Multifunctional Stimuli-Responsive Hydrogels with Self-Healing

Completely gelled hydrogel disk with a diameter of 20 mm and a thickness of 1000 μm ..... The mechanism of good resilience and fast recovery property...
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Article Cite This: Chem. Mater. 2018, 30, 1729−1742

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Multifunctional Stimuli-Responsive Hydrogels with Self-Healing, High Conductivity, and Rapid Recovery through Host−Guest Interactions Zexing Deng,† Yi Guo,† Xin Zhao,† Peter X. Ma,‡,§,∥,⊥ and Baolin Guo*,† †

Frontier Institute of Science and Technology, and State Key Laboratory for Mechanical Behavior of Materials, Xi’an Jiaotong University, Xi’an, 710049, China ‡ Department of Biomedical Engineering, University of Michigan, Ann Arbor, Michigan 48109, United States § Department of Biologic and Materials Sciences, University of Michigan, Ann Arbor, Michigan 48109, United States ∥ Macromolecular Science and Engineering Center, University of Michigan, Ann Arbor, Michigan 48109, United States ⊥ Department of Materials Science and Engineering, University of Michigan, Ann Arbor, Michigan 48109, United States S Supporting Information *

ABSTRACT: Self-healing hydrogels with multifunctionality as a type of fascinating material show potential application in various fields, such as biomedicine, tissue engineering, and wearable electronic devices. However, to combine the properties of autonomous self-healing property, high conductivity, excellent mechanical properties, and stimuli-responsive properties for hydrogel is still a great challenge. Herein, we present self-healing conductive hydrogels based on β-cyclodextrin (β-CD), Nisopropylacrylamide (NIPAM), multiwalled carbon nanotubes (CNT) and nanostructured polypyrrole (PPY). Among them, βCD served as the host molecule, and NIPAM served as the guest molecule, CNT as the physical cross-linker and conducting substrate, and PPY as the highly conductive component, respectively. The obtained hydrogels exhibit high conductivity, selfhealing property, flexible and elastic mechanical property and rapid stimuli-responsive property both to temperature and nearinfrared (NIR)-light together. The excellent characteristics of the hydrogels are further illustrated by pressure-dependent sensors, large-scale human motion monitoring sensors and self-healable electronic circuit. Cytotoxicity test indicated that they are nontoxic to L929 fibroblast cells and C2C12 myoblast cells. Taken together, these multifunctional hydrogels are excellent candidates for stimuli responsive electrical devices, artificial organs, and so on. functional self-healing hydrogels.19−22 We hypothesized that the hydrophobic isopropyl group in NIPAM can form host−guest interactions with CD to synthesize thermoresponsive selfhealing hydrogels. However, there is no report about self-healing hydrogels through β-CD and NIPAM. Various functions were brought into self-healing hydrogels to expand their applications.23 Among them, electrically conductive self-healing polymeric hydrogels have been a hot study spot, because of their excellent flexibility, porosity, desirable mechanical property, and good conductivity, demonstrating great potential application in self-healable electrical devices,24 tissue engineering scaffolds,25−28 drug delivery vehicle,29 wound dressing, and artificial skin.30,31 Great efforts have been made to exploit and develop conducting self-healing hydrogels. Conducting components or polymers such as multiwalled carbon

1. INTRODUCTION Self-healing hydrogels are a class of smart materials and they have the ability to repair and restore the hydrogels to their original functionality after being damaged.1−4 They have brought great interest from science and technology, because the self-healing characteristic can prolong the lifetime of materials.5−7 To design autonomous self-healing hydrogels, a noncovalently bonded system8,9 is an efficient method where the polymerization and/or the cross-linking occur via intermolecular interactions of the monomer units and/or the side chains by using hydrogen bonds,10−12 certain metal−ligand coordination bonds,13 ion interactions,14 or the host−guest interactions.15 Recently, cyclodextrins (CD) as host molecules to establish supramolecular hydrogel system through host−guest interactions have been extensively reported,16−18 because they can be easily chemically functionalized and can also interact with some guest molecules or groups specifically. Besides, N-isopropylacrylamide (NIPAM) is a typical thermoresponsive molecule with distinct chemical character and has been reported for preparation of © 2018 American Chemical Society

Received: January 1, 2018 Revised: February 9, 2018 Published: February 10, 2018 1729

DOI: 10.1021/acs.chemmater.8b00008 Chem. Mater. 2018, 30, 1729−1742

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Figure 1. (A) Synthesis route of self-healing hydrogels poly(NIPAM-co-β-CD). (B) Scheme of preparing conductive self-healing hydrogels poly(NIPAM-co-β-CD)/CNT/PPY.

nanotubes (CNT), graphene, nanostructured polypyrrole (PPY), and polyaniline were usually incorporated into the conductive hydrogels system to obtain desirable conductivity.32−40 In our previous work, we designed several types of conductive self-healing hydrogels, that are, chitosan-graf t-aniline tetramer and dibenzaldehyde-terminated poly(ethylene glycol)25 as raw materials to fabricate hydrogels as cell delivery vehicle for cardiac repair, quaternized chitosan-g-polyaniline and benzaldehyde group functionalized poly(ethylene glycol)-copoly(glycerol sebacate)30 as raw materials to fabricate hydrogels for wound dressing adhesiveness and γ-cyclodextrin dimer as the host molecule and tetraaniline-poly(ethylene glycol)41 as the guests to fabricate the conducting injectable hydrogels. However, these hydrogels showed low conductivity, because of the character of aniline oligomer, which is much lower than conventional conductive polymers. Yu’s group24 developed a flexible conductive autonomous self-healing gel by using a metal−ligand of G-Zn-2,2′:6′,2″-terpyridine and conductive nanostructured polypyrrole for self-healable electronic circuit, whereas the gel was not injectable. Park’s group42 fabricated a conductive self-healing hydrogel through polymerization of pyrrole within agarose solution for electronic skin and bioelectrodes. However, its self-healing behavior was induced by external heat or light stimuli. Therefore, developing injectable hydrogels with high conductivity, autonomous self-healing ability, and desirable mechanical property is still highly anticipated. In this work, we aim to design multifunctional conductive hydrogels with desirable mechanical property and self-healing ability by using β-cyclodextrin (β-CD), N-isopropylacrylamide (NIPAM), CNT, and PPY, and we further developed their potential applications in pressure-dependent sensors, large-scale human index finger motion sensing, bicipital muscle of arm

motion sensing, and self-healable electrical devices. The selfhealing hydrogels were prepared by copolymerization of acryloyl-β-cyclodextrin (AC-β-CD), NIPAM, and (poly(ethylene glycol)-b-poly(propylene glycol)-b-poly(ethylene glycol) (PF127))/CNT, and then subsequently placed into pyrrole solution for in situ deposition of electrically conductive PPY nanoparticles on its substrate. The chemical structure, morphology, electrical conductivity, temperature-dependent swelling ratio, swelling kinetics and deswelling kinetics, photothermal behavior, mechanical properties, and rheological properties of the hydrogels were systematically evaluated. The hydrogel exhibited a macroporous structure with an interconnected network of CNT and PPY nanoaggregates in the matrix, and the poly(NIPAM-co-β-CD)/CNT/PPY hydrogel displayed a high conductivity of 34.93 S/m. Moreover, the hydrogels displayed rapid response rates, both to temperature and nearinfrared (NIR) light within several minutes. Compression and cyclic test suggested their stable and excellent elasticity, and rheology testing revealed their rapid and highly efficient selfhealing ability. Furthermore, we designed an electrical circuit to illustrate their potential application in three-dimensional (3D) bulky pressure-dependent sensors and self-healable electronic device to demonstrate their autonomous self-healing property, desirable conductivity, and good elasticity. Cytotoxicity test indicated that they were nontoxic to L929 cells and C2C12 cells. All of these results indicated that these self-healing hydrogels exhibited great potential for application in intelligent sensors and wearable electronic devices.

2. EXPERIMENTAL SECTION 2.1. Materials. Multiwalled carbon nanotubes (CNT) were provided by XFNANO, Inc. (purity >95%). Poly(ethylene glycol)-bpoly(propylene glycol)-b-poly(ethylene glycol) (PF127), ammonium persulfate (APS), and N,N,N′,N′-tetramethylethylenediamine 1730

DOI: 10.1021/acs.chemmater.8b00008 Chem. Mater. 2018, 30, 1729−1742

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instrument. D2O was used as the solvent for β-CD, NIPAM, and NIPAM/β-CD. DMSO-d6 and CDCl3 were used as the solvents for ACβ-CD and PF127-diacrylate, respectively.46 The 2D NOESY NMR spectrum of the complex NIPAM/β-CD in D2O was also measured using a Bruker Ascend 400 MHz NMR instrument to demonstrate the spatial relationship of corresponding protons. 2.6.2. FT-IR Characterization. FT-IR spectra of dried poly(NIPAMco-β-CD), poly(NIPAM-co-β-CD)/CNT, and poly(NIPAM-co-β-CD)/ CNT/PPY were carried out on a Nicolet 6700 Fourier transform infrared (FT-IR) spectrometer (Thermo Scientific Instrument) in the range of 4000−600 cm−1 with the average of 32 scans at a resolution of 4 cm−1.47 2.6.3. Volume Phase Transition Temperature (VPTT) of Hydrogel. DSC measurements of the wet samples were carried out on a differential scanning calorimetry (DSC, TA Q200) with a nitrogen flow rate of 50 mL/min to test the volume phase transition temperature (VPTT) of the hydrogel. All of the samples were first heated from 10 °C to 50 °C, and equilibrated at 50 °C for 3 min, then cooled down from 50 °C to 10 °C at a heating rate of 2 °C/min. 2.6.4. Morphology of Hydrogels. The morphology of the hydrogels was recorded by scanning electron microscopy (SEM) (Quanta, Model 250 FEG FEI) with an operation voltage of 5 kV.40 The freezed hydrogels were cut into pieces and dried in a freeze dryer for 24 h before SEM observation. 2.6.5. Swelling Ratios of Hydrogels at Different Temperatures. The swelling ratios of the hydrogels from 25 °C to 50 °C were investigated, and the weight of the hydrogels at different temperatures was weighed after water on the surface of hydrogels was removed, using wet filter paper. The swelling ratio (SR) is calculated by the following equation:

(TEMED) were provided by Sigma−Aldrich. N-isopropylacrylamide (NIPAM), acryloyl chloride (AC), triethylamine (TEA), and anhydrous N,N-dimethylformamide (DMF) were purchased from J&K Scientific, Ltd., and used without further purification. Other reagents were analytical grade. 2.2. Synthesis of Acryloyl-β-cyclodextrin. Acryloyl-β-cyclodextrin was synthesized according to ref 43. β-CD (5 mmol) was first added to 20 mL of anhydrous DMF to solubilize under stirring at room temperature, and then 15 mmol of TEA was added to the solution to neutralize the HCl. Thereafter, the reaction was placed into an ice bath, followed by the dropwise addition of 15 mmol of CD in 20 mL of DMF. The solution was stirred for 24 h, and the reaction temperature increased to room temperature naturally. After reaction, the solution was filtrated to remove the TEA hydrochloride, and then the filtered solution was precipitated in precooled acetone. The precipitate was washed with acetone and chloroform three times and dried in a vacuum oven for further use. Typical peaks of ester groups at 1720 cm−1 (CO) and 1265 cm−1 (C−O) could be found on AC-β-CD curve, and double bonds (CC) at 810 cm−1 were also shown on FT-IR spectra of AC-βCD, which indicated the successful synthesis of AC-β-CD.43,44 2.3. Synthesis of PF127-Diacrylate. PF127-diacrylate was synthesized according to a previous report with modification.45 Briefly, 0.4 mmol of PF127 and 1.2 mmol of TEA were dissolved in 40 mL of anhydrous dichloromethane in an ice bath. Then, 1.2 mmol of acryloyl chloride was added dropwise into the solution. Similar with previous reactions, the solution was stirred for 24 h, and the reaction temperature increased to room temperature naturally. After reaction, the solvent was concentrated, and the product was purified by dialysis against DD water via dialysis tube with a MWCO of 3.5 kDa for three days, followed by lyophilization. 2.4. Synthesis of Poly(NIPAM-co-β-CD) and Poly(NIPAM-co-βCD)/CNT Hydrogels. Poly(NIPAM-co-β-CD) hydrogel was synthesized by copolymerization with NIPAM and AC-β-CD, as shown in Figure 1. For example, 10 mg of AC-β-CD and 90 mg of NIPAM were dissolved in 1 mL of precooled DD water, then 10 μL of precooled 100 mg/mL ammonium persulfate (APS) aqueous solution and 2 μL of TEMED were added and mixed well; 1 mL of solution was pipetted into 2 mL of EP tubes for polymerization. The hydrogel was washed with distilled water (DD water) after reaction to remove salts in the hydrogel matrix for purification. The dry weight of poly(NIPAM-co-β-CD) hydrogel was 74.3 ± 1.9 mg, according to three groups of freeze-dried hydrogels. Poly(NIPAM-co-β-CD)/CNT hydrogel was synthesized by copolymerization with NIPAM, AC-β-CD, and PF127-DA/CNT. One hundred milligrams (100 mg) of CNT, 100 mg of PF127-DA, and 25 mL of DD water were added into a 50 mL tube and sonicated in an ice bath for 4 h to obtain CNT solution, and was then treated for another hour before use. In a typical preparation process, 10 mg of AC-β-CD and 90 mg of NIPAM were dissolved in 1 mL of CNT solution, then 10 μL of precooled 100 mg/mL ammonium persulfate (APS) aqueous solution and 2 μL of TEMED were added and mixed well; 1 mL of the solution then was pipetted into 2 mL of EP tubes for polymerization. The purification process was the same as that of poly(NIPAM-co-β-CD) hydrogel. The dry weight of poly(NIPAM-co-β-CD)/CNT hydrogel was 88.0 ± 2.4 mg, according to three groups of freeze-dried hydrogels. 2.5. Preparation of Poly(NIPAM-co-β-CD)/CNT/PPY Hybrid Hydrogel. To prepare poly(NIPAM-co-β-CD)/CNT/PPY hybrid hydrogel, poly(NIPAM-co-β-CD)/CNT hydrogel was first heated to release the water in the matrix and then immersed into 12 mL of 0.2 mol/L pyrrole solution (1 mol/L p-toluenesulfonic acid) to reswell again. Twelve milliliters (12 mL) of precooled Fe(NO3)3 (2.4 mmol) aqueous solution was added to the pyrrole solution to react for 4 h to fabricate the poly(NIPAM-co-β-CD)/CNT/PPY gel. The purification process was the same as that used for poly(NIPAM-co-β-CD)/CNT hydrogel. The dry weight of poly(NIPAM-co-β-CD)/CNT/PPY hybrid hydrogel was 93.1 ± 0.4 mg, according to three groups of freeze-dried hydrogels. 2.6. Characterizations. 2.6.1. 1H NMR Characterization. 1H NMR (400 MHz) spectra of β-CD, NIPAM, NIPAM/β-CD, AC-β-CD, and PF127-diacrylate were measured using a Bruker Ascend 400 MHz NMR

SR =

Ws − Wd Wd

where Ws is the weight of the wet hydrogel at different temperatures and Wd is the dry weight of the hydrogel.41 2.6.6. Deswelling Behavior of Hydrogels at 50 °C and Reswelling Behavior of Hydrogels at 25 °C. The deswelling kinetics of the hydrogels was performed in a water bath at a temperature of 50 °C. The hydrogels were first immersed in DD water until the equilibrium was reached and were then placed into a water bath at a temperature of 50 °C. The hydrogels were weighed after the water on the surface of the hydrogels was removed by using filter paper at a specific time. Water retention (WR) is calculated by the following equation:

WR (%) =

Wt50 − Wd × 100 W0 − Wd

where Wt50 is the weight of the wet gel at a specific time at 50 °C, W0 the weight of the wet gel at 25 °C after equilibrium, and Wd the dry weight of the hydrogel. The hydrogels were shrunk at 50 °C in water bath and then placed into the DD water at 25 °C to reswell. The hydrogels were weighed after water on the surface of the hydrogels was removed by using filter paper at a specific time. The value of WR is calculated using the following equation: WR (%) =

Wt25 − Wd × 100 W0 − Wd

where Wt25 is the weight of the wet gel at a specific time at 25 °C, and other terms are the same as defined above. 2.7. Photothermal Irradiation Test. The hydrogels were exposed to NIR irradiation (PSU-III-LED, laser light with a wavelength of 808 nm) for 10 min at a distance of 3 cm. The temperature of hydrogels was immediately recorded by a Visual IR thermometer (Fluke, Model VT04A) at a specific time. 2.8. Electrical Conductivity Measurement. The electrical conductivity (σ) of slab hybrid hydrogels (50 mm (length) × 10 mm (width) × 0.25 mm (thickness)) was measured by an Agilent Model B2900A digital four-probe tester with a current of 1 mA and a linear probe head (1.0 mm space). Before test, the hydrogels were washed with the DD water and water on the surface of the hydrogels was removed by 1731

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Figure 2. (A) 1H NMR spectra of NIPAM, β-CD, and NIPAM/β-CD spectra. (B) FT-IR spectra of hydrogels. (C−H) SEM images of poly(NIPAM-coβ-CD) (panels (C and F)), poly(NIPAM-co-β-CD)/CNT (panels (D and G)), and poly(NIPAM-co-β-CD)/CNT/PPY hydrogel (panels (E and H)). filter paper. The electrical conductivity was calculated using the following equation:42

shearing rate was set from 0.1 rad/s to 100 rad/s, with a constant strain of 1%. (2) Completely gelled hydrogel between parallel plates was directly used to perform the strain amplitude sweep test (γ = 0.01%− 500%) with a constant frequency of 10 rad/s at 25 °C. (3) Completely gelled hydrogel disk with a diameter of 20 mm and a thickness of 1000 μm was placed between 20 mm parallel plates with a gap of 1000 μm at 25 °C. Then, the alternate step strain sweep test was performed at a fixed angular frequency (10 rad/s) at 25 °C. Amplitude oscillatory strains were switched from small strain (γ = 1.0%) to subsequent large strain (γ = 400%) with 100 s for every strain interval. (4) As-prepared cylindrical hydrogel which was cut into disks (with a diameter of 20 mm and thickness of 1 mm) was used to perform a time sweep test with 1% constant strain and a constant frequency of 10 rad/s at 25 °C. Then, the hydrogel was cut into two pieces, and after obtained self-healed hydrogel, the healed cylindrical hydrogel was then used to perform the time sweep test again. 2.11. Cytocompatibility Evaluation of the Hydrogels. To investigate their cytocompatibility of the hydrogels, a direct contact method was used to test their toxicity on C2C12 and L929 cells. Murine myoblast cells (C2C12 cells) and fibroblasts cell lines (L929 cells) were purchased from ATCC (American Type Culture Collection). The cells were cultured in Dulbecco’s Modified Eagle Medium (DMEM, GIBCO) with 10% (v/v) fetal bovine serum, 100 U/mL penicillin and 100 mg/mL streptomycin in an incubator with flowing air containing 5% CO2 at 37 °C. Cells were seeded on a 24-well plate (Costar) with a density of 8000 cells/cm2. The hydrogels were put into the wells after the cells adhered to plate.

⎛ 1 ⎞ σ=⎜ ⎟ ⎝ tR s ⎠ where t represents the thickness of the hydrogel and Rs is the sheet resistance of the hydrogel. The hydrogel conductivity was measured under different temperatures, and the temperature was controlled by a benchtop temperature controller (Model WT-0000-13S, Weitu, Shanghai, China). 2.9. Compression and Cycling Test and Tensile Stress−Strain Test. As prepared hydrogels (swollen in DI water) were first frozen and then cut into the cylindrical shape (∼8 mm high × 1.1 mm in diameter) for compression testing at 25, 30, and 40 °C, respectively. The test was investigated on a rheometer (Model DHR-2, TA Instruments) with a speed of 6 mm/min at 70% strain and then recovered to 0% strain with a speed of 6 mm/min. This cycle was repeated for 10 times to determine the compressive and recovery properties. The mechanical tensile stress− strain test was carried out by a MTS Criterion 43 tensile test machine equipped with a 50 N tension sensor at room temperature. All the hydrogel samples were cut into stripes (30 mm in length × 6 mm in width × 200 μm in thickness). The tensile strength, elongation at break, and modulus were obtained at a crosshead rate of 5 mm/min (at least triplicate for each sample). 2.10. Rheological Property of the Hydrogels. The rheological measurements of the hydrogels were performed by using a rheometer (Model DHR-2, TA Instruments) for four different methods: (1) The storage modulus (G′) and loss modulus (G″) of hydrogels were determined under oscillation frequency mode. The 1732

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Figure 3. (A) Temperature-dependent swelling ratios of hydrogels, (B) deswelling profiles at 50 °C, and (C) reswelling profiles at 25 °C. (D−J) SEM images of poly(NIPAM-co-β-CD) (panels (D and H)), poly(NIPAM-co-β-CD)/CNT (panels (E and I)), and poly(NIPAM-co-β-CD)/CNT/PPY hydrogel (panels (F and J)). Panels (D), (E), and (F) shows images of hydrogel at 25 °C and panels (H), (I), and (J) shows images of the hydrogel at 50 °C, respectively. Alamar blue assay (Molecular Probes) was used to evaluate the proliferation of cells after cultivation for 1, 2, and 3 days, respectively. The C2C12 and L929 cells were incubated in a medium containing 10% (v/v) Alamar Blue dye at 37 °C with 5% CO2 for 4 h. Then, 100 μL medium of each group was read by a SpectraMax fluorescence microplate reader (Molecular Devices) by using exciting wavelength of 530 nm and emission wavelength of 600 nm. After cultivation for 3 days, live/dead tests were performed after the samples were washed with phosphate buffer saline (PBS) for three times. Live/dead reagents (Ethidium homodimer-1 (0.5 μM) and calcein AM (0.25 μM)) (Molecular Probes) were added to the samples for 45 min. Then, cell viability was observed by an inverted fluorescence microscope (Model IX53, Olympus). The TCP group was used as a control group. 2.12. Statistical Analysis. The data were expressed as mean ± standard deviation. The Student’s t-test was used to evaluate the statistical significance, and it was considered to be significant when p < 0.05.

S1 and S2 in the Supporting Information. Compared with NIPAM and β-CD spectra, the hydrophobic aliphatic proton signals of isopropyl in the 1H NMR spectrum of NIPAM/β-CD shifted to a lower field and the proton signals of H-3 and H-5 in β-CD shifted to a higher field, indicating that NIPAM molecule was inserted into the cavity of β-CD molecules.41 The 2D NOESY NMR spectrum showed obvious cross peaks of the inner protons (H-3, H-5) of the β-CD with the protons of the isopropyl group of NIPAM, indicating that the corresponding protons were correlated to each other. Second, during the copolymerization of β-CD and NIPAM, CNT dispersion was incorporated into the matrix with PF127 diacrylate as a surfactant, and the conductive hydrogels poly(NIPAM-co-βCD)/CNT were prepared. Third, the highly conductive hydrogels poly(NIPAM-co-β-CD)/CNT/PPY were obtained via deposition of PPY nanoparticles on the surface of poly(NIPAM-co-β-CD)/CNT by a in situ polymerization of pyrrole. The chemical structure, composition and morphology of the hydrogels were investigated by FT-IR spectra and SEM images. The chemical structure of the hydrogels was characterized by FT-IR spectra (Figure 2B). From the curve of poly(NIPAM-coβ-CD), typical peaks at 3448 and 1644 cm−1 were assigned to N−H stretching vibration and carbonyl amide in NIPAM, and the peak at 1060 cm−1 corresponded to the C−O−C stretching vibration. Furthermore, the peak at 810 cm−1, which is assigned to double bonds of CC, disappeared in the curve of poly(NIPAM-co-β-CD), which indicated that AC-β-CD was copolymerized with NIPAM. As shown in poly(NIPAM-co-βCD)/CNT/PPY curve, the absorption peak at 1538 cm−1 was attributed to the pyrrole ring vibration, and peaks at 1045 and 1438 cm−1 were assigned to the in-plane deformation of N−H

3. RESULTS AND DISCUSSION 3.1. Preparation of Electrically Conductive Hybrid Hydrogels. Self-healing hydrogels have been extensively studied.48−50 However, self-healing hydrogels with conductivity and thermosensitivity have been rarely reported.50 In this work, the self-healing conductive hydrogels with multifunctional properties were designed and synthesized as shown in Figure 1. First, β-CD was chemically functionalized with vinyl groups, and then was copolymerized with a thermoresponsive monomer NIPAM via free radical polymerization (Figure 1A). The β-CD and NIPAM served as host and guest molecules, respectively. The host−guest interactions between NIPAM and β-CD would endow the hydrogels with good self-healing properties, and the host−guest interactions were confirmed by 1H NMR and 2D NOESY NMR spectra, as shown in Figure 2A, as well as Figures 1733

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Figure 4. (A) Photographs of compression and tension process for poly(NIPAM-co-β-CD)/CNT/PPY hydrogels. (B, C, and D) Compression and tension stress strain curves of hydrogels at strains from 10% to 70%. (E, F, and G) Compression and tension stress strain curves cycles of hydrogels at 70% strain. (H, I, and J) Rheology profiles of the hydrogels. (K) Mechanical properties of the hydrogels as determined by tensile testing.

cm−1 (−NH- stretching), 1644 cm−1 (amide band I) and 1542 cm−1 (amide band II) in poly(NIPAM-co-β-CD) curve showed no wavenumber shifts compared to pure PNIPAM curve. From the 1H NMR results of β-CD, NIPAM and β-CD/NIPAM in Figure S1, no obvious chemical shifts of − NH− in β-CD/ NIPAM complex compared to NIPAM was observed, indicating that β-CD had negligible influence on the inter- and intrahydrogen bonding of the NIPAM. Furthermore, the DSC measurement (Figure S3B) of PNIPAM polymer and poly(NIPAM-co-β-CD) hydrogel was carried out to study the influence of β-CD decoration on thermal-responsive temperature of PNIPAM based hydrogel. As shown in Figure S3B, the VPTT difference of PNIPAM polymer and poly(NIPAM-co-βCD) hydrogel was very small (0.6 °C), also indicating minor influence of copolymerization on VPTT change of PNIPAM. Therefore, all these FT-IR, NMR and DSC results demonstrated that the thermal-responsive behavior of poly(NIPAM-co-β-CD) hydrogel was not obviously influenced by β-CD decoration. This might be because the β-CD content in the hydrogels was very low with the molar ratio of β-CD to NIPAM = 1:95. These results agreed with some other reports in which the decoration of NIPAM chain exhibited little influence on its thermalresponsibility.52,53

bond and vibration of CC bond of pyrrole ring, respectively,51 which are the characteristic peaks of PPY. These results indicated that the PPY was formed in hydrogel matrix and the hybrid hydrogels were successfully obtained. From the SEM images, both the poly(NIPAM-co-β-CD) and poly(NIPAM-co-β-CD)/CNT hydrogels exhibited macroporous structure with a pore size of ∼200 μm (Figures 2C and 2D), which could allow large deformation of the hydrogel. The poly(NIPAM-co-β-CD) hydrogels showed a very smooth surface, as shown in Figure 2F. When CNT was incorporated into the hydrogels matrix (Figure 2G), the CNT formed the welldefined mesh network structure to act as the conducting pathway in the hydrogel matrix. After PPY aggregates were deposited, the porous morphology of the hydrogels was not affected (see Figure 2E), and a network of PPY nanoaggregates several hundred nanometers in size were loaded in the hydrogel matrix (Figure 2H), which could facilitate the transportation of electrons. 3.2. Swelling Behavior and Deswelling Behavior of the Hydrogels. The influence of copolymerization reaction on the thermal responsive behavior of PNIPAM based hydrogel was first studied by FT-IR, 1 H NMR and DSC measurement. From the FT-IR results of PNIPAM and poly(NIPAM-co-β-CD) in Figure S3A, the characteristic peaks of -NH- (in −CO-NH−) at 3448 1734

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that they were compressible and reversible. Furthermore, it was indicated that the elasticity of hydrogels was quite stable and well-maintained after 10 cycles without macroscopic fracture. Even though there were hysteresis loops (indicating dissipation) existing during compression and relaxation curves, it did not negatively affect the recovery behavior of the hydrogels. The mechanism of good resilience and fast recovery property of hydrogels can be explained by the elastic macroporous and soft− hard bicontinuous network structure of poly(NIPAM-co-βCD)/CNT/PPY hydrogel.45 The network comprised of hard CNT and soft PNIPAM coil chain, and CNT played as physical cross-linkers and soft PNIPAM coil chain could form a good resilient network preventing the mechanical failure of hydrogel, as well as the fracture of rigid PPY nanoaggregates. In addition, after bringing in rigid conductive components (CNT/PPY) in the hydrogel matrix, there was an obvious increase of compressive stress at 70% strain from 2.9 kPa (poly(NIPAMco-β-CD)) to 10.2 kPa (poly(NIPAM-co-β-CD)/CNT) and to 20.5 kPa (poly(NIPAM-co-β-CD)/CNT/PPY), demonstrating enhanced compressive stress of hybrid hydrogels compared to poly(NIPAM-co-β-CD) hydrogel, and the value of compressive stress at 70% strain was higher than previously reported PNIPAM gradient porous elastic hydrogels.59 The mechanical properties of the conductive hydrogels with different temperatures and water contents were also tested. The water content of the hydrogel would be changed correspondingly when the hydrogel was at different temperatures, because of the thermally sensitive nature of the hydrogel. Their mechanical properties at different temperatures, i.e., different water contents, is shown in Figure S4 in the Supporting Information. There was an obvious increase of the compression force with the increase of temperature when compressed to the same strain, and the possible reason was that the size of hydrogels would shrink and the amount of water released from the hydrogel with the temperature increases, especially upon their VPTT. In addition to compression and recovery properties, viscoelasticity is another characteristic mechanical property of polymeric hydrogels, and it reflects the ability of storage and dissipation of energy for hydrogels.60 The storage modulus (G′) and loss modulus (G″) of as-prepared hydrogels were first tested by oscillation−frequency sweeping mode. As demonstrated in Figures 4H−J, the storage modulus of poly(NIPAM-co-β-CD), poly(NIPAM-co-β-CD)/CNT, and poly(NIPAM-co-β-CD)/ CNT/PPY hydrogels were 130, 185, and 357 Pa, respectively, and it was obvious that the storage modulus curves and the loss modulus curves for all of hydrogels were not crossed with the increase of angular frequency, demonstrating stable mechanical properties during suitable shear rate range, and there was an enhanced modulus of G′ and G″ after bringing in rigid chains in the hydrogel substrate. Furthermore, the poly(NIPAM-co-βCD)/CNT and poly(NIPAM-co-β-CD)/CNT/PPY hydrogels still demonstrated good flexibility, despite the existence of rigid CNT or PPY chains. The possible reason was that the mechanical properties of bicontinuous hydrogels were dominated by the soft nonconductive coil chains. The tensile testing for these self-healing conductive hydrogels was also carried out as shown in Figure S5 in the Supporting Information, and the modulus, tensile stress, and elongation-atbreak results of the hydrogels are shown in Figure 4K. The poly(NIPAM-co-β-CD) hydrogel exhibited lower modulus (10.0 kPa) than poly(NIPAM-co-β-CD)/CNT (62.4 kPa) and poly(NIPAM-co-β-CD)/CNT/PPY (93.0 kPa) hydrogel. With the incorporation of rigid conductive components in the hydrogel

The characteristic thermoresponsive properties of PNIPAM hydrogel usually exhibited sharp phase transition and rapid swelling/deswelling rate.54,55 Thermal responsive and selfhealing properties of the poly(NIPAM-co-β-CD) hydrogel should not be negatively affected after bringing conductive CNT and PPY.56 The temperature-dependent swelling ratios from 25 °C to 50 °C, swelling behavior at 25 °C, and deswelling behavior at 50 °C test results are shown in Figure 3. The poly(NIPAM-co-β-CD) hydrogels exhibited similar temperature-dependent swelling ratios, compared to the pure PNIPAM hydrogels. There was an obvious sharp decrease of the swelling ratios from 32.9 to 16.6 when the temperature increased from 25 °C to 50 °C, and the reason is that the isopropyl groups in NIPAM became hydrophobic upon its VPTT (33.2 °C) and water outflow of the hydrogel matrix. After incorporation of CNT and PPY, the hybrid hydrogels exhibited lower swelling ratios, compared to the poly(NIPAM-co-β-CD) hydrogels. The CNT and PPY were hydrophobic components and increased the gel weight in dry state, and, as a result, the swelling ratios decreased. However, the hybrid hydrogels still had a swelling ratio from 23.2 to 17.7 for poly(NIPAM-co-β-CD)/CNT hydrogel and 23.0 to 14.9 for poly(NIPAM-co-β-CD)/CNT/ PPY hydrogel from 25 °C to 50 °C, respectively, which still exhibited a large and sharp phase transition. Apart from the temperature-dependent swelling ratios, the thermal responsive rate is also an important property for thermoresponsive hydrogels. The test results involving deswelling kinetics at 50 °C and swelling kinetics at 25 °C are shown in Figures 3B and 3C. The deswelling rate of all hydrogels, according to the change in temperature was fast, because of the large pore size and high porosity of hydrogel,57 and it only took 10 min to lose 33%, 26%, and 25% of water for the poly(NIPAMco-β-CD), poly(NIPAM-co-β-CD-co)/CNT, and poly(NIPAMco-β-CD)/CNT/PPY hydrogel, respectively. While the swelling rate of the hydrogels was desirable, it took ∼480 min to reswell to their original 87 wt %, 92 wt %, and 90 wt %. Moreover, the rate of swelling process was faster than that previously reported for PNIPAM/graphene conductive aerogel.58 Moreover, the morphology of porous structure of the hydrogel at 25 and 50 °C were also recorded to demonstrate their swelling and deswelling behavior. As shown in Figures 3D, 3E, and 3F, these images showed the porous structure of poly(NIPAM-co-βCD), poly(NIPAM-co-β-CD)/CNT, and poly(NIPAM-co-βCD)/CNT/PPY hydrogel, respectively, at 25 °C. Figures 3H−3J exhibited the porous structure of hydrogel at 50 °C. Compared to the images of hydrogels at 25 and 50 °C, it was obvious that the hydrogel had a larger pore size at 25 °C. This phenomenon further confirmed that the pore size of hydrogel was contracted in the 50 °C deswelling process. In summary, these hydrogels exhibited rapid, stable thermoresponsive ability and decent size changes upon temperature changes. 3.3. Mechanical Properties of the Hydrogels. Apart from the thermosensitive property of the hydrogels, the mechanical properties of the hydrogels were comprehensively tested. First, we investigated their compression and recovery properties. The photograph in Figure 4A demonstrated the good reversibility of hydrogel during compression and relaxation. Furthermore, as demonstrated in Figures 4B−G, when they endured external compression, the macroporous structure of the hydrogels could be deformed and compressed, and they could recover to their original shape after the loading was released. The narrow gap between the first compression/relaxation and last compression/ relaxation curve of hydrogels for 10 cycles further demonstrated 1735

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Figure 5. Temperature change of (A) poly(NIPAM-co-β-CD)/CNT hydrogels and (B) poly(NIPAM-co-β-CD)/CNT/PPY hydrogels after NIR light exposure; photographs of (C) nonconductive hydrogel and (D and E) conductive poly(NIPAM-co-β-CD)/CNT/PPY hydrogel for the NIR light on and off process. It was obvious that the hydrogels shrank significantly, both in diameter and height, when they were exposed to NIR light. Scale bar = 5 mm. (F) Photographs of potential application as an NIR-light-responsive valve for conductive hydrogel poly(NIPAM-co-β-CD)/CNT/PPY.

increased under laser exposure, and both poly(NIPAM-co-βCD)/CNT and poly(NIPAM-co-β-CD)/CNT/PPY hydrogels exhibited rapid and notable temperature change when the laser intensity was 1.25 W/cm2. The temperature change was ∼13.8 °C and ∼17.1 °C for poly(NIPAM-co-β-CD)/CNT and poly(NIPAM-co-β-CD)/CNT/PPY hydrogel, respectively, after 3 min of laser light exposure with a power of 1.25 W/ cm2, which was comparable to other reported PNIPAM-based hydrogel with NIR responsive property.59 The PNIPAM-based hydrogels were shrunk when the temperature surpassed their VPTT, exhibiting remarkable photothermal behavior. As demonstrated in Figures 5C, 5D, and 5E, the poly(NIPAM-coβ-CD)/CNT hydrogel displayed notable changes in size after laser light exposure. When the laser exposure was turned off, the shrinking phenomenon of the poly(NIPAM-co-β-CD)/CNT hydrogel ceased correspondingly, and then could gradually return to its original shape after water uptake. As a control, pure poly(NIPAM-co-β-CD) without CNT or PPY did not exhibit a change in shape after NIR laser light exposure. To further confirm that such shrinkage is a result of the water release from the hydrogels induced by NIR heating, the shrinking process of hydrogel exposed to NIR light was photographed as shown in Movie S1 in the Supporting Information. It was obvious that the water gradually released from the conductive hydrogel (released water dyed by crystal violet) when it was exposed to NIR light for

matrix, the moduli of the conductive hydrogels increased accordingly. Importantly, the elongation-at-break of poly(NIPAM-co-β-CD) hydrogel could reach to 1086%, indicating its superior stretchability. Although the elongation-at-break of conductive hydrogels decreased accordingly with incorporation of conductive components in the hydrogel matrix; they still remained at a high level, at ∼581% (poly(NIPAM-co-β-CD)/ CNT) and ∼515% (poly(NIPAM-co-β-CD)/CNT/PPY), respectively. Moreover, the strain of the hydrogel was much higher than that of other reported self-healing conductive gels.24,42 These tensile stress−strain test results further indicated that these hydrogels had excellent flexibility, elasticity, and stretchability. 3.4. Photothermal Properties of Hydrogels Triggered by Near-Infrared (NIR) Light. It has been reported that conductive nanoaggregates or polymers such as CNT or PPY possess the ability to absorb NIR light and transform NIR light to heat effectively.59,61,62 Therefore, it would be feasible that polymeric hydrogels could also exhibit photothermal properties during the incorporation of these conductive components into the hydrogel.63,64 As demonstrated in Figures 5A and 5B, the photothermal behavior of these hydrogels were tested. Obviously, there was no notable temperature change when the laser light intensity was 0.05). This result indicated that hydrogels do not negatively affect the cell adhesion. After two days of cultivation, the cell numbers of L929 fibroblasts cultured in hydrogel groups and TCP groups were similar to each other (p > 0.05), and L929 cells in the hydrogel groups and TCP groups showed significantly higher cell proliferation (p < 0.05) from day 1 to day 2. Moreover, the L929 cell number was obviously increased from day 2 to day 3 (p < 0.05). Similarly, C2C12 myoblast cells in the hydrogel groups and TCP groups showed significantly higher cell proliferation (p < 0.05) from day 1 to day 2 and from day 2 to day 3. Furthermore, the cell number for poly(NIPAM-co-β-CD)/CNT and poly(NIPAM-co-β-CD)/

CNT/PPY was >80% of that on TCP. In summary, these hydrogels showed good cytocompatibility in vitro.

4. CONCLUSIONS A conductive elastic flexible multifunctional hydrogels with selfhealing ability based on β-CD, NIPAM, CNT, and PPY have been successfully prepared. After loading conductive PPY nanoaggregates in hydrogel substrates, the hybrid hydrogels showed high conductivity and excellent self-healing properties and good elasticity together. The self-healing of poly(NIPAM-coβ-CD)/CNT/PPY hydrogel was mainly from supramolecular host−guest interaction between the β-CD and NIPAM in the system. Moreover, these conductive hydrogels exhibited rapid responsive rate both to heat and NIR light. Particularly, we demonstrated these multifunctional flexible conductive hydrogels possess great potential applications in pressure-dependent sensors, large-scale human motion monitoring sensors, and selfhealing electronic devices. Cytotoxicity test demonstrated that the hydrogels showed no toxicity for both L929 cells and C2C12 cells. Because of their excellent properties, it can be anticipated that these conductive hydrogels have great potential for a variety of applications in intelligent electronic devices and biomedical fields.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.chemmater.8b00008. 1740

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Chemistry of Materials H NMR spectrum, 2D NOESY NMR spectrum of β-CD/ NIPAM, FT-IR spectrum of the hydrogels, compression and tension curves of hydrogels at different temperature, representative tensile stress−strain curves, temperaturedependent conductivity of hydrogel, and self-healing behavior of hydrogel (PDF) Movie S1 (AVI) Movie S2 (AVI) Movie S3 (AVI) Movie S4 (AVI) Movie S5 (AVI)

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(12) Zhao, X.; Zhang, M. Y.; Guo, B. L.; Ma, P. X. Mussel-inspired injectable supramolecular and covalent bond crosslinked hydrogels with rapid self-healing and recovery properties via a facile approach under metal-free conditions. J. Mater. Chem. B 2016, 4, 6644−6651. (13) Burnworth, M.; Tang, L. M.; Kumpfer, J. R.; Duncan, A. J.; Beyer, F. L.; Fiore, G. L.; Rowan, S. J.; Weder, C. Optically healable supramolecular polymers. Nature 2011, 472, 334−U230. (14) Wang, Q.; Mynar, J. L.; Yoshida, M.; Lee, E.; Lee, M.; Okuro, K.; Kinbara, K.; Aida, T. High-water-content mouldable hydrogels by mixing clay and a dendritic molecular binder. Nature 2010, 463, 339− 343. (15) Nakahata, M.; Takashima, Y.; Yamaguchi, H.; Harada, A. Redoxresponsive self-healing materials formed from host-guest polymers. Nat. Commun. 2011, 2, 511. (16) Liao, X. J.; Chen, G. S.; Liu, X. X.; Chen, W. X.; Chen, F.; Jiang, M. Photoresponsive pseudopolyrotaxane hydrogels based on competition of host-guest interactions. Angew. Chem., Int. Ed. 2010, 49, 4409−4413. (17) Wei, P. F.; Yan, X. Z.; Huang, F. H. Supramolecular polymers constructed by orthogonal self-assembly based on host-guest and metalligand interactions. Chem. Soc. Rev. 2015, 44, 815−832. (18) Yu, G. C.; Jie, K. C.; Huang, F. H. Supramolecular amphiphiles based on host-guest molecular recognition motifs. Chem. Rev. 2015, 115, 7240−7303. (19) Guan, Y.; Zhao, H. B.; Yu, L. X.; Chen, S. C.; Wang, Y. Z. Multistimuli sensitive supramolecular hydrogel formed by host-guest interaction between PNIPAM-Azo and cyclodextrin dimers. RSC Adv. 2014, 4, 4955−4959. (20) Bai, X.; Lu, S. Y.; Cao, Z.; Gao, C. M.; Duan, H. G.; Xu, X. B.; Sun, L.; Gao, N. N.; Feng, C.; Liu, M. Z. Self-reinforcing injectable hydrogel with both high water content and mechanical strength for bone repair. Chem. Eng. J. 2016, 288, 546−556. (21) Zhao, J.; Zhao, X.; Guo, B. L.; Ma, P. X. Multifunctional interpenetrating polymer network hydrogels based on methacrylated alginate for the delivery of small molecule drugs and sustained release of protein. Biomacromolecules 2014, 15, 3246−3252. (22) Ma, C.; Shi, Y.; Pena, D. A.; Peng, L.; Yu, G. H. Thermally responsive hydrogel blends: a general drug carrier model for controlled drug release. Angew. Chem., Int. Ed. 2015, 54, 7376−7380. (23) Guo, B. L.; Glavas, L.; Albertsson, A. C. Biodegradable and electrically conducting polymers for biomedical applications. Prog. Polym. Sci. 2013, 38, 1263−1286. (24) Shi, Y.; Wang, M.; Ma, C. B.; Wang, Y. Q.; Li, X. P.; Yu, G. H. A Conductive self-healing hybrid gel enabled by metal-ligand supramolecule and nanostructured conductive polymer. Nano Lett. 2015, 15, 6276−6281. (25) Dong, R. N.; Zhao, X.; Guo, B. L.; Ma, P. X. Self-Healing conductive injectable hydrogels with antibacterial activity as cell delivery carrier for cardiac cell therapy. ACS Appl. Mater. Interfaces 2016, 8, 17138−17150. (26) Zhao, X.; Li, P.; Guo, B. L.; Ma, P. X. Antibacterial and conductive injectable hydrogels based on quaternized chitosan-graft-polyaniline/ oxidized dextran for tissue engineering. Acta Biomater. 2015, 26, 236− 248. (27) Wang, L.; Wu, Y. B.; Guo, B. L.; Ma, P. X. Nanofiber yarn/ hydrogel core-shell scaffolds mimicking native skeletal muscle tissue for guiding 3d myoblast alignment, elongation, and differentiation. ACS Nano 2015, 9, 9167−9179. (28) Wu, Y. B.; Wang, L.; Guo, B. L.; Ma, P. X. Interwoven aligned conductive nanofiber yarn/hydrogel composite scaffolds for engineered 3d cardiac anisotropy. ACS Nano 2017, 11, 5646−5659. (29) Cong, H. P.; Wang, P.; Yu, S. H. Stretchable and self-healing graphene oxide-polymer composite hydrogels: a dual-network design. Chem. Mater. 2013, 25, 3357−3362. (30) Zhao, X.; Wu, H.; Guo, B. L.; Dong, R. N.; Qiu, Y. S.; Ma, P. X. Antibacterial anti-oxidant electroactive injectable hydrogel as selfhealing wound dressing with hemostasis and adhesiveness for cutaneous wound healing. Biomaterials 2017, 122, 34−47. (31) Tee, B. C. K.; Wang, C.; Allen, R.; Bao, Z. N. An electrically and mechanically self-healing composite with pressure- and flexion-sensitive

AUTHOR INFORMATION

Corresponding Author

*Tel.:+86-29-83395363. Fax: +86-29-83395131. E-mail: [email protected]. ORCID

Baolin Guo: 0000-0001-6756-1441 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The National Natural Science Foundation of China (Grant Nos. 51673155 and 21304073) and “The Fundamental Research Funds for the Central Universities”, and Xi’an Jiaotong University are acknowledged for financial support of this work.

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REFERENCES

(1) Wu, D. Y.; Meure, S.; Solomon, D. Self-healing polymeric materials: A review of recent developments. Prog. Polym. Sci. 2008, 33, 479−522. (2) Wu, M.; Johannesson, B.; Geiker, M. A review: Self-healing in cementitious materials and engineered cementitious composite as a selfhealing material. Constr. Build. Mater. 2012, 28, 571−583. (3) Qu, J.; Zhao, X.; Ma, P. X.; Guo, B. L. pH-responsive self-healing injectable hydrogel based on N-carboxyethyl chitosan for hepatocellular carcinoma therapy. Acta Biomater. 2017, 58, 168−180. (4) Guo, B. L.; Ma, P. X. Synthetic biodegradable functional polymers for tissue engineering: A brief review. Sci. China: Chem. 2014, 57, 490− 500. (5) Huynh, T. P.; Sonar, P.; Haick, H. Advanced materials for use in soft self-healing devices. Adv. Mater. 2017, 29, 1604973. (6) Merindol, R.; Diabang, S.; Felix, O.; Roland, T.; Gauthier, C.; Decher, G. Bio-inspired multiproperty materials: strong, self-healing, and transparent artificial wood nanostructures. ACS Nano 2015, 9, 1127−1136. (7) Toohey, K. S.; Sottos, N. R.; Lewis, J. A.; Moore, J. S.; White, S. R. Self-healing materials with microvascular networks. Nat. Mater. 2007, 6, 581−585. (8) Kakuta, T.; Takashima, Y.; Nakahata, M.; Otsubo, M.; Yamaguchi, H.; Harada, A. Preorganized hydrogel: self-healing properties of supramolecular hydrogels formed by polymerization of host guestmonomers that contain cyclodextrins and hydrophobic guest groups. Adv. Mater. 2013, 25, 2849−2853. (9) Shi, Y.; Ha, H.; Al-Sudani, A.; Ellison, C. J.; Yu, G. H. Thermoplastic elastomer-enabled smart electrolyte for thermoresponsive self-protection of electrochemical energy storage devices. Adv. Mater. 2016, 28, 7921−7928. (10) Cordier, P.; Tournilhac, F.; Soulie-Ziakovic, C.; Leibler, L. Selfhealing and thermoreversible rubber from supramolecular assembly. Nature 2008, 451, 977−980. (11) Wu, Y. B.; Wang, L.; Zhao, X.; Hou, S.; Guo, B. L.; Ma, P. X. Selfhealing supramolecular bioelastomers with shape memory property as a multifunctional platform for biomedical applications via modular assembly. Biomaterials 2016, 104, 18−31. 1741

DOI: 10.1021/acs.chemmater.8b00008 Chem. Mater. 2018, 30, 1729−1742

Article

Chemistry of Materials properties for electronic skin applications. Nat. Nanotechnol. 2012, 7, 825−832. (32) Bai, H.; Sheng, K. X.; Zhang, P. F.; Li, C.; Shi, G. Q. Graphene oxide/conducting polymer composite hydrogels. J. Mater. Chem. 2011, 21, 18653−18658. (33) Yang, Z. H.; Cao, Z.; Sun, H.; Li, Y. Composite films based on aligned carbon nanotube arrays and a poly(N-isopropyl acrylamide) hydrogel. Adv. Mater. 2008, 20, 2201−2205. (34) Guo, B. L.; Finne-Wistrand, A.; Albertsson, A. C. Facile synthesis of degradable and electrically conductive polysaccharide hydrogels. Biomacromolecules 2011, 12, 2601−2609. (35) Xu, Y. X.; Sheng, K. X.; Li, C.; Shi, G. Q. Self-Assembled graphene hydrogel via a one-step hydrothermal process. ACS Nano 2010, 4, 4324−4330. (36) Guo, B. L.; Huang, D. W.; Li, Q. X.; Sun, C. Y. Dynamics for generalized incompressible Navier−Stokes equations in R2. Adv. Nonlinear Stud. 2016, 16, 249−272. (37) Zhao, F.; Shi, Y.; Pan, L. J.; Yu, G. H. Multifunctional nanostructured conductive polymer gels: Synthesis, properties, and applications. Acc. Chem. Res. 2017, 50, 1734−1743. (38) Guo, B. L.; Sun, Y.; Finne-Wistrand, A.; Mustafa, K.; Albertsson, A. C. Electroactive porous tubular scaffolds with degradability and noncytotoxicity for neural tissue regeneration. Acta Biomater. 2012, 8, 144− 153. (39) Xie, M. H.; Wang, L.; Ge, J.; Guo, B. L.; Ma, P. X. Strong electroactive biodegradable shape memory polymer networks based on star-shaped polylactide and aniline trimer for bone tissue engineering. ACS Appl. Mater. Interfaces 2015, 7, 6772−6781. (40) Guo, B. L.; Finne-Wistrand, A.; Albertsson, A. C. Degradable and electroactive hydrogels with tunable electrical conductivity and swelling behavior. Chem. Mater. 2011, 23, 1254−1262. (41) Wu, Y. B.; Guo, B. L.; Ma, P. X. Injectable electroactive hydrogels formed via host guest interactions. ACS Macro Lett. 2014, 3, 1145− 1150. (42) Hur, J.; Im, K.; Kim, S. W.; Kim, J.; Chung, D. Y.; Kim, T. H.; Jo, K. H.; Hahn, J. H.; Bao, Z. A.; Hwang, S.; Park, N. Polypyrrole/agarosebased electronically conductive and reversibly restorable hydrogel. ACS Nano 2014, 8, 10066−10076. (43) Constantin, M.; Bucatariu, S.; Ascenzi, P.; Simionescu, B. C.; Fundueanu, G. Poly(NIPAAm-co-beta-cyclodextrin) microgels with drug hosting and temperature-dependent delivery properties. React. Funct. Polym. 2014, 84, 1−9. (44) Munk, T.; Baldursdottir, S.; Hietala, S.; Rades, T.; Nuopponen, M.; Kalliomaki, K.; Tenhu, H.; Rantanen, J.; Strachan, C. J. Investigation of the phase separation of PNIPAM using infrared spectroscopy together with multivariate data analysis. Polymer 2013, 54, 6947−6953. (45) Liu, Y. Q.; Xu, K. G.; Chang, Q.; Darabi, M. A.; Lin, B. J.; Zhong, W.; Xing, M. Highly flexible and resilient elastin hybrid cryogels with shape memory, injectability, conductivity, and magnetic responsive properties. Adv. Mater. 2016, 28, 7758−7767. (46) Xie, M. H.; Wang, L.; Guo, B. L.; Wang, Z.; Chen, Y. E.; Ma, P. X. Ductile electroactive biodegradable hyperbranched polylactide copolymers enhancing myoblast differentiation. Biomaterials 2015, 71, 158− 167. (47) Wu, Y. B.; Wang, L.; Guo, B. L.; Shao, Y. P.; Ma, P. X. Electroactive biodegradable polyurethane significantly enhanced Schwann cells myelin gene expression and neurotrophin secretion for peripheral nerve tissue engineering. Biomaterials 2016, 87, 18−31. (48) Yesilyurt, V.; Webber, M. J.; Appel, E. A.; Godwin, C.; Langer, R.; Anderson, D. G. Injectable self-healing glucose-responsive hydrogels with ph-regulated mechanical properties. Adv. Mater. 2016, 28, 86−91. (49) Bai, T.; Liu, S. J.; Sun, F.; Sinclair, A.; Zhang, L.; Shao, Q.; Jiang, S. Y. Zwitterionic fusion in hydrogels and spontaneous and timeindependent self-healing under physiological conditions. Biomaterials 2014, 35, 3926−3933. (50) Darabi, M. A.; Khosrozadeh, A.; Mbeleck, R.; Liu, Y. Q.; Chang, Q.; Jiang, J. Z.; Cai, J.; Wang, Q.; Luo, G. X.; Xing, M. Skin-inspired multifunctional autonomic-intrinsic conductive self-healing hydrogels

with pressure sensitivity, stretchability, and 3D printability. Adv. Mater. 2018, 30, 1705922. (51) Lu, Y.; He, W. N.; Cao, T.; Guo, H. T.; Zhang, Y. Y.; Li, Q. W.; Shao, Z. Q.; Cui, Y. L.; Zhang, X. T. Elastic, conductive, polymeric hydrogels and sponges. Sci. Rep. 2015, 4, 5792. (52) Jin, S. P.; Liu, M. Z.; Chen, S. L.; Gao, C. M. Synthesis, characterization and the rapid response property of the temperature responsive PVP-g-PNIPAM hydrogel. Eur. Polym. J. 2008, 44, 2162− 2170. (53) Rivero, R. E.; Molina, M. A.; Rivarola, C. R.; Barbero, C. A. Pressure and microwave sensors/actuators based on smart hydrogel/ conductive polymer nanocomposite. Sens. Actuators, B 2014, 190, 270− 278. (54) Zhang, C. L.; Cao, F. H.; Wang, J. L.; Yu, Z. L.; Ge, J.; Lu, Y.; Wang, Z. H.; Yu, S. H. Highly stimuli-responsive Au nanorods/poly(nisopropylacrylamide) (pnipam) composite hydrogel for smart switch. ACS Appl. Mater. Interfaces 2017, 9, 24857−24863. (55) Wang, J. F.; Lin, L.; Cheng, Q. F.; Jiang, L. A Strong bio-inspired layered pnipam-clay nanocomposite hydrogel. Angew. Chem., Int. Ed. 2012, 51, 4676−4680. (56) Shi, Y.; Ma, C. B.; Peng, L. L.; Yu, G. H. Conductive “Smart” hybrid hydrogels with pnipam and nanostructured conductive polymers. Adv. Funct. Mater. 2015, 25, 1219−1225. (57) Tokuyama, H.; Kanehara, A. Novel synthesis of macroporous Poly(n-isopropylacrylamide) hydrogels using oil-in-water emulsions. Langmuir 2007, 23, 11246−11251. (58) Qiu, L.; Liu, D. Y.; Wang, Y. F.; Cheng, C.; Zhou, K.; Ding, J.; Truong, V. T.; Li, D. Mechanically robust, electrically conductive and stimuli-responsive binary network hydrogels enabled by superelastic graphene aerogels. Adv. Mater. 2014, 26, 3333−3337. (59) Luo, R. C.; Wu, J.; Dinh, N. D.; Chen, C. H. Gradient porous elastic hydrogels with shape-memory property and anisotropic responses for programmable locomotion. Adv. Funct. Mater. 2015, 25, 7272−7279. (60) Chakraborty, P.; Bairi, P.; Roy, B.; Nandi, A. K. Improved mechanical and electronic properties of co-assembled folic acid gel with aniline and polyaniline. ACS Appl. Mater. Interfaces 2014, 6, 3615−3622. (61) Molina, M.; Wedepohl, S.; Calderon, M. Polymeric near-infrared absorbing dendritic nanogels for efficient in vivo photothermal cancer therapy. Nanoscale 2016, 8, 5852−5856. (62) Li, W.; Luo, R. C.; Lin, X. D.; Jadhav, A. D.; Zhang, Z. C.; Yan, L.; Chan, C. Y.; Chen, X. F.; He, J. F.; Chen, C. H.; Shi, P. Remote modulation of neural activities via near-infrared triggered release of biomolecules. Biomaterials 2015, 65, 76−85. (63) Li, W.; Wang, J. S.; Ren, J. S.; Qu, X. G. 3D Graphene oxidepolymer hydrogel: Near-infrared light-triggered active scaffold for reversible cell capture and on-demand release. Adv. Mater. 2013, 25, 6737−6743. (64) Zhu, C. H.; Lu, Y.; Peng, J.; Chen, J. F.; Yu, S. H. Photothermally sensitive poly(n-isopropylacrylamide)/graphene oxide nanocomposite hydrogels as remote light-controlled liquid microvalves. Adv. Funct. Mater. 2012, 22, 4017−4022. (65) Odent, J.; Wallin, T. J.; Pan, W. Y.; Kruemplestaedter, K.; Shepherd, R. F.; Giannelis, E. P. Highly elastic, transparent, and conductive 3D-printed ionic composite hydrogels. Adv. Funct. Mater. 2017, 27, 1701807. (66) Guarino, V.; Alvarez-Perez, M. A.; Borriello, A.; Napolitano, T.; Ambrosio, L. Conductive PANi/PEGDA macroporous hydrogels for nerve regeneration. Adv. Healthcare Mater. 2013, 2, 218−227. (67) Hao, G. P.; Hippauf, F.; Oschatz, M.; Wisser, F. M.; Leifert, A.; Nickel, W.; Mohamed-Noriega, N.; Zheng, Z. K.; Kaskel, S. Stretchable and semitransparent conductive hybrid hydrogels for flexible supercapacitors. ACS Nano 2014, 8, 7138−7146. (68) Pan, L. J.; Yu, G. H.; Zhai, D. Y.; Lee, H. R.; Zhao, W. T.; Liu, N.; Wang, H. L.; Tee, B. C. K.; Shi, Y.; Cui, Y.; Bao, Z. N. Hierarchical nanostructured conducting polymer hydrogel with high electrochemical activity. Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 9287−9292.

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