sought after in the bioinspired materials design strategy to mimic biological tissue. 22


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TEM images reveal that NC gels present a highly interconnected network with incorporated TA@CNC-PVA clusters, where flexible PVA chains wrap onto the neighboring rigid TA@CNC closely associated by extensive hydrogen bonds. The dynamic TA@CNC-PVA clusters contribute to the significant mechanical reinforcement of NC gels via sacrificial rupture of reversible bonds. The synergetic interactions of reversible bonds involving borate-diol bonds and hydrogen bonds promote the self-healing properties of NC gels within the time scale of seconds and meet the requirement of tissue substitutes thereby. Besides, the dynamic adhesiveness of the NC gels to nonporous and porous substrates ascribed to the presence of catechol groups, exhibiting particularly advantageous to be a candidate of tissue substitute for fixing on bones. Looking ahead, we expect this elegant strategy that incorporating sacrificial bonds associated CNC motifs paves a way to design multifunctional cellulosic hydrogels with mechanically robust, rapidly self-healing and dynamically adhesive properties for their practical applications.

ASSOCIATED CONTENT Supporting Information Mechanical properties summary of the NC gels; Compositions of the NC gels; dimension distribution histograms and AFM images of CNCs and TA@CNC; FTIR spectra of PVA, TA@CNC and NC gel; The TEM pictures of NC gels with different TA@CNC contents.

AUTHOR INFORMATION * Corresponding author: [email protected]

Tel: 86-10-62337223

ACKNOWLEDGMENTS This work is financially supported by Natural Science Foundation of China (21674013).

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