Self-healable mussel-mimetic nanocomposite hydrogel based on catechol-containing polyaspartamide and graphene oxide

Materials Science and Engineering C 69 (2016) 160–170

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Materials Science and Engineering C journal homepage: www.elsevier.com/locate/msec

Self-healable mussel-mimetic nanocomposite hydrogel based on catechol-containing polyaspartamide and graphene oxide Bo Wang, Young Sil Jeon, Ho Seok Park, Ji-Heung Kim ⁎ School of Chemical Engineering, Sungkyunkwan University, Suwon 440–746, Republic of Korea

a r t i c l e

i n f o

Article history: Received 23 February 2016 Received in revised form 8 June 2016 Accepted 22 June 2016 Available online 25 June 2016

a b s t r a c t Stimuli-responsive and self-healing materials have a wide range of potential uses, and some significant research has focused on cross-linking of hydrogel materials by means of reversible coordination bonding. The resulting materials, however, tend to have poor mechanical properties with pronounced weakness and brittleness. In this work, we present a novel mussel-inspired graphene oxide(GO)–containing hydrogel based on modified polyaspartamide with γ-amino butyric acid (GABA), 3.4-dihydroxyphenethylamine (DOPA), and ethanolamine (EA), termed PolyAspAm(GABA/DOPA/EA). Here both GO nanosheets and boric acid (H3BO3) act as cross-linkers, interacting with polar functional groups of the PolyAspAm(GABA/DOPA/EA). Compared to PolyAspAm(GABA/ DOPA/EA)/B3+ gel without GO, the same containing 5 wt% of GO yielded a 10-fold increase in both the storage and loss moduli, as well as 134% and 104% increases in the tensile and compressive strengths, respectively. In addition, the GO-containing polyaspartamide hydrogel exhibited rapid and autonomous self-healing property. Two types of bonding, boron–catechol coordination and strong hydrogen bonding interactions between PolyAspAm side chains and GO nanosheets, would impart the enhanced mechanical strength and good reversible gelation behavior upon pH stimulation to the hydrogel, making this biocompatible hydrogel a promising soft matter for biomedical applications. © 2016 Elsevier B.V. All rights reserved.

1. Introduction Hydrogels are a class of soft matter possessing three-dimensional polymeric networks and high water content. Hydrogels can be further classified as chemical hydrogels or physical hydrogels, according to whether covalent bonding or noncovalent interactions form their three-dimensional polymeric networks, respectively. Recently, some significant research has been focused on physical hydrogels; the noncovalent bonds in physical hydrogels can include hydrogen bonds, hydrophobic interactions, metal–ligand coordination bonding, or guest–host interactions [1–7]. These physical hydrogels can easily respond to the external environment, including stimuli such as temperature, pH, and light, and can have self-healing properties [8–10]. However, because of the low density of the polymer chains, low friction between the polymer chains, and weak bonding, most noncovalent hydrogels have poor mechanical properties, often restricting their further industrial and biomedical application [11].

⁎ Corresponding author E-mail address: [email protected] (J.-H. Kim).

http://dx.doi.org/10.1016/j.msec.2016.06.065 0928-4931/© 2016 Elsevier B.V. All rights reserved.

Self-healing is a fascinating property of materials to heal or repair their surface or internal damage autonomously and spontaneously. In recent years, there has been increasing interest in the field of selfhealing hydrogels, because more safe lifetime and environmental impact of synthetic materials can be achieved by self-healing ability, although self-healing hydrogels have very weak mechanical performance in general [12–14]. Marine mussels withstand high-energy wave impacts in rocky seashore habitats by fastening tightly to surfaces with tough and self-healing proteinaceous fibers called byssal threads, which are heavily decorated with DOPA, a catecholic functionality. In some studies, the catechol moiety of DOPA form strong, reversible interactions with metal ions, leading to the formation of rapid self-healing smart materials [15–17]. Boric acid is a typical Lewis acid, which can react with water to abstract OH− in aqueous media and convert the trigonal boron to an anionic tetrahedral geometry [18]. Under alkaline conditions, the boron atom has four coordinative bonds to form bis-complexes with diols from catechol groups. In our previous works, we exploited the reversible boron– catechol coordinative bonds to impart self-healing characteristics in dopamine-conjugated polyaspartamide gels with rather week mechanical properties [19].

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Significant approach used to form nanocomposite hydrogels with unique structures and high mechanical strength includes the addition of organic or inorganic nanofillers such as clays, carbon nanotubes, and cellulose. Graphene and graphene oxide have also been identified as nanofillers that can mechanically reinforce hydrogels. Graphene oxide (GO), a two-dimensional single-layer nanomaterial, is prepared from graphite by means of chemical oxidation and exfoliation [20–34]. GO can be stably dispersed in aqueous solutions owing to its various oxygen functional groups, including hydroxyl (\\OH), epoxy (\\C\\O\\C), carbonyl (\\C_O) and carboxyl (\\COOH) [35–42]. Moreover, depending on these functional groups, GO can make strong covalent or noncovalent interactions with polar small molecules or polymers, and also function as nanofillers to mechanically reinforce hydrogels [43–49]. Zhang et al. reported on a high-strength composite hydrogel prepared from GO and PVA by means of a freeze/thaw process [20]. The incorporation of GO in PVA hydrogels resulted in a significant increase of tensile and compressive strength. Without use of organic cross-linkers, GO nanosheets and calcium ions as double cross-linkers trigger the polar groups of the PAM side chains to form the double network with hydrogen bonding and coordination interactions [22]. Cong et al. have reported highly elastic and stretchable GO–PAM nanocomposite hydrogels with high tensile strengths and large stretchability; in these gels, a cross-linked double network is formed by Ca2 + ions and a chemical cross-linker [22]. Although many researchers have reported on GO-containing hydrogels with excellent mechanical characteristics, only a few reports have been devoted to highly stretchable smart hydrogels containing GO. Cong et al. also designed a novel kind of GO/PAACA hydrogel endowed with enhanced mechanical properties and self-healing capability [23]. Zhong and coworkers proposed a facile method for fabricating self-healing, super tough graphene oxide (GO)– poly(acrylic acid) (PAA) nanocomposite hydrogels by using Fe3+ ions as a cross-linker; the resulting GO–PAA nanocomposite hydrogels exhibit superior toughness, tensile strength, and stretchability [35]. Furthermore, these nanocomposite hydrogels exhibit good self-healing properties after being treated at 45 °C for 48 h. Sun and Wu have demonstrated dual thermal and pH response with good reversibility in hydrogels combining graphene and poly(N-isopropylacrylamine) (PNIPAM) [27]. In the present work, inspired by our previous studies, we prepared a novel GO-containing nanocomposite hydrogel based on GABA, DOPA, and EA-conjugated polyaspartamide, hereafter termed PolyAspAm(GABA/DOPA/EA). Polyaspartamides are promising watersoluble, nontoxic, nonantigenic, and biodegradable polymers and can be obtained from the aminolysis of polysuccinimide (PSI), which is easily prepared by thermal polycondensation of D,L-aspartic acid, the thermal polycondensation product of aspartic acid monomer. The hydrogel networks in GO/PolyAspAm(GABA/DOPA/EA)/B3+ are formed by GO nanosheets and boric acid as cross-linkers. The pH-responsive and adhesive catechol group can reversibly undergo gelation through metal boron–catechol coordinative bonding, and the polar functional groups of PolyAspAm(GABA/DOPA/EA) side chains should interact with oxygen-containing groups on the GO nanosheets by means of hydrogen bonding to reinforce the mechanical properties of the hydrogel. Both these types of reversible bonds would impart self-healing characteristics to the PolyAspAm gels.

2. Experimental section 2.1. Materials L-aspartic acid (98%+), ortho-phosphoric acid (98%), N,Ndimethylformamide (99.8% anhydrous, DMF), γ-aminobutyric acid (99%+), chlorotrimethylsilane (99%+), dopamine hydrochloride (DOPA), ethanolamine (99%, EA), dibutylamine (99.5%+), sodium hydrosulfite (ca. 85%), acetic acid (99%+), boric acid (99.5%+), and

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methanol (99.9%+) were purchased from Sigma–Aldrich. Acetone and ethyl ether were obtained from DaeJung Chemical Co. (Siheung, Korea). All other chemicals purchased were of sufficient quality and were used as received. 2.2. Synthesis of polysuccinimide (PSI) L-aspartic acid (30 g) and 98% ortho-phosphoric acid (30 g) (50:50 wt. ratio) were put into a round-bottom flask and mixed at room temperature. The mixture was heated slowly from room temperature to 180 °C under reduced pressure in about 30 min and then maintained at 180 °C for 4.5 h. The reaction mixture was then cooled and DMF was added to dissolve the product. The resulting solution was precipitated in excess water and the precipitate was washed several times with water to remove residual phosphoric acid until the solution reached pH 7. The product was finally dried at 70 °C in vacuum for 3 d to obtain PSI in white powder form. The molecular weight was estimated to be approximately 75,000 Da, as calculated from an empirical equation relating the solution viscosity to the molecular weight [50].

2.3. Synthesis of polyaspartamide derivatives, PolyAspAm(GABA/DOPA/EA) 2.3.1. Synthesis of γ-aminobutyric methyl ester hydrochlorides (GABAME) γ-Aminobutyric acid (0.01 mol) was weighed into a round-bottom flask and dissolved in 30 mL of methanol. Chlorotrimethylsilane (0.02 mol) was then added slowly to this solution with gentle magnetic stirring. The reaction mixture was stirred for 24 h at room temperature. After reaction, the solution was precipitated using ethyl ether. The filtered powder was washed with fresh ethyl ether several times and dried under vacuum. 2.3.2. Synthesis of PolyAspAm(GABA/DOPA/EA) PSI of 0.97 g (corresponding to 0.01 mol succinimide unit) was dissolved in 20 mL of DMF. GABAME of 6.5 mmol (0.66 g) and 6.5 mmol (1.1 mL) of dibutylamine (DBA) were dissolved in 20 mL of DMF. This solution was then added to the PSI solution under vigorous stirring at room temperature. After reaction for 5 d, 0.005 mol of DOPA and 0.005 mol of DBA were added. The reaction was carried out under a nitrogen atmosphere in the presence of 0.05 g sodium hydrosulfite. The reaction mixture was placed in an 80 °C water bath and stirred for 24 h. EA of 10 mol% excess was added slowly to the reaction mixture and stirred at room temperature for 24 h. The resulting mixture was precipitated in 300 mL of cold acetone, from which the product, PolyAspAm(GABA/DOPA/EA), was removed by filtration. The product was dispersed in a pH 10 solution of sodium hydroxide in distilled water; additional sodium hydroxide solution was dropped into the dispersion to maintain its pH at about 10. The mixture was stirred overnight and then hydrochloric acid was dropped into the solution until its pH stabilized at pH 4.0. The resulting solution was filtered, dialyzed, and then lyophilized to obtain solid polymer. 2.4. Gelation of PolyAspAm(GABA/DOPA/EA) with GO and boric acid PolyAspAm(GABA/DOPA/EA) samples of different graphene oxide contents were used for the preparation of aqueous solutions and reversible gels. As an example, 0.5 g of PolyAspAm(GABA/DOPA/EA) was dissolved in 3.5 mL of deionized water, into which a sufficient amount of B(OH)3 solution (catechol/B(OH)3 M ratio: 2.0) was then added. A 5 mg/mL GO solution (5 wt%) was then added; the GO in this solution was prepared by means of a modified Hummer's method (Fig. S.1 and S.2) [36,51]. The pH of the mixture was increased to the desired final pH of 9 by the addition of 0.1 N NaOH solution under a nitrogen blanket. The mixture was mechanically mixed to promote the formation of gel by means of B-catechol coordination bonding.

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2.5. Characterization techniques 2.5.1. Nuclear magnetic resonance 1 H NMR spectra of samples dissolved in dimethyl sulfoxide (DMSO) were acquired using a Unity Inova-500 (Varian, Palo Alto, CA, USA) spectrometer. 2.5.2. Fourier transform infrared spectroscopy The structures of the GO and of PolyAspAm derivatives were analyzed by means of Fourier transform infrared spectroscopy (FT-IR; Perkin Elmer System 2000 FT-IR). 2.5.3. Ultraviolet-visible spectroscopy UV–vis absorption data were recorded by using a spectroscope (SpectraMax M5, Molecular Devices, CA, USA); samples were contained in quartz cuvettes of 1 cm path length and were analyzed at room temperature. To prepare samples for analysis, solutions of 20 mg/mL PolyAspAm (GABA/DOPA/EA) with 5 wt% GO and a sufficient amount of B(OH)3 solution (2.0:1 catechol/B(OH)3 M ratio) were prepared. The solutions were increased in pH by means of adding NaOH solution under a nitrogen blanket, followed by stirring for 12 h and then diluting the solutions with buffer. 2.5.4. Thermogravimetric analysis Thermogravimetric analysis (TGA) was conducted in a TGA instrument (TGA 7, Perkin Elmer); samples were analyzed under nitrogen atmosphere and heated at the rate of 5 °C min−1. 2.5.5. X-ray diffractometry X-ray diffractometry (XRD) structural analyses of pure PolyAspAm(GABA/DOPA/EA), lyophilized GO5%–PolyAspAm(GABA/ DOPA/EA) /B3+ hydrogel, and GO were performed using an XRD instrument (Rigaku Rotaflex D/Max) equipped with a Cu Kα radiation source (λ = 1.54056 Å).

2.5.6. X-ray photoelectron spectroscopy X-ray photoelectron spectroscopy (XPS) analyses of GO and of lyophilized GO5%–PolyAspAm(GABA/DOPA/EA)/B3+ hydrogels were carried out using an XPS instrument (Auger Electronics, ESCA20000). 2.5.7. Scanning electronic microscopy The cross-sectional morphologies of PolyAspAm hydrogels were observed by means of high-resolution field emission scanning electron microscopy (FE-SEM, JEOL JSM-7401F); samples were prepared by means of quick quenching in liquid nitrogen followed by cross-sectioning. 2.5.8. Rheological properties The rheological properties of PolyAspAm hydrogels were measured using a Bohlin Rotational Rheometer (Malvern Instruments, UK) equipped with a temperature control system (Smart Swap, TA Instruments). Oscillatory shear testing of gels over a range of frequencies was performed at the constant strain of 1% to measure storage modulus (G′), loss modulus (G″), and complex viscosity at 25 °C. The selected strain (1%) was previously confirmed to be in the linear viscoelastic region (LVER). 2.5.9. Mechanical tests Tensile strength measurements were performed on a UTM(QC508E, Cometech, Taiwan) at a crosshead speed of 20 mm min−1; both GO5%–PolyAspAm(GABA/DOPA/EA)/B3 + and PolyAspAm(GABA/ DOPA/EA)/B3 + hydrogel samples were tested, with sample size of about 30 mm length, 8 mm width and 6 mm thickness. Compressive testing was conducted using the same instrument; the hydrogel samples tested were of 15 mm diameter and 10 mm height. Both tensile and compressive tests were conducted at 25 °C. 2.5.10. Water content To get the water content of hydrogels, we used gravimetric determination of hydrogels according to weight loss upon drying. The hydrated specimen was weighted as quickly as possible to avoid loss of water

Scheme 1. Synthesis of PolyAspAm(GABA/DOPA/EA).

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from the sample by evaporation and then lyophilized to obtain dry gel. Water content was obtained according to the equation water contentð%Þ ¼

ðW h −W d Þ  100 Wh

where Wd is the weight of dried gel and Wh is the weight of hydrated gel. 3. Results and discussion 3.1. Synthesis and characterization of PolyAspAm(GABA/DOPA/EA) As shown in Scheme 1, novel PolyAspAm(GABA/DOPA/EA) derivatives were synthesized from PSI by means of successive aminolysis

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reaction with quantitative γ-aminobutyric acid (GABA), dopamine hydrochloride (DOPA), and ethanolamine (EA). An 1H NMR spectrum and chemical structure assignments of γ-aminobutyric methyl ester hydrochlorides (GABAME) in DMSO are shown in Fig. 1a. The methyl(ester) proton of GABAME yielded a peak at 3.7 ppm. The structure and composition of the PSI and PolyAspAm(GABA/DOPA/EA) were confirmed using 1H NMR spectroscopy Fig. 1b. The methine proton (at 5.3 ppm) of the initial succinimide ring disappeared completely the series of aminolysis reactions, suggesting a quantitative ring opening to produce the PolyAspAm derivatives. Peaks d, e, and f were assigned to the aromatic protons of the dopamine phenyl group, and peaks a, b, c and i, j were assigned to the methylene protons of the GABA and the EA pendant, respectively. The amount of each group in the PolyAspAm(GABA/DOPA/EA) copolymer was determined from the integration ratio between peaks a, b, and c (6.3–6.8 ppm) and b

Fig. 1. 1H NMR spectra of (a) GABAME, (b) PSI, and PolyAspAm(GABA/DOPA/EA).

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B. Wang et al. / Materials Science and Engineering C 69 (2016) 160–170 Table 1 Amount of each pendant group in the polyAspAm(GABA/DOPA/EA) copolymers. PolyAspAm

Content (mol%)

GABA DOPA Ethanolamine(EA)

31 19 50

As determined from 1H NMR analysis.

(1.6 ppm). Table 1 lists the composition of the PolyAspAm(GABA/DOPA/ EA) copolymer. 3.2. Preparation and characterization of polyaspartamide derivative nanocomposite hydrogel-containing catechol groups and graphene oxide GO–nanocomposite hydrogels were synthesized by adding GO dispersion (Fig. S.1 and S.2) and boric acid into PolyAspAm(GABA/DOPA/ EA) solution. Scheme 2 illustrates the structure of this novel PolyAspAm(GABA/DOPA/EA) hydrogel, including the boron crosslinking. As shown in Scheme 2a, compared to the dark red PolyAspAm/B3+ hydrogel, the color of GO5%–PolyAspAm/B3+ hydrogel was a characteristic black owing to the presence of GO that was incorporated through hydrogen bonds. Scheme 2c shows the general overall reactions, including both the addition reaction (with one ligand donor atom present in an unoccupied site on boron) and the substitution reaction (the second ligand donor atom displacing an OH− from boron). The boron is four-coordinate with bidentate catechol ligands. Based on the above theories, Scheme 2b shows two types of reversible hydrogen bonding and boron–catechol coordinative complexation in the PolyAspAm(GABA/DOPA/EA) hydrogel network. FT-IR spectra of graphene oxide (GO), PolyAspAm(GABA/DOPA/EA) polymer, and GO5%–PolyAspAm(GABA/DOPA/EA)/B3 + hydrogel was collected as shown in Fig. 2. The spectrum of GO powders showed characteristic bands at 3201.6, 1721.7, 1616.1, and 1061.9 cm−1 (Fig. 2a), which were respectively attributed to\\OH stretching vibration, C_O carbonyl stretching, aromatic C_C stretching vibration, and

Fig. 2. FT-IR spectra of (a) GO, (b) PolyAspAm(GABA/DOPA/EA) polymer, and (c) GO5%– PolyAspAm(GABA/DOPA/EA)/B3+ hydrogel.

asymmetric and symmetric C\\O stretching vibration in C\\O\\C groups; these results confirmed the synthesis of GO-containing carboxylic acid, epoxide, and hydroxide functional groups. In the spectrum of the GO5%–PolyAspAm(GABA/DOPA/EA)/B3+ hydrogel (Fig. 2c), weak absorption bands belonging to GO carbonyl at 1723.3 cm− 1 and GO epoxy C\\O at 1058.9 cm−1 were observed, owing to the low content of GO in the hydrogel. A broad band around 3294.5 cm−1 was assigned to \\OH and \\NH groups in the hydrogel. Characteristic absorption bands of amide I and amide II appeared at 1645.5 and 1529.4 cm− 1, and a band at 1179.8 cm−1 was assigned to C\\N stretching. In addition, the characteristic bands of amide I and phenolic C\\O\\H were observed to shift from 1635.4 to 1645.5 cm− 1 and from 1365.2 to 1362.3 cm−1, respectively, accompanied by considerable increases in their relative peak intensities. The shifts and increasing strengths of these bands suggested that GO and PolyAspAm(GABA/DOPA/EA) were

Scheme 2. (a) Photographs of PolyAspAm(GABA/DOPA/EA) hydrogel with and without GO. (b) Illustration of the bonding networks in GO5%–PolyAspAm(GABA/DOPA/EA)/B3+ hydrogel. (c) Equilibrium reactions between the catechol groups of PolyAspAm(GABA/DOPA/EA) and boric acid.

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Fig. 3. TGA curves of (a) powdery GO, (b) pure PolyAspAm(GABA/DOPA/EA) polymer, (c) lyophilized GO5%–PolyAspAm/B3+ hydrogel, and (d) lyophilized PolyAspAm/B3+ hydrogel.

intertwined via strong hydrogen bonding interactions between carboxyl and hydroxyl groups of PolyAspAm(GABA/DOPA/EA) chains and oxygen-containing groups on GO sheets. Furthermore, vibrations observed at 818.8 cm−1 were ascribed to the stretching vibrations of tetrahedral BO4, originating from boron–catechol coordinative complexation. Overall, these FT-IR results confirmed the synthesis of

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double-network PolyAspAm(GABA/DOPA/EA) hydrogel with GO and boric acid. To further confirm the presence of GO in the nanocomposite gel, the thermal properties of GO, PolyAspAm(GABA/DOPA/EA), and two lyophilized hydrogels of GO5%–PolyAspAm(GABA/DOPA/EA)/B3 + and PolyAspAm(GABA/DOPA/EA) /B3+ were investigated by means of TGA measurements (Fig. 3); samples of these four materials were heated from 25 to 600 °C at the rate of 10 °C min−1 under a nitrogen atmosphere. Under these conditions, GO first lost about 8% of its weight owing to evaporation of water molecules, and then lost about 32% of its weight from 180 to 250 °C owing to the loss of oxygen-containing functional groups. The measured weight losses during TGA were 48.5% of the GO, 81.3% of the pure PolyAspAm(GABA/DOPA/EA), 60.3% of the GO5%–PolyAspAm/B3 +, and 69.4% of the PolyAspAm/B3 +. GO5%– PolyAspAm/B3 + and PolyAspAm/B3 + showed similar patterns of weight loss during TGA, but the former showed increased thermal stability owing to the presence of GO. The residual weight of GO5%– PolyAspAm/B3+ hydrogel was higher than that of the PolyAspAm/B3+ hydrogel and that of the pure PolyAspAm(GABA/DOPA/EA) polymer, indicating that interactions between GO and the PolyAspAm matrix can improve the thermal stability of the GO–PolyAspAm/B3+ nanocomposite gels. X-ray diffraction analysis and X-ray photoelectron spectroscopy were conducted to further confirm the synthesis of PolyAspAm(GABA/ DOPA/EA) hydrogel with GO and boric acid and to analyze its chemical and physical structure. GO itself exhibited a characteristic XRD peak at 2θ of 11.2°, corresponding to the interlayer spacing of 9.5 Å, and an amorphous halo appeared in the XRD spectrum of pure

Fig. 4. (a) XRD patterns of pure PolyAspAm(GABA/DOPA/EA) polymer, lyophilized GO–PolyAspAm/B3+ hydrogel, and GO; (b) XPS spectra of GO and of GO5%–PolyAspAm/B3+ hydrogel; (c) deconvoluted C 1s XPS spectrum of GO; and (d) deconvoluted C 1 s XPS spectrum of GO5%–PolyAspAm/B3+ hydrogel.

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Fig. 5. FE-SEM images showing the morphologies of two lyophilized hydrogels, at the same magnification: (a) PolyAspAm(GABA/DOPA/EA)/B3+ and (b) GO5%–PolyAspAm(GABA/DOPA/ EA)/B3+.

PolyAspAm(GABA/DOPA/EA), with a maximum at 2θ of around 21.5° (Fig. 4a). The gel sample containing GO showed only a broad diffraction halo similar to that of PolyAspAm; the diffraction peak of GO did not appear. These XRD results suggested that the GO nanosheets were uniformly dispersed and intercalated within the polymer gels owing to the strong interactions between GO and PolyAspAm(GABA/DOPA/EA). The GO5%–PolyAspAm/B3+ nanocomposite hydrogel showed an N 1s peak at 399.6 eV, arising from amine groups in the PolyAspAm (Fig. 4b). The C 1s XRD peaks of the GO and of the GO-containing gel were deconvoluted; for GO, this revealed peaks centered at 284.6, 286.7, and 288.5 eV that were respectively assigned to C_C and/or C\\C bonds in aromatic rings, C\\OH (epoxy and alkoxy) groups, and O\\C_O groups (Fig. 4c). The deconvoluted C 1 s peak of GO– PolyAspAm/B3 + hydrogel showed three similarly located peaks at 284.6, 285.9, and 288.9 eV; however, the peak intensities were decreased dramatically, suggesting that most of the epoxy and hydroxyl functional groups were removed from the GO; an additional peak observed at 287.6 eV was assigned to the O_C\\NH group of PolyAspAm. To investigate the microstructure and morphology of the hydrogels, lyophilized samples of the PolyAspAm(GABA/DOPA/EA)/B3 + and GO5%–PolyAspAm(GABA/DOPA/EA)/B3+ gels were subjected to scanning electron microscopy (SEM) as shown in Fig. 5. The PolyAspAm(GABA/DOPA/EA)/B3+ sample exhibited a 3D flexible porous structure with pore sizes ranging from the submicrometer scale to several micrometers. We believe that in this material, the boron atom from boric acid forms four coordinative bonds with the diols from catechol groups, thereby forming a noncovalent cross-linking network. The lyophilized GO5%–PolyAspAm(GABA/DOPA/EA)/B3+ hydrogel showed a loose PolyAspAm/B3+-based network structure in which the pore walls were increased dramatically. This change in morphology may have arisen from the effect of PolyAspAm chains grafting onto the GO surfaces by means of hydrogen bonding interactions between GO and PolyAspAm(GABA/DOPA/EA). In many prior investigations on the reversible noncovalent catechol– boron bonds, oxidation of the catechol groups was a critical issue. UV– vis spectra of PolyAspAm(GABA/DOPA/EA) and GO were acquired, yielding further evidence of the presence of catechol–B3+ complexes. The UV–vis curve of pure PolyAspAm(GABA/DOPA/EA) showed only one peak at λmax = 280 nm, assigned to catechol groups; this peak decreased in intensity upon the gel's interaction with GO and boric acid at pH 5, indicating that catechol interacted partially with boric acid to form monocomplexes of B3+–DOPA (Fig. 6a). However, when the pH of the solution was increased from 5 to 9, the catechol peak at 280 nm and a GO absorption peak at 302 nm both disappeared, suggesting the formation of hydrogen bonds between GO and the PolyAspAm(GABA/DOPA/ EA) side chains as well as coordinative complexation between boron and catechol groups at pH 9. Photographs showing the reversibility of

GO5%–PolyAspAm(GABA/DOPA/EA)/B3 + gel formation are given in Fig. 6b: the gel formed at pH 9 (picture 1) turned to a liquid after adjusting the pH to 5 (picture 2), and then the gelation occurred again (picture 3) when the pH was increased back to pH = 9. This observation suggests that the dynamic noncovalent network formed at pH 9 allows reversible gelation. 3.3. Self-healing properties It has been previously reported that dynamic complexation between B3 + and catechol coordination can allow the reversible formation of self-healing gels [19,52]. When GO was added to the PolyAspAm(GABA/DOPA/EA)/B3 + system, the resulting GO5%–

Fig. 6. (a) UV–vis absorbance spectra of GO, PolyAspAm(GABA/DOPA/EA), and PolyAspAm(GABA/DOPA/EA) including both GO and boric acid solution, at both pH 5 and 9. (b) Photographs illustrating the reversible formation of GO–PolyAspAm(GABA/ DOPA/EA)/B3+ hydrogel. The gel formed at pH 9 (❶) became liquid after its pH was adjusted to 5 (❷), and gelated again when the pH was returned to 9 (❸).

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between the connected gels after fusion, and the jointed parts after healing were strong enough to be stretched without fracturing by the tweezers as are shown in (c) and (d). When the healed gel was cut again into two pieces where it had originally been fractured, the same self-healing phenomenon was observed again, showing that the healing was both effective and repeatable. This result can be ascribed to the noncovalent reversible double-network of bonds in the gel: coordinative bonding between boron and catechol groups and hydrogen bonding between the polar functional groups of PolyAspAm(GABA/DOPA/ EA) side chains and oxygen-containing groups on the GO nanosheets. 3.4. Rheological properties of GO–PolyAspAm nanocomposite hydrogel

Fig. 7. Photographs giving evidence of self-healing: (a) sample cut into two pieces, (b) rejoined pieces, (c) healed sample, and (d) the extension of healed sample.

PolyAspAm/B3+ hydrogel also exhibited self-healing property, as demonstrated in Fig. 7. Namely, a piece of GO–PolyAspAm/B3+ gel was cut into two parts (a). Two pieces of fractured gels were placed into contact with each other and underwent autonomous and rapid healing without requiring any additional intervention (b). No obvious cut line was seen

To investigate the rheological behavior of GO–PolyAspAm(GABA/ DOPA/EA)/B3 + hydrogel, three hydrogel samples with different GO contents (2, 5, and 10 wt%) were subjected to dynamic mechanical analysis; G′ and G″ were measured over a range of frequencies at the constant strain of 1% and at the constant temperature of 25 °C. As shown in Fig. 8a, the storage moduli of these three gel samples were nearly constant, showing slight increases at higher frequencies. For all samples, G′ was always at least 10 times greater than G″, indicating an elastic rather than viscous nature, and a permanent network structure. Moreover, the storage and loss moduli of the nanocomposite hydrogels increased when the GO content was increased from 2 to 5 wt%, probably due to an increase in the cross-linking density. However, the further increase in the GO content to 10 wt% yielded decreased G′ and G″, indicating that there was an optimal extent of interaction between GO and PolyAspAm(GABA/DOPA/EA) side chains. Fig. 8b compares the moduli of two different hydrogel samples: the gel with 5 wt% GO content and

Fig. 8. (a, b) Dynamic rheological behaviors of PolyAspAm(GABA/DOPA/EA)/B3+ hydrogels having various GO contents; (c) complex viscosity curves of GO5%–PolyAspAm(GABA/DOPA/ EA)/B3+ and PolyAspAm(GABA/DOPA/EA)/B3+ hydrogels; and (d) moduli G′ and G″ versus temperature of the hydrogel containing 5% GO.

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that without GO. Both G′ and G″ of the GO-containing gel were more than 10 times those of the non-GO gel, indicating that the plentiful hydroxyl, carbonyl, and epoxy functional groups on the GO surface could form hydrogen bonds with the PolyAspAm(GABA/DOPA/EA) chains to form highly elastic nanocomposite hydrogel. In addition, comparing PolyAspAm(GABA/DOPA/EA)/B3 + hydrogel and PolyAspAm(DOPA/ EA) hydrogel shown in our previous paper [19], both of two hydrogels displayed almost same G′ and G′′ modulus, suggesting hydrogen bonds by GABA and EA from PolyAspAm(GABA/DOPA/EA) side chains have little effect on rheological performance of PolyAspAm(GABA/ DOPA/EA)/B3+ hydrogel. From the above, comparing the other hydrogen bonds in GO containing PolyAspAm(GABA/DOPA/EA)/B3+ hydrogel, hydrogen bonds between GO and PolyAspAm side chains showed main influence to increase the properties of hydrogel. To further verify the results presented above regarding the effect of GO, complex viscosity curves were prepared for both GO5%–PolyAspAm/B3 + and PolyAspAm/B3 + gel samples and are shown in Fig. 8c. The material showed dramatic decreases in viscosity under shear, typical behavior of a physically cross-linked hydrogel system. As expected, the viscosity of the GO-containing PolyAspAm gel was much greater than that of the hydrogel that did not contain GO. Because of their weakly interconnected networks, many hydrogels show unstable thermal properties and change to the sol state at higher temperatures. However, the GO-containing PolyAspAm(GABA/DOPA/EA)/B3+ hydrogel showed good thermal stability, as demonstrated by its invariable G′ and G″ over the temperature range of 25–100 °C (Fig. 8d). These rheological results

provided evidence that the addition of GO in PolyAspAm(GABA/ DOPA/EA)/B3+ hydrogel can considerably increase the modulus and impart thermal stability in the hydrogel. 3.5. Mechanical properties of GO–PolyAspAm nanocomposite hydrogel The tensile and compressive strengths were measured of hydrogels with and without GO nanosheets in their cross-linked networks. Fig. 9a shows tensile stress–strain curves of PolyAspAm(GABA/DOPA/ EA)/B3+ gel without GO and GO5%–PolyAspAm(GABA/DOPA/EA)/B3+ gel having the same water content. The PolyAspAm/B3+ hydrogel behaved as a soft gel with the maximum strain of 153% and tensile stress failure at 29 kPa, respectively. The GO-containing gel showed the much higher fracture stress of 68 kPa, about 2.3 times that of the gel without GO. The stiffness of the hydrogel including GO increased remarkably, suggesting strong hydrogen bonding interactions between the GO sheets and the polymer chains, in addition to the inherent filler effect of the GO. However, the elongation at break obviously decreased with added GO, owing to the increased cross-linking density, which reduced the critical strain of the material. In addition, variation in water content was found to meaningfully influence the mechanical properties of the GO5%–PolyAspAm(GABA/ DOPA/EA)/B3 + nanocomposite gels. For GO5%–PolyAspAm/B3 + with the water content of 90%, the critical strain value was about 60%, and the corresponding fracture stress was only 17 kPa. Decreasing the water content from 90% to 50% monotonically increased the tensile

Fig. 9. Tensile stress–strain curves illustrating the mechanical properties of PolyAspAm(GABA/DOPA/EA)/B3+ hydrogels: GO5%–PolyAspAm/B3+ and PolyAspAm/B3+ hydrogels (a); GO5%–PolyAspAm(GABA/DOPA/EA)/B3+ gels having various water contents (b); compressive stress–strain curves of GO5%–PolyAspAm/B3+ and PolyAspAm/B3+ hydrogels (c); GO5%–PolyAspAm/B3+ hydrogel during three cycles of loading to 50% strain (d).

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strength; the sample with 50% water content had the tensile strength of 102 kPa, about 6 times higher than that of the sample with 90% water content (Fig. 9b). As expected, however, the elongation was decreased as the water content was lowered, which made the gel stiffer and more brittle. When the water content was decreased to 50%, the gel's elongation at break was only 18%. From the above tensile measurements, it seemed that the mechanical properties of the gel were controllable within some range by means of controlling its water content. At the intermediate water content of 70%, GO5%–PolyAspAm/B3+ hydrogel exhibited reasonable mechanical toughness, with the fracture stress of 68 kPa and the critical strain of 37%. Fig. 9c shows compressive stress–strain curves of PolyAspAm(GABA/DOPA/EA)/B3 + and GO5%–PolyAspAm(GABA/ DOPA/EA)/B3 + hydrogels, both having 70% water content. While the compressive strength reached 289 kPa at the maximum strain of 69% in the PolyAspAm(GABA/DOPA/EA)/B3 + sample, the compressive strength of the GO5%–PolyAspAm(GABA/DOPA/EA)/B3+ gel significantly increased to 590 kPa at its maximum strain of 55%, suggesting that the compressive mechanical properties were also enhanced considerably by introducing GO to the given PolyAspAm hydrogel system. Hysteretic stress–strain loops were acquired during cyclic loading of the GO5%–PolyAspAm(GABA/DOPA/EA)/B3+ hydrogel to the maximum of 50% strain (Fig. 9d). A large hysteresis loop was observed during the first loading–unloading cycle, indicating the gel's strong ability to dissipate energy. Although the hysteresis loops of the second and third cycles were reduced somewhat, these results confirmed that the dynamic cross-linking among PolyAspAm chains by GO and B3 + imparted reversible recovery properties to the GO5%– PolyAspAm(GABA/DOPA/EA)/B3+ hydrogel. 4. Conclusion We demonstrated a novel pH-responsive self-healing nanocomposite hydrogel based on catechol-containing polyaspartmides and graphene oxide. These novel semi-IPNs hydrogels exhibited good thermal stability and low cytotoxicity. By adding optimal 5 wt% of GO, the resulting semi-IPNs hydrogel exhibited 10-fold increases in both storage and loss moduli compared to that without GO. Also the hydrogel exhibited good mechanical properties with high tensile and compressive strengths. Furthermore, the hydrogels retained autonomously and rapidly self-healing performance at room temperature without any external stimuli, which provide these GO-containing biocompatible polyaspartamide hydrogels with various potential biomedical applications. Acknowledgment This work was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Education, Science and Technology (#2011-0011464). Appendix A. Supplementary data Additional data on the GO preparation and characterization, and also the result on the in vitro cytotoxicity test of hydrogel can be found in appendix to this article. Supplementary data to this article can be found online at http://dx.doi.org/10.1016/j.msec.2016.06.065. References [1] S. Strandman, X.X. Zhu, Self-healing supramolecular hydrogels based on reversible physical interactions, Gels (2016) 1–31. [2] A. Phadke, C. Zhang, B. Arman, C.C. Hsu, R.A. Mashelkar, A.K. Lele, S. Varghese, Rapid self-healing hydrogels, PNAS 109 (2012) 4383–4388. [3] G. Akay, A. Hassan–Raeisi, D.C. Tuncaboylu, N. Orakdogen, S. Abdurrahmanoglu, W. Oppermann, O. Okay, Self-healing hydrogels formed in catanionic surfactant solutions, Soft Matter 9 (2013) 2254–2261.

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