Noncovalent Muscle-Inspired Hydrogel with Rapid Recovery and

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Applications of Polymer, Composite, and Coating Materials

A Noncovalent Muscle-Inspired Hydrogel with Rapid Recovery and Anti-Fatigue Property Under Cyclic Stress Zengqiang Wang, Shaoyu Lü, Yanhui Liu, Tao Li, Jia Yan, Xiao Bai, Boli Ni, Jing Yang, and Mingzhu Liu ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.9b10753 • Publication Date (Web): 01 Aug 2019 Downloaded from pubs.acs.org on August 2, 2019

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ACS Applied Materials & Interfaces

A Noncovalent Muscle-Inspired Hydrogel with Rapid Recovery and Anti-Fatigue Property Under Cyclic Stress Zengqiang Wanga, Shaoyu Lüa,*, Yanhui Liua, Tao Lia, Jia Yana, Xiao Baib, Boli Nic, Jing Yanga, Mingzhu Liua,* a

State Key Laboratory of Applied Organic Chemistry, Key Laboratory of Nonferrous Metal Chemistry and Resources Utilization of Gansu Province, College of Chemistry and Chemical Engineering, Lanzhou University, Lanzhou 730000, People’s Republic of China b Key Laboratory of Life-Organic Analysis of Shandong Province, School of Chemistry and Chemical Engineering, Qufu Normal University, Qufu 273100, People’s Republic of China c Gansu Tobacco Industrial Co., Ltd., Lanzhou 730050, People’s Republic of China

ABSTRACT: Designing muscle-inspired hydrogels that possess structure and bioactivity similar to muscle is an eternal pursuit in material sciences and tissue engineering. However, the development of a muscle-inspired hydrogel via the formation of noncovalent interactions remains challenging, and its application in sustained loading situations such as cyclic stresses is limited. Herein, H-bonds and microcrystalline domains were introduced, and a noncovalent muscle-inspired hydrogel was developed to mimic both the physical structure and functionality of muscle at the macroscopic level. The hydrogel exhibited excellent mechanical properties (a fracture strength of 2.16±0.08 MPa, fracture strain of 830±23%, elastic modulus of 275±9 KPa, and toughness of 7.04±0.80 MJ/m3), a large energy dissipation (2.00±0.27 MJ/m3 at 600% elongation), and a rapid self-recovery (92±1% toughness recovery within 20 min). Anti-fatigue behavior of the muscleinspired hydrogel was observed upon successive tensile and compressive cyclic loadings. Under 100 cycles of loads, the robustness of the hydrogel has been maintained and even improved, which are achieved due to the strain-induced orientation. Furthermore, the hydrogel was found to be selfhealed. This hydrogel promises to be among the most relevant drivers for the development of newgeneration muscle-inspired hydrogels in the next decade. KEYWORDS: Hydrogels, Muscle-inspired, Noncovalent, Anti-fatigue, Orientation

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INTRODUCTION Biomimetics is a very attractive route for developing new materials and new methods of processing.1-4 Humans are always facing new challenges to which nature has already given solutions, which are examples of reduced materials and energy input with maximizing functionality. For example, great interest now exists regarding supramolecular self-assembly as a means to form complex and hierarchical structures using relatively few constituent elements.5-7 This parallels the method often used by living organisms. Another example can be found in muscle, which is elastic, tough and strong, and possesses a high deformability and recoverability to external stress. Currently, one of the main purposes of biomimetics is to produce muscle-inspired hydrogels.811

Several muscle-inspired hydrogels have previously been developed, such as those based on GB1

domains and resilin;12 ABA-type block proteins and four-armed polyethylene glycol;13 and cucurbit[8]uril14 or aligned cellulose nanofibers and polyacrylamide10. Similar structure and bioactivity have been achieved for these muscle-inspired hydrogels. However, in most cases, interactions that include both noncovalent cross-linking as well as covalent cross-linking have been engineered, while in nature, noncovalent interactions are more pervasive. The covalent cross-linking maintains the shape of the hydrogels and imparts them with elasticity. However, increases in covalent cross-linking density leads to a low toughness, while decreases may yield weak mechanical strength.15 Even though hydrogels formed via covalent cross-linking are shown to be mechanically stable structures, their healable behavior is limited because of the irreversibility of their crosslinks. Meanwhile, the irreversible breakage of the covalent cross-linking hampers their application in sustained loading situations such as cyclic stresses.16 Muscle is largely governed by the muscle protein titin.9 It has been reported that individual titin molecules contain unstructured unique sequences and folded immunoglobulin-like domains.17 The domains in the titin protein that can reversibly unfold may allow muscles to withstand large deformations.18 In addition, individual titin molecules are well-aligned and organized in the filament lattice of muscle. 19 The target of this study is to design a muscle-inspired hydrogel via noncovalent interactions to mimic both the physical structure and functionality of muscle at the macroscopic level. As far as we know, this is the first noncovalent cross-linked muscle-inspired hydrogel. This material enables us to examine how noncovalent interactions impart muscle-like features to the

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hydrogel including toughness, rapid recovery, resilience and self-healing. As shown in Scheme 1, the hydrogel was composed of poly(N-methylol acrylamide) (PNMA) and polyvinyl alcohol (PVA) and treated with freezing/thawing (PNMA-PVA-FT). PVA microcrystalline domains, generated by freezing/thawing, was used to mimic folded titin immunoglobulin domains and random-coil-like PNMA chains were introduced to mimic unstructured sequences. During stretching, the orientation of the PNMA-PVA-FT hydrogel emerges, inducing a uniaxial polymer chain alignment. The hydrogel showed excellent elasticity, toughness as well as a healable behavior, revealing a high deformability and recoverability to external stress.

Scheme 1. Inspired by muscle protein titin, which contains unstructured unique sequences and 3



folded immunoglobulin-like domains, a noncovalent muscle-inspired hydrogel was developed using polyvinyl alcohol (PVA) microcrystalline domains, generated by freezing/thawing, to mimic folded titin immunoglobulin domains and random-coil-like poly(N-methylol acrylamide) (PNMA) chains to mimic unstructured sequences. During stretching, the orientation of the hydrogel emerges, inducing a uniaxial polymer chain alignment.

MATERIALS AND METHODS Material. N-methylol acrylamide (NMA), poly(vinyl alcohol) (PVA 1799, alcoholysis degree 98%~99%), N, N, N', N'-tetramethylethylenediamine (TEMED) were purchased from Aladdin reagent co., Ltd (Shanghai, China). Potassium persulfate (KPS) was obtained from Tianjin Feng Yue Chemical Co., Ltd (Tianjin, China). Deionized water was used throughout. Preparation of Muscle-inspired PNMA-PVA-FT Hydrogel. First, PVA powder was dispersed in deionized water at 90 oC, and was stirred for 2 h until the solution became homogeneous. After the PVA solution was cooled to room temperature, NMA and KPS (0.5 wt% relative to NMA) were added. The solution was allowed to stand for 3 h at room temperature to remove residual bubbles. Then, TEMED (0.55 wt% relative to NMA) was added into the solution. The mixture was quickly placed in a glass mold (100 mm × 50 mm × 1 mm) or a plastic tube (inner diameter 11±1 mm, length 20 mm), and the polymerization was carried out at room temperature for 6 h. After that, PNMAPVA hydrogel was obtained. The samples were treated with freezing/thawing cycle (-20 oC for 12 h, followed by thawing at room temperature for 12 h) to obtain PNMA-PVA-FT hydrogel. PNMA hydrogel and PVA hydrogel were prepared with the same method without PVA and NMA, respectively. Characterization. The samples of PVA hydrogel, PNMA hydrogel, and PNMA-PVA-FT hydrogel were analyzed using a FTIR spectra (Nicolet NEXUS 670 FTIR Spectrometer, USA). The crystal structures of PVA hydrogel, PNMA hydrogel, PNMA-PVA hydrogel, and PNMA-PVA-FT hydrogel were recorded on an X-ray powder diffractometer (XRD, D/Max-2400, Rigaku). In addition, XRD spectra of PNMA-PVA-FT hydrogels subjected to stretching for 0, 50 and 100 cycles were recorded, respectively. Tensile and Compressive Properties Determination. The tensile and compressive properties of the hydrogels were tested using an electrical universal mechanical tester (EZ-Test, SHIMADZU) with a 500 N load cell. For tensile tests, hydrogels were cut into dumbbell-shaped samples (length

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35 mm, width 2 mm, gauge length 12 mm and thickness 1 mm). The speed of uniaxial and loadingunloading cyclic tests remained 100 mm/min. Hydrogels surface was covered with silicone oil to avoid the evaporation of water during the loading-unloading test. Elastic moduli were estimated by the slope over 5~15% of elongation ratio of the tensile stress-strain curve. Toughness was calculated from the area of tensile stress-strain curves or the loading-unloading curves. Recovery Efficiency Determination. To examine the recovery behavior of PNMA-PVA-FT hydrogel, the loading-unloading tests were conducted at fixed strain of 300%, the first area of hysteresis is calculated as W0. At determined time points, the second loading-unloading was carried out, and the area of hysteresis is defined as W1. Recovery efficiency was calculated as W1/W0. Equilibrium Water Content (EWC) Determination. EWC of PNMA-PVA-FT hydrogel was measured by a gravimetric method at room temperature. The hydrogel samples were first weighed and followed by soaking in deionized water completely. At specific time intervals, the hydrogel samples were taken out and the surface water was removed using a filter paper. The hydrogels were weighed until swelling equilibrium was achieved. Then, the swollen hydrogel samples were dried at an oven of 80 oC until reaching a constant mass. All samples were determined in triplicates. EWC of the hydrogels was calculated using the following equation:

EWC =

𝑊𝑠 ― 𝑊𝑑 𝑊𝑠

(S1)

× 100%

where Ws is the weight of the swollen hydrogel samples, while Wd is the dry weight of the hydrogel samples. Rheological Property Determination. The rheological property of PNMA-PVA-FT hydrogel was determined by a rheometer (DISCOVERY HR-2, TA, USA) with a parallel plate of 20 mm in diameter, and the frequency sweep was set from 0.1 to 100 Hz at room temperature. Self-healing Property Determination. PNMA-PVA-FT hydrogel samples were cleaved in half with a blade, and one piece was stained with rhodamine B. The two pieces were brought into contact for 48 h at room temperature. Then, the healed hydrogel was stretched and bend to observe the healing effect. Furthermore, tensile strain-stress curves of the original and healed hydrogels are determined.

RESULTS AND DISCUSSION 5



FTIR and XRD Characterization. The FTIR and XRD profiles were determined to confirm that the muscle-inspired hydrogel was cross-linked by H-bonding interactions and that microcrystalline PVA domains were formed. The samples of PVA hydrogel, PNMA hydrogel, and PNMA-PVA-FT hydrogel were analyzed using a FTIR spectrometer, and the results are shown in Figure S1 (Supporting Information). PVA hydrogel showed characteristic peaks at 3436, 2900 and 1093 cm-1, which are corresponded to O-H stretching, C-H stretching and C-OH stretching, respectively.20 In the spectrum of PNMA hydrogel, some characteristic peaks can be ascribed as 3399 cm-1 for O-H stretching, 3103 cm-1 for N-H stretching, and 1660 cm-1 for C=O stretching, respectively. In the spectrum of PNMA-PVA-FT hydrogel, new peaks were not observed. However, it is noted that redshift in the stretching vibration of O-H (from 3399 to 3381 cm-1) occurred, and the O-H stretching and C-OH stretching bands became broader, suggesting the formation of intermolecular H-bonds between PNMA and PVA chains.21-22 The crystal structures of PVA hydrogel, PNMA hydrogel, PNMA-PVA hydrogel (without freezing-thawing), and PNMA-PVA-FT hydrogel were recorded on an X-ray powder diffractometer. The results are shown in Figure S2 (Supporting Information). PNMA hydrogel is amorphous, as shown by its XRD profile, which exhibits a typical broad diffraction peak centered at 2θ=22.7o. The most prominent diffraction in the profile of PVA hydrogel is due to the (101) reflection peak at 2θ=19.3o.23 The crystal peak was also observed in the profile of PNMA-PVA-FT hydrogel, although it became weaker. This is due to the formation of intermolecular hydrogen bonds among the polymer chains. However, incorporation of PVA in the amorphous PNMA chains without freezing-thawing (PNMA-PVA hydrogel) does not induce crystallization. In addition, the increased crystal intensity with more freezing/thawing cycles also confirmed the formation of the microcrystalline PVA domains.

Mechanical Property of the Muscle-inspired Hydrogel. Effect of PVA content and freezing/thawing cycle on mechanical property. Tensile measurements of the muscle-inspired PNMA-PVA-FT hydrogel with different PVA content and different freezing/thawing cycle were carried out to characterize their mechanical properties at room temperature. The representative stress-strain curves are shown in Figure S3 (Supporting Information). The crystalline regions impart a certain stiffness to PNMA-PVA-FT hydrogel, 6


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compared to PNMA hydrogel and PNMA-PVA hydrogel. When the PVA content increased from 0% to 10 wt%, the mechanical strength of PNMA-PVA-FT hydrogels increased from 0.07 MPa to 0.97 MPa, toughness increased from 0.33 MJ/m3 to 2.56 MJ/m3, and elastic modulus increased from 20 KPa to 148 KPa. However, brittleness was induced when PVA content is above 13%, which is due to the stiffening effect caused by the rigid PVA domains.24 For hydrogel with 13% PVA, the mechanical strength, toughness, elastic modulus was 0.35 MPa, 0.67 MJ/m3 and 117 KPa, respectively. The mechanical strength of PNMA-PVA-FT hydrogel was obviously improved for more freezing-thawing cycles. It is noted that the strength increased from 0.50 MPa to 1.36 MPa, toughness increased from 1.25 MJ/m3 to 3.71 MJ/m3, and elastic modulus increased from 101 KPa to 194 KPa, when the freezing/thawing cycle changed from 0 to 2. The freezing/thawing cycle induces ice crystals to form. Then PVA is expelled from these crystals and concentrates in the interstitial sites.25 More freezing/thawing cycles are favorable for the formation of microcrystalline sites, which act as cross-linkers.26 Therefore, the mechanical strength of PNMA-PVA-FT hydrogel was improved with more freezing/thawing cycles. Effect of PNMA content on mechanical property. The effect of PNMA content on the tensile and compressive property of PNMA-PVA-FT hydrogel was also determined (Figure S4, Supporting Information). In general, PVA hydrogel synthesized by freezing-thawing approach is brittle and compliant.27 Figure S4 exhibited that PVA hydrogel (the content of PNMA is 0) showed low tensile and compressive strength, and low water content. However, compared to the neat PVA hydrogel, all the hydrogels with PNMA exhibited larger resistance to the applied load. PNMA-PVA-FT hydrogel is an amorphous elastomer in which are embedded temporary crosslink sites in the form of PVA microcrystalline domains. More PNMA resulted in more flexible chains and more H-bonds, providing porous three-dimensional structures, as evidenced by the increased equilibrium water content with more PNMA (Figure S4c). Mechanical load can be distributed along the threedimensional structure, resulting in higher mechanical strength of the hydrogels (Figure S4a and b). Meanwhile, more H-bonds provided by PNMA chains prevent the chains from slipping past each other when the applied tension is excessive or prolonged. The rheological determination (Figure S4d) indicated that the storage modulus (Gʹ) is higher than loss modulus (Gʹʹ) for all hydrogels, demonstrating the elastic characteristic of the hydrogels. Gʹ of PNMA-PVA-FT hydrogel with 40% PNMA is greater than that of other hydrogels, demonstrating that this hydrogel is stiffest. The results 7



are consistent with the tensile and compressive assays. Tensile and Compressive Properties of the Muscle-inspired Hydrogel. This muscle-inspired hydrogel represents a compromise between the flexible amorphous chains and the rigid PVA crystallinity, exhibiting a large resistance to stretching or compression, as indicated in Figure 1. PNMA-PVA-FT hydrogel, composed of 10% PVA and 40% PNMA, treated with two freezingthawing cycles, exhibited an excellent tensile property. Their original lengths can be stretched by approximately 7 times when subjected to forces, regardless of whether they were crossed over each other, knotted or twisted (Figure 1a, b and c). In addition, the hydrogel can support a large load of 4000× its own weight without fracture (Figure 1d). A uniaxial compression assay was performed, and PNMA-PVA-FT hydrogel did not fracture, reaching a compressive strength of 4.31 MPa (Figure 1e). These results suggest the tough and ductile behavior of PNMA-PVA-FT hydrogel. This behavior was further tested using an electrical universal mechanical tester and the results are exhibited in Figure 1f and 1g. As indicated in the figure, PNMA hydrogel exhibited a soft and ductile behavior, characteristic of typical noncovalent cross-linking;28 it broke at a strain as high as 728±21%, while the tensile strength was only 0.13±0.02 MPa. By contrast, PNMA-PVA hydrogel reached a tensile strength of 1.47±0.11 MPa without fracturing until a deformation of 785±12%. Remarkably, PNMA-PVA-FT hydrogel did not break at a strain of 830±23% and showed a maximum tensile strength of 2.16±0.08 MPa, exceeding that of PNMA hydrogel by more than 16 times. Moreover, the compressive modulus of PNMA-PVA-FT hydrogel was approximately three times that of PNMA hydrogel (4.31±0.22 MPa vs 1.26±0.09 MPa). The toughness and elastic modulus of the hydrogels also confirm the enhancement in the mechanical properties (Figure S5, Supporting Information). The improved mechanical properties suggest a synergistic effect arising from the H-bond interactions between PNMA and PVA networks and PVA microcrystalline domains. On the molecular level, the double-layered crystallites of PVA are facilitated by intermolecular H-bonds as well as by the weak Van der Waals forces.29 These ordered crystallites scattered in the unordered, amorphous polymer hydrogels. For this reason, PVA crystallite domains function as cross-links for amorphous regions and provide the resistance to deformation. However, it is important to recognize that such ordered PVA arrangements usually exist only in small domains within the hydrogel. Therefore, on a macroscopic level, the introduction of PVA domains changes the hydrogel from soft to tough and flexible, rather than brittle. Previous studies have revealed that 8


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the crystallization of polymeric chains makes them brittle and robust.

28, 30-32

In this study, the

problem was solved by introducing less-ordered crystallite domains.

Figure 1. Photographs of PNMA-PVA-FT hydrogel: stretching to 7 times its initial length under crossover stretching (a), knotted stretching (b), and twisted stretching (c); supportting a large load of 4000× its own weight without fracture (d); enduring compression (e) and tensile stress-strain curves (f) and compressive stress-strain curves (g) of PNMA hydrogel, PNMA-PVA hydrogel and PNMA-PVA-FT hydrogel. The PNMA-PVA-FT hydrogel composed of 10 wt% PVA, 40 wt% NMA, treated with two freezing-thawing cycles. Energy Dissipation of the Muscle-inspired Hydrogel. Tensile hysteresis assays of PNMA hydrogel, PNMA-PVA hydrogel and PNMA-PVA-FT hydrogel at a strain of 500% were conducted to evaluate the samples’ ability to dissipate energy (Figures 2a and 2b). PNMA hydrogel exhibited a negligible hysteresis loop with a dissipated energy of 45±9 KJ/m3, while PNMA-PVA hydrogel and PNMA-PVA-FT hydrogel exhibited higher hysteresis values of 0.90±0.10 MJ/m3 and 9



1.18±0.12 MJ/m3, respectively. These results revealed that the presence of H-bonds and PVA microcrystalline domains provided an effective dissipation mechanism.

Figure 2. Loading-unloading curves (a) and the total energy and dissipated energy (b) of PNMA hydrogel, PNMA-PVA hydrogel and PNMA-PVA-FT hydrogel at a strain of 500%; cyclic loadingunloading curves (c) and the total energy and dissipated energy (d) of PNMA-PVA-FT hydrogel at different strains; (e) cyclic loading-unloading curves of an individual PNMA-PVA-FT hydrogel subjecting to successive stretching at different strains; (f) elastic moduli of an individual PNMAPVA-FT hydrogel subjecting to successive stretching at different strains.

To further illustrate the dissipation mechanism of PNMA-PVA-FT hydrogel, loading-unloading tests were carried out. PNMA-PVA-FT hydrogel exhibited an evident hysteresis between the cyclic 10


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loading-unloading curves at different strains (Figure 2c). With increasing strain, the hydrogel showed a remarkably improved hysteresis loop, which illustrates PNMA-PVA-FT hydrogel efficiently dissipated energy. When the strain increased to 600%, the hydrogel could dissipate as much energy as 2.00±0.27 MJ/m3, which represented 62.8% of the total work (Figure 2d). These features mimic muscles at the macroscopic level, which exhibit a Young’s modulus close to 100 KPa, and present energy dissipation at high strain.12 The loading-unloading behavior of an individual sample at different strains showed similar trends (Figure 2e). These results further evidence that the H-bonds and PVA microcrystalline domains provided the powerful energy dissipation. The elastic moduli of PNMA-PVA-FT hydrogel at different strains were calculated (Figure 2f). When the strain was larger than 200%, a decrease in the elastic modulus was observed, which was because that H-bonds were broken at a small applied strain (50%-200%) due to their weak bond energy.

Self-recovery Behavior of the Muscle-inspired Hydrogel. Considering the dissipation mechanism, it is expected that PNMA-PVA-FT hydrogel could achieve a rapid self-recovery at room temperature. Therefore, the ability of the hydrogel to recover was determined by first subjecting it to a strain of 300%, followed by a second cycle after different recovery times (Figure 3a and 3b). It was found that PNMA-PVA-FT hydrogel preserved 47.8±2.2% of its original toughness without resting. After 20 min, the hydrogel can recover 91.5±1.5% of its original toughness. To determine the mechanism of the rapid self-recovery, an individual PNMA-PVA-FT hydrogel was subjected to successive stretching after different resting times at strains of 50% and 300%, respectively (Figure 3c and 3d). As expected, PNMA-PVA-FT hydrogel exhibited self-recovery properties, whose peak stress was always higher than the previous test at different interval times. When the resting time was up to 20 min, the hydrogel exhibited larger hysteresis loops. Furthermore, it was noted that the toughness of PNMA-PVA-FT hydrogel apparently increased after waiting for a longer time (Figure S6, Supporting Information). 120% and 160% of original toughness were achieved at strains of 50% and 300%, respectively. These results indicated the rapid self-recovery behavior of the muscleinspired hydrogel, which made the hydrogel free from fatigue damage.

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Figure 3. (a) Tensile strain-stress curves of PNMA-PVA-FT hydrogel subjecting to a strain of 300% (original sample), followed by a second cycle after 20 min of recovery; (b) toughness recovery efficiency of PNMA-PVA-FT hydrogel when first subjecting to a strain of 300%, followed by a second cycle after different recovery times; tensile strain-stress curves of an individual PNMAPVA-FT hydrogel subjected to successive stretching after different resting times at strains of 50% (c) and 300% (d). Anti-fatigue Behavior of the Muscle-inspired Hydrogel Under Cyclic Stress. Resilience can be used to measure the ability of a material to deform reversibly without a loss of energy.33-34 The resilience of the hydrogel over 100 cycles of stretching at strains of 50% and 300% was determined, and the results are shown in Figures 4a and 4b, respectively. There is a small hysteresis between the stretching and relaxation curves of the hydrogel at low strain, demonstrating the high resilience of the hydrogel at low strain. However, hysteresis starts to develop at high strain, and the stretching and relaxation curves are no longer superimposable, suggesting that some of the energy was dissipated.35 The peak stress of PNMA-PVA-FT hydrogel at a strain of 300% increased from 0.37 MPa to 0.65 MPa after 100 cycles of stretching, far more than that at a strain of 50% (73 KPa and 77 KPa for the 1st and 100th stretch, respectively). This contrast further suggests that the dynamic hydrogen bonds were ruptured prior to the crystallite domains due to their lower bond energy. At a 12


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strain of 50%, the random-coil chains slide, and the H-bonds between PNMA and PVA chains dislocate from their positions to adjust the concentrated force to avoid failure. At a larger strain (300%), the folded PVA crystallite domains orient toward the extension, which dissipates energy and prevents the local concentration of applied stress that breaks the hydrogel during elongation. It can also be found that the hysteresis increases with the strain, which is similar to the behavior of muscles. 36

Figure 4. Loading-unloading curves of PNMA-PVA-FT hydrogel under successive cycles of stretching at strains of 50% (a) and 300% (b); (c) cyclic loading-unloading curves of PNMA-PVAFT hydrogel when five successive loading-unloading tests without resting were conducted firstly and then the sample was restored at room temperature for 40 min, and another five successive 13



loading-unloading tests were carried out; (d) dissipated energy of PNMA-PVA-FT hydrogel subjected to five successive cyclic loading-unloading; (e) compressive cyclic stress-time curves of PNMA-PVA-FT hydrogel, involving 10 cycles at strain of 80%; (f) compressive stress-strain curves of PNMA-PVA-FT hydrogel at different strains.

Five successive loading-unloading tests of PNMA-PVA-FT hydrogel without resting were conducted. Then, the continuously loaded-unloaded sample was restored at room temperature for 40 min, and another five successive loading-unloading tests were carried out. The experiment was repeated twice. The stress increased from 0.40 MPa (1-5 cycles) to 0.58 MPa (6-10 cycles) and 0.66 MPa (11-15 cycles) (Figure 4c), suggesting that PNMA-PVA-FT hydrogel could recover its initial mechanical properties after 40 min. The dissipated energy of every cycle is shown in Figure 4d. It was found that the dissipated energy increased with the number of cycles. In addition, a reduced and steady decrease in the dissipated energy was observed for 11-15 successive loading-unloading cycles, compared with that of 1-5 and 6-10 cycles. The results indicated that the ordered structures were re-established when the external load is removed and that the original mechanical properties were improved. The results of cyclic compressive assays also confirmed the anti-fatigue behavior (Figure 4e and 4f). The mechanism for the anti-fatigue property of PNMA-PVA-FT hydrogel under cyclic stresses is proposed as follows. The noncovalent muscle-inspired hydrogel is composed of a largely unstructured PNMA matrix and individual PVA microcrystalline domains. However, the crystallites tend to be few in number and randomly oriented relative to each other. When the hydrogel is macroscopically extended uniaxially, molecular orientation is achieved, pulling the individual chains into a roughly parallel orientation. Stretching forces the PNMA amorphous phase to preferentially extend along the extension direction. Then, under a very large extension, the regular packing of adjacent chains occurs, leading to the PVA crystallites themselves being aligned along the same axis.37 Therefore, the improved mechanical property was achieved from the strain-induced orientation. Strain-stiffening behavior has always been found for PVA polymer-clay nanocomposite hydrogels.38-43 However, there are only several reports for PVA hydrogels.44 The mechanism was confirmed by the crystal peak at 2θ=19.3o observed by XRD (Figure 5). The crystal intensity increased with increasing stretching cycles. After stretching for 100 cycles, the intensity at 2θ=19.3o intensified while that at 2θ=22.7o (amorphous state) decreased, indicating that 14


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the hydrogel presents strain-induced orientation.

Figure 5. XRD patterns of PNMA-PVA-FT hydrogel after stretching for 0, 50 and 100 cycles. Self-healing Behavior of the Muscle-inspired Hydrogel. Noncovalent interactions are always introduced to form healable hydrogels. However, these healable hydrogels are usually soft and deformable.28,

45-46

In this study, the hydrogel is mechanically stable and healable, as shown in

Figure 6. PNMA-PVA-FT hydrogel samples were cleaved in half with a blade, and one piece was stained with rhodamine B (Figure 6a). The two pieces were brought into contact for 48 h at room temperature. Evidence of the cut on the surface can be found with a microscope (Figure 6b); however, the hydrogel can be stretched from 3.3 mm to 4.3 mm (Figure 6c) and bend from 180° to 90° (Figure 6d) without breaking. The self-healing behavior was also evaluated by a quantitative method (Figure S7, Supporting Information). An elongation of 224% and stress of 0.29 MPa for the healed sample were achieved. The healing efficiency was estimated to be 24% by comparing the elongation at break of the healed and original samples at room temperature. The healing ability was imparted by the reversible nature of H-bonds. However, the introduction of the PVA microcrystalline domains reduces the mobility of the polymer chains within the hydrogel, delaying the recovery process and resulting in noncomplete healing. Nevertheless, in contrast to other muscle-inspired hydrogels without self-healing properties,10 the self-healing ability of PNMAPVA-FT hydrogel would improve its lifetime and safety when used for load-bearing applications.

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Figure 6. Self-healing properties of PNMA-PVA-FT hydrogel: (a) the hydrogel was cut into half and one piece was stained with rhodamine B; (b) the healed hydrogel after contacting for 48 h at room temperature; (c) the hydrogel can be stretched from 3.3 mm to 4.3 mm; (d) the hydrogel can be bend from 180° to 90°.

CONCLUSION In summary, a noncovalent cross-linked muscle-inspired hydrogel was demonstrated to mimic the architecture and mechanical properties of muscle at the macroscopic level. PVA microcrystalline domains were introduced to mimic folded titin immunoglobulin domains, and random-coil-like PNMA chains were employed to mimic the unstructured sequences of titin. The hydrogel is tough, stretchable, compressive and self-healable; it shows efficient energy dissipation and the ability to recover and anti-fatigue upon successive tensile and compressive loadings. Our results demonstrated that the incorporation of microcrystalline PVA domains into hydrogels provides a novel approach to mimic the behavior of muscle, and the mechanism was proposed. This achievement offers an opportunity to develop muscle-mimicking hydrogels via noncovalent interactions. The strategy is of the utmost importance for applications in material sciences and tissue engineering, including sensor devices, soft tissues, artificial muscles and cartilage replacement.

Supporting Information. FTIR and XRD spectra, tensile toughness, elastic modulus, and compressive stress of PVA hydrogel, PNMA hydrogel and PNMA-PVA-FT hydrogel; Toughness and peak stress of an individual PNMA-PVA-FT hydrogel subjected to successive stretching; Tensile strain-stress curves of the original and self-healed PNMA-PVA-FT hydrogel.

AUTHOR INFORMATION Corresponding Authors *S. Lü. Tel.: +86-931-8912387. Fax: +86-931-8912582. E-mail: [email protected]. *M. Liu. Tel.: +86-931-8912387. Fax: +86-931-8912582. E-mail: [email protected].

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Notes The authors declare no competing financial interest.

ACKNOWLEDGMENTS The authors gratefully acknowledge the financial support of National Natural Science Foundation of China (21875094, 51503091, 51273086, 51541304), and Fundamental Research Funds for the Central Universities (lzujbky-2018-82).

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Noncovalent Muscle-Inspired Hydrogel with Rapid Recovery and

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