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A bio-inspired adhesive hydrogel driven by adenine and thymine Xin Liu, Qin Zhang, Zijian Gao, Ruibin Hou, and Guanghui Gao ACS Appl. Mater. Interfaces, Just Accepted Manuscript • Publication Date (Web): 03 May 2017 Downloaded from http://pubs.acs.org on May 4, 2017

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ACS Applied Materials & Interfaces

A Bio-Inspired Adhesive Hydrogel Driven by Adenine and Thymine

Xin Liu, Qin Zhang, Zijian Gao, Ruibin Hou, Guanghui Gao*

Polymeric and Soft Materials Laboratory, School of Chemical Engineering and Advanced Institute of Materials Science, Changchun University of Technology, Changchun 130012, China Corresponding authors: E-mail: [email protected] (G. Gao)

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ABSTRACT Bio-inspired strategies have drawn much attention for designing intelligent hydrogels with promising performance. Herein, we present a bio-inspired adhesive hydrogel driven by adenine and thymine, which are the basic units of deoxyribonucleic acid (DNA). The adhesive hydrogel exhibited promising adhesive for the surface of various solid materials, including muscle tissue, plastics, rubbers, glasses, metals, ceramics, carnelians and woods. The maximum peeling strength of hydrogels was 330 N m-1 on aluminum, superior to that of PAAm hydrogels with 70 N m-1. The strong adhesive behavior remained more than 30 times repeated peeling tests. Moreover, the swelling behavior, morphological structure, mechanical strength, peeling adhesive strength were also investigated and confirmed the formation and various characteristics of adhesive hydrogels driven by adenine and thymine. Thus, the biomimetic strategy to design promising adhesive hydrogels can provide various opportunities in tissue engineering, such as wound dressing, bio-glues, and tissue adhesives.

KEYWORDS: Bio-inspired; Adhesive hydrogel; Polyacrylamide; Adenine; Thymine

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INTRODUCTION Hydrogels have aroused growing interest in many fields due to resembling the biological tissues1-7. Up to now, intense efforts have been devoted to create a hydrogel with remarkable performance, such as adhesive1-3, toughness4,5, self-healing6 and shape memory7. And the adhesive hydrogels would be applied into biomedical applications, including electronic devices for human body8,9, damaged tissue repair7,10, 3D printing for tissues11 and bio-glue12,13. In general, the adhesive behavior of hydrogels is weakened owing to large amounts of water in the system1,14. The water molecules interact with the adhesive groups in hydrogels via hydrogen bonding, which significantly weakens adhesion between hydrogels and surface of solids. The ordinary adhesives exhibit alternative adhesive for organic or inorganic surfaces. However, the multi-purpose and strong adhesion is significant for complicated interfaces, such as human portable equipment, wound dressing, and bio-glues. In the previous works, primary strategies for the formulation of multi-purpose hydrogel adhesives have been chemical anchorage on solids1,15,16 and physical adhesion to the substrate surfaces17–21. Yuk et al. have successfully manufactured an adhesive hydrogel via chemical anchorage of silanation process on the various solid surfaces1. However, the adhesive behavior vanishes after the chemical anchorage bonding is destroyed. Therefore, physical interactions between adhesives and solid surfaces are worth to be considered to design adhesive hydrogels for multi-purpose and reusable adhesive behaviors. Up to now, the existing adhesive hydrogels are mostly inspired by mussel, barnacle and sandcastle worm. The effective strategies 3



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have been explored based on catechol22–24 and its analogs25–27. These investigations were primarily based on the structure of catechol molecules. However, a proverbial drawback of catechol is easily oxidized, leading to gradually weakened adhesive behavior of hydrogels with the increase of time28. In order to pursue possible adhesive components, some stable biological molecules should also be considered for introduction into hydrogels for multi-purpose and reusable adhesion via physical synergistic interactions with the surface of solids. Nucleobases are nitrogen-containing compounds (nitrogenous bases), which are linked to a sugar within the nucleosides. They are the basic building blocks of deoxyribonucleic acid (DNA) and ribonucleic acid (RNA). Adenine (A) and thymine (T), two vital nucleobases, have some special properties and corresponding applications in various fields, such as organic light emitting diodes29, transistors30, pressure-sensitive adhesive31 and supramolecular fibres32. Moreover, due to their unique molecular structures, adenine and thymine, can provide hydrogen bonding, metal-complexation and hydrophobic interaction with the corresponding components of the solid materials. It is envisioned that the adhesive hydrogels driven by nucleobases would exhibit a multi-purpose and reusable adhesive behavior on the surface of solid materials. In the current work, we present a bio-inspired strategy to prepare an adhesive hydrogel driven by adenine and thymine. Adenine and thymine were distributed in the PAAm to act as adhesive groups and the hydrogen bonding from them endowed hydrogels with certain mechanical properties. Based on the structure of adenine and 4


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thymine, the possible adhesion interactions should include hydrogen bonding, metal-complexation and hydrophobic interaction. So, it is anticipated that adhesive hydrogels driven by adenine and thymine could also effectively adhere to a variety of solids, including plastic, rubber, glass, metal and biological tissue. The biomimetic strategy is well dependent on physical interactions without any chemical treatment and can open a new avenue in hydrogel-based adhesives for biomedical engineering.

EXPERIMENTAL SECTION Materials Adenine (A, 98.0%), thymine (T, 99.0%), acryloyl chloride (AC, 96.0%), triethylamine (AR, 99.0%), acrylamide (AAm, 99.0%), potassium persulfate (KPS, 99.5%) and N,N-dimethylformamide (DMF, 99.8%) were supplied by Aladdin (Shanghai, China). Diethyl ether (AR, 96%) was purchased from Tiantai Chemical Works in Tianjing. Deionized water (18.2 MΩ cm resistivity at 25°C) was used in the experiment. Synthesis of Acrylated Adenine A suspension of adenine (1.35 g, 0.01 mol) and triethylamine (1.05 mL, 0.013 mol) in DMF (20 mL) were stirred in ice bath for 30 min, and thereafter, acryloyl chloride (1.3 mL, 0.011 mmol) was added into the reaction system. The reaction system was carried out with continuous stirring at room temperature for 6 h and added dropwise into a diethyl ether solution (400 mL) to precipitate acrylated adenine (Aa). Finally, acrylated adenine was placed in vacuum to remove all the solvents. 1H NMR (400 5



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MHz, DMSO-d6) δ ppm: 12.19 (2H, -NH2), 7.33 (1H, -N=CH-N=), 8.10 (1H, -N=CH-N=), 4.58, 4.37, 4.33 (3H, -CH=CH2). Synthesis of Acrylated Thymine A suspension of thymine (1.26 g, 0.01 mol) and triethylamine (1.5 mL, 0.011 mol) in DMF (20 mL) were stirred in ice bath for 30 min, and thereafter, acryloyl chloride (1.05 mL, 0.013 mol) was added into the reaction system. The reaction system was carried out with continuous stirring at room temperature for 6 h and added dropwise into a diethyl ether solution (400 mL) to precipitate acrylated thymine (Ta). Finally, acrylated thymine was placed in vacuum to remove all the solvents. 1H NMR (400 MHz, DMSO-d6) δ ppm: 10.97 (1H, -CO-NH-CO-), 7.24 (1H, -C=CH-N-), 6.41, 6.24, 5.96 (3H, -CH=CH2), 1.57 (3H, -CH3). Preparation of Hydrogels In the first step, AAm (2 g), Aa (0.3 g), Ta (0.3 g), KPS (0.02 g), water (10 mL) were poured into the beaker and the solution was stirred to prepare a homogeneous solution. Subsequently, the solution was injected into a reaction mold (100×20×6 mm3), which composed of a pair of glass plates and a silica gel sideline with 6.0 mm thickness. Finally, the samples were placed in an oven at 70 ºC for 5 h to obtain the adhesive hydrogels. The formulations of hydrogels were denoted as H-AT-x-y-z, where, x, y and z were masses of AAm, Aa and Ta, respectively. For example, the hydrogel obtained through the above method was named as H-AT-2-0.3-0.3. PAAm hydrogels were prepared as follows: AAm (2 g), KPS (0.02 g) and water (10 mL) were poured into the beaker and stirred to prepare a homogeneous solution. 6


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Thereafter, the solution was injected into a reaction mold (100×20×6 mm3), which composed of a pair of glass plates and a silica gel sideline with 6.0 mm thickness. Finally, the samples were placed in an oven at 70 ºC for 5 h to obtain PAAm hydrogels. FT-IR Analysis The chemical structures of the acrylated A and T were analyzed by an FTIR spectrometer (Avatar-360; Nicolet). FTIR spectra were obtained in the spectral range of 400-4000 cm-1 with a resolution of 4 cm-1 and 64 scans for each sample. Before measurement, the samples were ground and dispersed in KBr by compression to form a sheet. Peeling Measurement In order to assess the peeling adhesive strength, 90º peeling test was employed. A texture analyzer (CT3-1000, made in U.S.A) was used to evaluate the adhesive strength between hydrogels and solid surfaces. Firstly, the hydrogel samples were attached with a cloth foil in order to obtain original peeling adhesive strength in order to prevent their elongation along the peeling direction. The hydrogel specimen was attached to the surface of different solid materials, such as aluminum, silica rubber and glass with 700 g of weight pressure for 10-30 min. Thereafter, the peeling adhesion test was carried out at a rate of 5 mm min-1 and peel angle of 90o. Measurements of each samples were repeated at least five times and were averaged for a given sample. As for the test of reversible adhesive, the same adhesive hydrogel sample was 7



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carried out with abovementioned process, where the waiting time attached to the surface of substrate was 10 min. Mechanical Property Tests The tensile performances were performed by a tensile tester (SHIMADZU, model AGS-X, 100N, Japan). All simples were cut into dumbbell shape (30 mm × 4 mm × 6 mm. The tests were performed with constant velocity of 100 mm min-1. The Young’s modulus was calculated from the slope of the initial linear region (ε = 10%-20%) of the stress-strain curves of hydrogels. For compression measurement, the samples were cylindrical with diameter of 20 mm and thickness of 15 mm. The compression tests were carried out by a texture analyzer (CT3-1000, made in U.S.A) with a constant velocity of 5 mm min-1, to the strain of 90% for the hydrogel samples. All mechanical tests were carried out at room temperature. Measurements of each samples were repeated at least five times and were averaged for a given sample. Swelling Behavior Hydrogel samples were prepared to investigate the properties of the swelling equilibrium in water. To reach swelling equilibrium, the samples were soaked in distilled water for 24 h at room temperature. As is known, the equilibrium swelling ratio is defined as follows: Equilibrium swelling ratio=

ௐ௦ିௐ௜ ௐ௜

× 100%

where Ws and Wi are the weights of the swollen and initial samples, respectively. Scanning Electron Microscopy (SEM) 8


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The morphologies of the hydrogels were characterized by SEM (JSM-6510; JEOL; Japan) with a working distance of 15 mm and the accelerating voltage of 10 kV. Before observation, the hydrogel samples for SEM analysis were freeze-dried, and the sections of samples were coated with platinum to provide a conductive environment. The magnification factor was 1000 times.

RESULTS AND DISCUSSION It is well known that the bonding strength depends on the balance of cohesion and adhesion33. In order to prepare an adhesive hydrogel, adenine and thymine were introduced into the polyacrylamide backbone to improve the balance of cohesion and adhesion (Fig. 1). The FT-IR spectroscopy of A and Aa was measured to confirm successful synthesis of acrylated adenine and shown in Fig. 2a. The strong band at 1635 cm-1 was associated with the functionalized acrylic group of Aa. As for T and Ta, the FT-IR curve exhibited a significant enhancement at the peak of 1734 cm-1 in Fig. 2b, which attributed to conjugated carbonyl groups of acrylated thymine. Adenine and thymine are basic nucleobases which can provide physical crosslinking via hydrogen bonding between them to ensure cohesive behavior and possible adhesion interactions with the solid surfaces. The PAAm hydrogels driven by adenine and thymine exhibited an excellent adhesive property, which can adhere to the surface of various solids. As shown in Fig. 3, the adhesive hydrogels could easily adhere to plastic, polytetrafluoroethylene, polythene, rubber, silica rubber, ceramics, glass, silica glass, 9



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carnelian, wood, stainless steel, gold, silver, copper and aluminum. The formulated multi-purpose bio-inspired adhesive can be potentially utilized in various fields of medical electrodes, joints for articulation, and human portable equipment. Figure 1 Figure 2 Figure 3 Based on the molecular structure of hydrogels modified by adenine and thymine, the strong adhesion could only depend on physical interactions between hydrogels and solids. Moreover, the physical interactions were different for various solids2. The possible adhesive interactions should be due to hydrogen bonding, metal-coordination, and hydrophobic interaction. Meanwhile, several synergetic interactions might simultaneously exist at the interface between hydrogels and solid substrates. As shown in Fig. 4, the N−H and −NH2 groups from adenine and thymine can form hydrogen bonds with N, O and F components of solid materials to improve the adhesion28,34. Moreover, the C=O and −N= components can easily form hydrogen bonding with −OH and −NH2 groups of the solid materials. The −N= and C=O groups of adenine and thymine in hydrogels can generate metal-complexation with the metal ions on the solid surface for adhesion35. The hydrophobic interactions should be considered due to the weak hydrophobic property of adenine and thymine consisting of heterocyclic structure13,35,36. Besides, it was deduced that other interactions, such as π-π stacking and cation-π interaction, could exist between hydrogels and solid surface due to the unsaturated heterocyclic structure of adenine and thymine13,35,37,38. To 10


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summarize, the multi-purpose adhesive properties of hydrogels driven by adenine and thymine were well-demonstrated and were based on the possible physical interactions between the special molecular structure of nucleobases and various solids. Figure 4 In order to clearly demonstrate the adhesive performance of adhesive hydrogels, the macroscopic peeling process is displayed. It can be clearly seen that there were significant differences between PAAm-A-T hydrogels and PAAm hydrogels from Supplementary Movie 1, 2 and Fig. 5. The stripping lag is that the adhesive hydrogels could not be immediately peeled off from the substrate during the process of peeling test. A clear crack and stripping lag existed at the interface between PAAm-A-T hydrogels and substrates. Since the degree of crack and stripping lag demonstrate excellent adhesive behavior, a large crack and stripping lag suggested the balance of cohesion and adhesion in hydrogels1. However, there was almost no crack and stripping lag process in PAAm hydrogels. It was evident that the adhesion force of PAAm hydrogels was significantly enhanced due to the introduction of A and T components. Figure 5 To measure the adhesive strength of A and T modified PAAm hydrogels, four representative substrates, including aluminum, glasses, silica rubber, hogskin, and Polytetrafluoroethylene (PTFE), were chosen under the mode of 90º peeling adhesion test and the results are shown in Fig. 6a. The adhesive force of hydrogels on the surface of aluminum was the highest among the substrates. The primary adhesive 11



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interaction

between

hydrogels

and

aluminum

should

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be

the

effects

of

metal-complexation and hydrogen bonding. Moreover, the hydrophobic interaction and hydrogen bonding are probably the two primary factors in the adhesion of hydrogels for glasses and PTFE, while the adhesion of hogskin and silica rubber for hydrogels should be derived from hydrogen bonding. Consequently, the effective adhesion strength was different based on different physical interactions. In regards to the dependence of non C-C covalent interactions for adhesive behavior, the contact time of adhesives and receptors should be of considerable importance in influencing the adhesive strength. The effect of different contact times from 10 min to 30 min on the adhesion strength between A and T modified hydrogels and aluminum substrates was measured and the results are shown in Fig. 6b. The adhesive force was about 150 N m-1 for a contact time of 10 min. As the contact time increased from 10 to 30 min, the interface strength significantly enhanced and the maximum adhesive force was 330 N m-1. The above results suggested that the formation of physical interface adhesion would need a process. At the beginning, when hydrogels contacted the substrate surfaces, water in hydrogels provided a wetting environment on the solid surface. This promotes the movement of molecular chains and offers the chance of polymeric molecules contacting the substrates39. Thereafter, more molecular chains contact the solid surfaces to reduce the entropy of hydrogels generating effective adhesive interactions such as hydrogen bonding, metal-complexation, hydrophobic interaction，π-π stacking and cation-π interactions. Finally, the effective bonding interactions become saturated after a period of contact 12


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time and the adhesive strength exhibited the maximum value. Therefore, the adhesive interaction was not just dynamic but slow, and the number of adhesive groups for effective adhesion interaction increased with an increase in contact time, leading to enhancement in the adhesive strength. The effect of A and T dosages in PAAm hydrogels on the adhesive behavior was measured. As shown in Fig. 6c, the PAAm hydrogels exhibited very low interface force, and the adhesive strength of A and T modified PAAm hydrogels was significantly enhanced with the increase in contents of A and T. The highest adhesive force was 330 N m-1 for H-AT-2-0.3-0.3. There could be two possible explanations for this result. On the one hand, the crosslinking density increased because of the addition of A and T via intermolecular and/or intramolecular hydrogen bonds, resulting in the cohesive improvement of hydrogels. On the other hand, the residual A and T components could contribute to significantly enhance the interface adhesive strength of hydrogels and substrates due to strong interactions between nucleobases and adhesive receptors. In comparison with chemical anchorage, the physical interactions offer more possibility of reversible adhesion for hydrogels. This is because the adhesive property of hydrogels still existed even after the interface between hydrogels and solids was separated. As shown in Fig. 6d, the peeling adhesion strength was almost unaffected even after 30 times repetition. The reversible adhesion overcame the non-reusable shortcoming of chemical anchorage, improving the utilization frequency of resources. As a result, the adhesive hydrogels with reusable adhesion can attract significant 13



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attention in the practical applications. Moreover, the underwater adhesive was also investigated and exhibited immediate adhesive behavior after the water was removed from the surface of hydrogels. A simple demonstration processes of adhesion between adhesive hydrogels and PTFE was as shown in Supplementary Movie 3. As for adhesive hydrogels, the adhesion for tissue of the creature is crucial for the specific biological applications, such as tissue adhesive, cell adhesive, and wound dressing. The adhesion between adhesive hydrogels and the endothelial tissue of mice was exhibited at the Fig. 7(a-c). And no residual adhesive behavior of hydrogels after peeling from the arm was shown in Fig. 7(d-f). The adhesive hydrogels were easily peeled off from the skin of arm without any anaphylactic reaction. It is envisioned that the adhesive hydrogels with excellent tissue adhesion would endow hydrogels with more promising opportunities for biological applications. Figure 6 Figure 7 The mechanical performance of adhesive hydrogels was crucial for the application of adhesive hydrogels. However, excellent adhesive and toughness existing in one adhesive hydrogel remains a challenge, so the study of toughness in adhesive hydrogels is significant. The mechanical performance of hydrogels was shown in Fig. 8, the tensile properties of PAAm hydrogels were enhanced by introducing the Aa and Ta components. The fracture stress and corresponding elastic modulus were enhanced at first and then decreased with the increase of the content of Aa and Ta (Fig. 8a-b). The same phenomenon was found in the compression loading-unloading process of 14


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hydrogels (Fig. 8c-d). The mechanical results indicated the role of Aa and Ta in PAAm hydrogels and the suitable mechanical strength could contribute to the balance of cohesion and adhesion for a promising adhesive property. Figure 8 To demonstrate morphological structure of PAAm hydrogels with adenine and thymine, the swelling behaviors and scanning electron microscopy (SEM) images were shown in Fig. 9. It was found that all the hydrogels showed a steady increment in swelling ratio at different time. However, the structure of PAAm hydrogels was collapsed after swelling 72 h, and the PAAm-AT adhesive hydrogel could keep the complete structure even for swelling up to 450 h (Fig. 9a). Moreover, the swelling ratio of A-T modified adhesive hydrogels decreased as the content of Aa and Ta increased due to the subsequent increase of crosslinking degree. The corresponding morphological structures of hydrogels were shown in Fig. 9c-d and the images exhibited the hydrogels were equipped with an open and interconnected porous structure, due to the loss of water during the freeze-drying process. However, the significant differences on the thickness and roughness of the pore walls were observed. Comparing to PAAm hydrogels (Fig. 9c), PAAm-AT adhesive hydrogels exhibited relatively wide thickness and smoother roughness for the pore walls (Fig. 9d), indicating the incorporation of Aa and Ta had a significant effect on the microstructure of PAAm hydrogels. Figure 9

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CONCLUSION In summary, we demonstrated an adhesive hydrogels driven by adenine and thymine with a remarkable adhesive and suitable toughness. The adhesive was effective for the surface of different solids, including plastics, rubbers, glasses, metals, ceramics, carnelians and woods, owing to hydrogen bonding, metal-complexation and hydrophobic interaction. The maximum peeling strength of hydrogels was 330 N m-1, superior to that of PAAm hydrogels of 70 N m-1. Moreover, the adhesive hydrogels exhibited a time-dependent, no residual, reusable adhesion behavior and tissue adhesive. The bio-inspired adhesive hydrogels with multiple hard-won properties could hold considerable promise for biological applications in the future, including wound dressing, bio-glues, cell adhesives and tissue adhesives. It is also anticipated that the biomimetic adhesive strategy would open an avenue in designing novel adhesive materials.

ACKNOWLEDGMENT This research was supported by a grant from National Natural Science Foundation of China (NSFC) (Nos. 51473023 and 51103014).

ASSOCIATED CONTENT Supporting Information Supplementary Figure S1: Peeling strength of PAAm hydrogels modified by A, T, and A-T. Supplementary Figure S2: Peeling strength of PAAm hydrogels on various substrates. 16


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Supplementary Movie 1: the peeling process movie of the H-AT-2-0.03-0.03 hydrogel. Supplementary Movie 2: the peeling process movie of the PAAm hydrogel. Supplementary Movie 3: the process of that adhesive remained after the water was removed from the surface of hydrogels. This information is available free of charge via the Internet at http://pubs.acs.org/.

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Fig. 1. (a) The structural illumination and (b) chemical formula of adhesive hydrogels driven by adenine and thymine.

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Fig. 2. FT-IR spectroscopy of (a) A-Aa and (b) T-Ta.

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Fig. 3. Adhesion between different adherends and hydrogels, including plastic, polytetrafluoroethylene, polythene, rubber, silica rubber, ceramics, glass, silica glass, carnelian, wood, stainless steel, gold, silver, copper and aluminum (from left to right and then from top to bottom).

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Fig.

4.

Possible

adhesion

mechanisms

including

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hydrogen

bonding,

metal-complexation, hydrophobic association and others interactions (cation-π and/or π-π stacking).

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Fig. 5. Peeling process of adhesive hydrogels on aluminum substrate: (a-c) adhesive PAAm hydrogels driven by adenine and thymine and (d-f) original PAAm hydrogels.

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Fig. 6. Peeling strength of adhesive hydrogels (a) on various substrates for H-AT-2-0.3-0.3 hydrogel after contacting 30 min, (b) at different contact times of H-AT-2-0.3-0.3 hydrogel for aluminum substrate, (c) with different A and T contents for aluminum substrate after contacting 30 min and (d) under the repeated adhesion tests for H-AT-2-0.3-0.3 hydrogel for aluminum substrate after contacting 10 min.

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Fig. 7. (a-c) the exhibition of adhesion between adhesive hydrogels and the endothelial tissue of mice; (d-f) the exhibition of no residual behavior in the process of peeling from the skin of arms.

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Fig. 8. (a) Tensile curves and (b) the elastic modulus of PAAm hydrogels and adhesive hydrogels. (c) The compression loading-unloading curves and (d) corresponding stress at 90% strain of (c) hydrogels with different ratio between AAm and Aa-Ta.

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Fig. 9. The swelling behaviors of hydrogels: (a) the swelling photographs of PAAm hydrogels and PAAm-AT adhesive hydrogels and (b) swelling curves；SEM images of (c) PAAm hydrogels and (d) PAAm-AT adhesive hydrogels.

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51x31mm (300 x 300 DPI)


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Bioinspired Adhesive Hydrogel Driven by Adenine ... - ACS Publications

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