Review

Mussel-Inspired Hydrogels for Tissue Healing

  • Geng Huimin ,
  • Cui Jiwei ,
  • Hao Jingcheng
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  • Key Laboratory of Colloid and Interface Chemistry of the Ministry of Education, Shandong University, Jinan 250100

Received date: 2020-01-11

  Online published: 2020-01-13

Supported by

Project supported by the National Natural Science Foundation of China (Nos. 21603120, 21872085) and the Natural Science Foundation of Shandong Province (Nos. ZR2018ZA0547, ZR2019BB056).

Abstract

Surgical sutures, staples and clips have been widely used for wound closure, tissue reconstruction and tissue adhesives are one of the versatile alternatives especially for friable tissues. Some synthetic and semisynthetic tissue adhesives are available elsewhere. However, there are some drawbacks, such as poor adhesion on wet substrates and potential toxicity, for the reported tissue adhesives. Fibrin glues as biological tissue adhesives are effective hemostatic agents while presenting relatively weak tensile and adhesion strengths and being expensive. Biomimetic adhesives as tissue adhesives, hemostatic agents, or tissue sealants have attracted great attention for clinical operations in last three decades. However, engineering of bio-adhesive materials with good water resistance, high adhesive strength, and good biocompatibility and multi-functionality remains a challenge for tissue healing. Since the first report of mussel-inspired surface chemistry for functional coatings of polydopamine by the Messersmith group in 2007, materials containing plenty of phenolic hydroxyl groups have been widely used in medical applications, food, cosmetics, water treatment and so on, due to the antioxidant, antibacterial, and anti-inflammatory effects of polyphenols. Polyphenol-based hydrogel is an ideal bio-adhesive material due to its good tissue adhesion even on wet substrates, hemostatic and antimicrobial capabilities. Moreover, these hydrogels with porous structures have similar physiochemical properties to that of natural extracellular matrix and different shapes from nanometer to centimeter scales can be remolded to seal irregular defects on tissues. In this review, we report the recent progress of the engineering of polyphenol-synthetic polymer hydrogels, polyphenol-biomacromolecule hydrogels, polyphenol-inorganic nanocomposite hydrogels, and polydopamine nanoparticle composite hydrogels, as well as their applications of tissue adhesives, hemostasis, antimicrobials for wound closure and tissue regeneration. The challenges as well as prospects for future development of polyphenol-based tissue adhesives, sealants, hemostatic agents are also summarized and discussed, which is helpful to promote the next generation of tissue adhesives for biomedical applications.

Cite this article

Geng Huimin , Cui Jiwei , Hao Jingcheng . Mussel-Inspired Hydrogels for Tissue Healing[J]. Acta Chimica Sinica, 2020 , 78(2) : 105 -113 . DOI: 10.6023/A19080301

References

[1] Zhu, W.; Chuah, Y. J.; Wang, D. A. Acta Biomater. 2018, 74, 1.
[2] Duarte, A. P.; Coelho, J. F.; Bordado, J. C.; Cidade, M. T.; Gil, M. H. Prog. Polym. Sci. 2012, 37, 1031.
[3] Bré, L. P.; Zheng, Y.; Pêgo, A. P.; Wang, W. Biomater. Sci. 2013, 1, 239.
[4] Liu, Z.; Meyers, M. A.; Zhang, Z.; Ritchie, R. O. Prog. Mater. Sci. 2017, 88, 467.
[5] Lee, H.; Dellatore, S. M.; Miller, W. M.; Messersmith, P. B. Science 2007, 318, 426.
[6] Harrington, M. J.; Masic, A.; Holten-Andersen, N.; Waite, J. H.; Fratzl, P. Science 2010, 328, 216.
[7] Maier, G. P.; Rapp, M. V.; Waite, J. H.; Israelachvili, J. N.; Butler, A. Science 2015, 348, 628.
[8] Rahim, M. A.; Kristufek, S. L.; Pan, S.; Richardson, J. J.; Caruso, F. Angew. Chem., Int. Ed. 2019, 58, 1904.
[9] Liu, Y.; Ai, K.; Lu, L. Chem. Rev. 2014, 114, 5057.
[10] Lee, H.; Lee, B. P.; Messersmith, P. B. Nature 2007, 448, 338.
[11] Lee, H. D., S.; Miller, W.; Messersmith, P. Science 2011, 318, 5.
[12] Dai, Q.; Geng, H.; Yu, Q.; Hao, J.; Cui, J. Theranostics 2019, 9, 3170.
[13] Patil, N.; Jérôme, C.; Detrembleur, C. Prog. Polym. Sci. 2018, 82, 34.
[14] Ejima, H. R., J.; Liang, K.; Best, J.; Koeverden, M.; Such, G.; Cui, J.; Caruso, F. Science 2013, 341, 5.
[15] Faure, E.; Falentin-Daudré, C.; Jérôme, C.; Lyskawa, J.; Fournier, D.; Woisel, P.; Detrembleur, C. Prog. Polym. Sci. 2013, 38, 236.
[16] Shukla, A.; Fang, J. C.; Puranam, S.; Jensen, F. R.; Hammond, P. T. Adv. Mater. 2012, 24, 492.
[17] Chen, J.; Cheng, W.; Chen, S.; Xu, W.; Lin, J.; Liu, H.; Chen, Q. Nanoscale 2018, 10, 22818.
[18] Gopalakrishnan, L.; Ramana, L. N.; Sethuraman, S.; Krishnan, U. M. Carbohyd. Polym. 2014, 111, 215.
[19] Scalbert, A. Phytochemistry 1991, 30, 3875.
[20] Choi, Y. S.; Kang, H.; Kim, D. G.; Cha, S. H.; Lee, J. C. ACS Appl. Mater. Interfaces 2014, 6, 21297.
[21] Qi, C.; Fu, L.-H.; Xu, H.; Wang, T.-F.; Lin, J.; Huang, P. Sci. China Chem. 2019, 62, 162.
[22] Wang, X.; Sheng, J.; Yang, M. Chinese Chem. Lett. 2019, 30, 533.
[23] Ghobril, C.; Grinstaff, M. W. Chem. Soc. Rev. 2015, 44, 1820.
[24] Zhang, K.; Zhang, F.; Song, Y.; Fan, J. B.; Wang, S. Chin. J. Chem. 2017, 35, 811.
[25] Zhang, H.; Zhao, T.; Newland, B.; Liu, W.; Wang, W.; Wang, W. Prog. Polym. Sci. 2018, 78, 47.
[26] Han, L.; Yan, L.; Wang, K.; Fang, L.; Zhang, H.; Tang, Y.; Ding, Y.; Weng, L. T.; Xu, J.; Weng, J.; Liu, Y.; Ren, F.; Lu, X. NPG Asia Mater. 2017, 9, e372.
[27] Huang, K.; Lee, B. P.; Ingram, D. R.; Messersmith, P. B. Biomacromolecules 2002, 3, 397.
[28] Krogsgaard, M.; Andersen, A.; Birkedal, H. Chem. Commun. 2014, 50, 13278.
[29] North, M. A.; Del, Grosso, C. A.; Wilker, J. J. ACS Appl. Mater. Interfaces 2017, 9, 7866.
[30] Mu, Y.; Wu, X.; Pei, D.; Wu, Z.; Zhang, C.; Zhou, D.; Wan, X. ACS Biomater. Sci. Eng. 2017, 3, 3133.
[31] Lee, B. P.; Dalsin, J. L.; Messersmith, P. B. Biomacromolecules 2002, 3, 1038.
[32] Burke, S. A.; Ritter-Jones, M.; Lee, B. P.; Messersmith, P. B. Biomed. Mater. 2007, 2, 203.
[33] Bilic, G.; Brubaker, C.; Messersmith, P. B.; Mallik, A. S.; Quinn, T. M.; Haller, C.; Done, E.; Gucciardo, L.; Zeisberger, S. M.; Zimmermann, R.; Deprest, J.; Zisch, A. H. Am. J. Obstet. Gynecol. 2010, 202, 85.
[34] Brubaker, C. E.; Kissler, H.; Wang, L. J.; Kaufman, D. B.; Messersmith, P. B. Biomaterials 2010, 31, 420.
[35] Mehdizadeh, M.; Weng, H.; Gyawali, D.; Tang, L.; Yang, J. Biomaterials 2012, 33, 7972..
[36] Brubaker, C. E.; Messersmith, P. B. Biomacromolecules 2011, 12, 4326.
[37] Mou, C.; Ali, F.; Malaviya, A.; Bettinger, C. J. J. Mater. Chem. B 2019, 7, 1690.
[38] Holten-Andersen, N.; Harrington, M. J.; Birkedal, H.; Lee, B. P.; Messersmith, P. B.; Lee, K. Y.; Waite, J. H. Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 2651.
[39] He, L.; Fullenkamp, D. E.; Rivera, J. G.; Messersmith, P. B. Chem. Commun. 2011, 47, 7497.
[40] Guo, J.; Sun, W.; Kim, J. P.; Lu, X.; Li, Q.; Lin, M.; Mrowczynski, O.; Rizk, E. B.; Cheng, J.; Qian, G.; Yang, J. Acta Biomater. 2018, 72, 35.
[41] Li, N.; Yang, X.; Liu, W.; Xi, G.; Wang, M.; Liang, B.; Ma, Z.; Feng, Y.; Chen, H.; Shi, C. Macromol. Biosci. 2018, 18, e1800209.
[42] Wang, C.; Zhou, H.; Niu, H.; Ma, X.; Yuan, Y.; Hong, H.; Liu, C. Biomater. Sci. 2018, 6, 3318.
[43] Erel-Unal, I.; Sukhishvili, S. A. Macromolecules 2008, 41, 3962.
[44] Kim, K.; Shin, M.; Koh, M. Y.; Ryu, J. H.; Lee, M. S.; Hong, S.; Lee, H. Adv. Funct. Mater. 2015, 25, 2402.
[45] Xu, R.; Ma, S.; Lin, P.; Yu, B.; Zhou, F.; Liu, W. ACS Appl. Mater. Interfaces 2018, 10, 7593.
[46] Nam, H. G.; Nam, M. G.; Yoo, P. J.; Kim, J. Soft Matter 2019, 15, 785.
[47] Zhou, L.; Fan, L.; Yi, X.; Zhou, Z.; Liu, C.; Fu, R.; Dai, C.; Wang, Z.; Chen, X.; Yu, P.; Chen, D.; Tan, G.; Wang, Q.; Ning, C. ACS Nano 2018, 12, 10957.
[48] Fan, H.; Wang, L.; Feng, X.; Bu, Y.; Wu, D.; Jin, Z. Macromolecules 2017, 50, 666.
[49] Fan, H.; Wang, J.; Zhang, Q.; Jin, Z. ACS Omega 2017, 2, 6668.
[50] Zheng, L. Y.; Shi, J. M.; Chi, Y. H. Macromol. Chem. Phys. 2018, 219, 1800234.
[51] Sahiner, N.; Sagbas, S.; Sahiner, M.; Silan, C.; Aktas, N.; Turk, M. Int. J. Biol. Macromol. 2016, 82, 150.
[52] Sahiner, N.; Sagbas, S.; Aktas, N. Polym. Degrad. Stabil. 2016, 129, 96.
[53] Hong, S. H.; Shin, M.; Lee, J.; Ryu, J. H.; Lee, S.; Yang, J. W.; Kim, W. D.; Lee, H. Adv. Healthcare Mater. 2016, 5, 75.
[54] Shao, C.; Meng, L.; Wang, M.; Cui, C.; Wang, B.; Han, C. R.; Xu, F.; Yang, J. ACS Appl. Mater. Interfaces 2019, 11, 5885.
[55] Ryu, J. H.; Hong, S.; Lee, H. Acta Biomater. 2015, 27, 101.
[56] Zhu, W.; Iqbal, J.; Wang. D. A. J. Mater. Chem. B 2019, 7, 1741.
[57] Levengood, S. L.; Zhang, M. J. Mater. Chem. B 2014, 2, 3161.
[58] Ryu, J. H.; Lee, Y.; Kong, W. H.; Kim, T. G.; Park, T. G.; Lee, H. Biomacromolecules 2011, 12, 2653.
[59] Shin, M.; Park, S. G.; Oh, B. C.; Kim, K.; Jo, S.; Lee, M. S.; Oh, S. S.; Hong, S. H.; Shin, E. C.; Kim, K. S.; Kang, S. W.; Lee, H. Nat. Mater. 2017, 16, 147.
[60] Shin, M.; Ryu, J. H.; Kim, K.; Kim, M. J.; Jo, S.; Lee, M. S.; Lee, D. Y.; Lee, H. ACS Biomater. Sci. Eng. 2018, 4, 2314.
[61] Zhu, W.; Peck, Y.; Iqbal, J.; Wang, D. A. Biomaterials 2017, 147, 99.
[62] Natarajan, V.; Krithica, N.; Madhan, B.; Sehgal, P. K. J. Biomed. Mater. Res. B 2013, 101, 560.
[63] Fan, C.; Fu, J.; Zhu, W.; Wang, D. A. Acta Biomater. 2016, 33, 51.
[64] Lu, D.; Wang, H.; Li, T. E.; Li, Y.; Wang, X.; Niu, P.; Guo, H.; Sun, S.; Wang, X.; Guan, X.; Ma, H.; Lei, Z. Chem. Mater. 2017, 29, 5493.
[65] Wang, R.; Li, J.; Chen, W.; Xu, T.; Yun, S.; Xu, Z.; Xu, Z.; Sato, T.; Chi, B.; Xu, H. Adv. Funct. Mater. 2017, 27, 1604894.
[66] Han, X.; Meng, G.; Wang, Q.; Cui, L.; Wang, H.; Wu, J.; Liu, Z.; Guo, X. J. Biomater. Appl. 2019, 33, 915.
[67] Shin, M.; Ryu, J. H.; Park, J. P.; Kim, K.; Yang, J. W.; Lee, H. Adv. Funct. Mater. 2015, 25, 1270.
[68] Schexnailder, P.; Schmidt, G. Colloid Polym. Sci. 2008, 287, 1.
[69] Thoniyot, P.; Tan, M. J.; Karim, A. A.; Young, D. J.; Loh, X. J. Adv. Sci. 2015, 2, 1400010.
[70] Rose, S.; Prevoteau, A.; Elziere, P.; Hourdet, D.; Marcellan, A.; Leibler, L. Nature 2014, 505, 382.
[71] Li, L.; Smitthipong, W.; Zeng, H. Polym. Chem. 2015, 6, 353.
[72] Han, L.; Lu, X.; Liu, K.; Wang, K.; Fang, L.; Weng, L. T.; Zhang, H.; Tang, Y.; Ren, F.; Zhao, C.; Sun, G.; Liang, R.; Li, Z. ACS Nano 2017, 11, 2561.
[73] Ding, X.; Vegesna, G. K.; Meng, H.; Lee, B. P.; Winter, A. Macromol. Chem. Phys. 2015, 216, 1109.
[74] Liu, Y.; Meng, H.; Qian, Z.; Fan, N.; Choi, W.; Zhao, F.; Lee, B. P. Angew. Chem. Int. Ed. 2017, 56, 4224.
[75] Lynge, M. E.; Schattling, P.; Stadler, B. Nanomedicine 2015, 10, 2725.
[76] Wang, X.; Wang, C.; Wang, X.; Wang, Y.; Zhang, Q.; Cheng, Y. Chem. Mater. 2017, 29, 1370.
[77] Wang, C.; Zhang, Q.; Wang, X.; Chang, H.; Zhang, S.; Tang, Y.; Xu, J.; Qi, R.; Cheng, Y. Angew. Chem. Int. Ed. 2017, 56, 6767.
[78] Hu, W.; Lu, S.; Zhang, Z.; Zhu, L.; Wen, Y.; Zhang, T.; Ji, Z. Biomater. Sci. 2019, 7, 1323.
[79] Han, L.; Zhang, Y.; Lu, X.; Wang, K.; Wang, Z.; Zhang, H. ACS Appl. Mater. Interfaces 2016, 8, 29088.
[80] Zhu, S.; Gu, Z.; Xiong, S.; An, Y.; Liu, Y.; Yin, T.; You, J.; Hu, Y. RSC Adv. 2016, 6, 66180.
[81] Tang, P.; Han, L.; Li, P.; Jia, Z.; Wang, K.; Zhang, H.; Tan, H.; Guo, T.; Lu, X. ACS Appl. Mater. Interfaces 2019, 11, 7703.
[82] Gao, G.; Jiang, Y. W.; Jia, H. R.; Wu, F. G. Biomaterials 2019, 188, 83.
[83] Jing, X.; Mi, H. Y.; Napiwocki, B. N.; Peng, X. F.; Turng, L. S. Carbon 2017, 125, 557.
[84] Han, L.; Lu, X.; Wang, M.; Gan, D.; Deng, W.; Wang, K.; Fang, L.; Liu, K.; Chan, C. W.; Tang, Y.; Weng, L. T.; Yuan, H. Small 2017, 13, 1601916.
[85] Chen, Q.; Wang, C.; Zhang, X.; Chen, G.; Hu, Q.; Li, H.; Wang, J.; Wen, D.; Zhang, Y.; Lu, Y.; Yang, G.; Jiang, C.; Wang, J.; Dotti, G.; Gu, Z. Nat. Nanotechnol. 2019, 14, 89.
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