Skip to main content
SpringerLink
Log in

Enzymatic Crosslinked Hydrogels for Biomedical Application

  • REVIEWS
  • Published:
Polymer Science, Series A Aims and scope Submit manuscript

Abstract

Self-assembled structures primarily arise through enzyme-regulated phenomena in nature under persistent conditions. Enzymatic reactions are one of the main biological processes constructing supramolecular hydrogel networks required for biomedical applications. Such enzymatic processes provide a unique opportunity to integrate hydrogel formation. In most cases, the structure and substrates of hydrogels are adjusted by enzyme catalysis due to enzymes’ chemo-, regio- and stereo-selectivity. Such hydrogels processed using various enzyme schemes showed remarkable characteristics as dynamic frames for cells, bioactive molecules, and drugs in tissue engineering, drug delivery, and regenerative medicine. The enzyme-mediated crosslinking hydrogels mimic the extracellular matrices by displaying unique physicochemical properties and functionalities such as water-retention capacity, biodegradability, biocompatibility, biostability, bioactivity, optoelectronic properties, self-healing ability, and shape memory ability. In recent years, many enzymatic systems investigated polymer crosslinking. Herein, we review efficient strategies for enzymatic hydrogelation, including hydrogel synthesis and chemistry, and demonstrate their applicability in biomedical systems. Furthermore, the advantages, challenges, and prospects of enzymatic-crosslinkable hydrogels are discussed. The results of biocompatible hydrogel products show that these crosslinking mechanisms can fulfill requirements for a variety of biomedical applications, including tissue engineering, wound healing, and drug delivery.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.
Fig. 8.

Similar content being viewed by others

AVALIBILITY OF DATA AND MATERIALS

The datasets used and or analyzed in the current study are available from the corresponding author upon reasonable request.

REFERENCES

  1. P. M. Kharkar, K. L. Kiick, and A. M. Kloxin, Chem. Soc. Rev. 42, 7335 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. I. M. El-Sherbiny and M. H. Yacoub, Global Cardiol. Sci. Pract. 2013, 316 (2013).

    Google Scholar 

  3. S. V. Gohil, A. Padmanabhan, H.-M. Kan, M. Khanal, and L. S. Nair, Tissue Eng., Part A 27, 867 (2021).

    Article  CAS  Google Scholar 

  4. N. Bahrami, M. Bayat, A. Farzin, M. Sadredin Hajseyedjavadi, A. Goodarzi, M. Salehi, R. Karimi, A. Mohamadnia, A. Ahmadi, and M. Khanmohammadi, Arch. Neurosci. 6 (2), e85118 (2019).

  5. A. Fathi, M. Khanmohammadi, A. Goodarzi, L. Foroutani, Z. T. Mobarakeh, J. Saremi, Z. Arabpour, and J. Ai, J. Biol. Eng. 14, 1 (2020).

    Article  Google Scholar 

  6. S. Shafei, M. Khanmohammadi, R. Heidari, H. Ghanbari, V. Taghdiri Nooshabadi, S. Farzamfar, M. Akbariqomi, N. S. Sanikhani, M. Absalan, and G. Tavoosidana, J. Biomed. Mater. Res. 108, 545 (2020).

    Article  CAS  Google Scholar 

  7. V. T. Nooshabadi, M. Khanmohamadi, E. Valipour, S. Mahdipour, A. Salati, Z. V. Malekshahi, S. Shafei, E. Amini, S. Farzamfar, and J. Ai, J. Biomed. Mater. Res. 108, 2138 (2020).

    Article  CAS  Google Scholar 

  8. K. Tomita, S. Sakai, M. Khanmohammadi, T. Yamochi, S. Hashimoto, M. Anzai, Y. Morimoto, M. Taya, and Y. Hosoi, J. Assisted Reprod. Genet. 33, 501 (2016).

    Article  Google Scholar 

  9. M. Khanmohammadi, M. B. Dastjerdi, A. Ai, A. Ahmadi, A. Godarzi, A. Rahimi, and J. Ai, Biomater. Sci. 6, 1286 (2018).

    Article  CAS  PubMed  Google Scholar 

  10. W. Zhang, Y. Zhang, A. Zhang, C. Ling, R. Sheng, X. Li, Q. Yao, and J. Chen, Mater. Sci. Eng., C 127, 112215 (2021).

  11. X. Qu, L. Yan, S. Liu, Y. Tan, J. Xiao, Y. Cao, K. Chen, W. Xiao, B. Li, and X. Liao, J. Mater. Sci., Polym. Ed. 32 (12), 1635(2021).

    CAS  Google Scholar 

  12. X. Wang and Q. Wang, Acc. Chem. Res. 54, 1274 (2021).

    Article  CAS  PubMed  Google Scholar 

  13. J. N. Rodríguez-López, D. J. Lowe, J. Hernández-Ruiz, A. N. Hiner, F. García-Cánovas, and R. N. Thorneley, J. Am. Chem. Soc. 123, 11838 (2001).

    Article  PubMed  Google Scholar 

  14. L.-S. Wang, J. E. Chung, P.-Y. Chan, and M. Kurisawa, Biomaterials 31, 1148 (2010).

    Article  PubMed  Google Scholar 

  15. A. Sala, M. Ehrbar, D. Trentin, R. G. Schoenmakers, J. Vörös, and F. E. Weber, Langmuir 26, 11127 (2010).

    Article  CAS  PubMed  Google Scholar 

  16. L. S. M. Teixeira, S. Bijl, V. V. Pully, C. Otto, R. Jin, J. Feijen, C. A. van Blitterswijk, P. J. Dijkstra, and M. Karperien, Biomaterials 33, 3164 (2012).

    Article  Google Scholar 

  17. M. Khanmohammadi, V. Zolfagharzadeh, Z. Bagher, H. Soltani, and J. Ai, Biomed. Phys. Eng. Express 6, 015022 (2020).

  18. J. I. Kang and K. M. Park, J. Mater. Chem. B 9, 1503 (2021).

    Article  CAS  PubMed  Google Scholar 

  19. L. Li, K. H. Bae, S. Ng, A. Yamashita, and M. Kurisawa, Acta Biomater. 81, 103 (2018).

    Article  CAS  PubMed  Google Scholar 

  20. R. Jin, L. M. Teixeira, P. Dijkstra, C. Van Blitterswijk, M. Karperien, and J. Feijen, Biomaterials 31, 3103 (2010).

    Article  CAS  PubMed  Google Scholar 

  21. C. S. Greenberg, P. J. Birckbichler, and R. H. Rice, FASEB J. 5, 3071 (1991).

    Article  CAS  PubMed  Google Scholar 

  22. S. Sakai and M. Nakahata, Chem. – Asian J.12, 3098 (2017).

    Article  CAS  PubMed  Google Scholar 

  23. R. Jin, L. S. Moreira Teixeira, P. J. Dijkstra, Z. Zhong, C. A. van Blitterswijk, M. Karperien, and J. Feijen, Tissue Eng., Part. An 16, 2429 (2010).

    CAS  Google Scholar 

  24. M. P. Savoca, E. Tonoli, A. G. Atobatele, and E. A. Verderio, Micromachines 9, 562 (2018).

    Article  PubMed Central  Google Scholar 

  25. H. Ando, M. Adachi, K. Umeda, A. Matsuura, M. Nonaka, R. Uchio, H. Tanaka, and M. Motoki, Agric. Biol. Chem. 53, 2613 (1989).

    CAS  Google Scholar 

  26. N. E. Domeradzka, M. W. Werten, F. A. de Wolf, and R. de Vries, Curr. Opin. Biotechnol. 39, 61 (2016).

    Article  CAS  PubMed  Google Scholar 

  27. N. E. Davis, S. Ding, R. E. Forster, D. M. Pinkas, and A. E. Barron, Biomaterials 31, 7288 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. W. Song, J. Ko, Y. H. Choi, and N. S. Hwang, APL Bioeng. 5, 021502 (2021).

  29. S. Sakai, K. Ueda, and M. Taya, Acta Biomater. 24, 152 (2015).

    Article  CAS  PubMed  Google Scholar 

  30. J. Pisano, J. Finlayson, and M. P. Peyton, Science 160, 892 (1968).

    Article  CAS  PubMed  Google Scholar 

  31. S. G. Priglinger, C. S. Alge, D. Kook, M. Thiel, R. Schumann, K. Eibl, A. Yu, A. S. Neubauer, A. Kampik, and U. Welge-Lussen, Invest. Ophthalmol. Visual Sci. 47, 3835 (2006).

    Article  Google Scholar 

  32. S.-Y. Kim, P. Grant, J.-H. Lee, H. C. Pant, and P. M. Steinert, J. Biol. Chem. 274, 30715 (1999).

    Article  CAS  PubMed  Google Scholar 

  33. G. M. Guebitz and G. S. Nyanhongo, Trends Biotechnol. 36, 1040 (2018).

    Article  CAS  PubMed  Google Scholar 

  34. S. Sakai, M. Tsumura, M. Inoue, Y. Koga, K. Fukano, and M. Taya, J. Mater. Chem. B 1, 5067 (2013).

    Article  CAS  PubMed  Google Scholar 

  35. S. G. Priglinger, C. S. Alge, T. C. Kreutzer, A. S. Neubauer, C. Haritoglou, A. Kampik, and U. Welge-Luessen, Invest. Ophthalmol. Visual Sci. 47, 4990 (2006).

    Article  Google Scholar 

  36. M. Griffin, R. Casadio, and C. M. Bergamini, Biochem. J. 368, 377 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. N. Annabi, A. Tamayol, J. A. Uquillas, M. Akbari, L. E. Bertassoni, C. Cha, G. Camci-Unal, M. R. Dokmeci, N. A. Peppas, and A. Khademhosseini, Adv. Mater. 26, 85 (2014).

    Article  CAS  PubMed  Google Scholar 

  38. M. Khanmohammadi, S. Sakai, T. Ashida, and M. Taya, J. Appl. Polym. Sci. 133, 43107 (2016).

    Article  Google Scholar 

  39. Y. Liu, S. Sakai, and M. Taya, Heliyon 2, e00067 (2016).

  40. E. Gantumur, M. Nakahata, M. Kojima, and S. Sakai, Int. J. Bioprint. 6, 250 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. S. A. Irvine, A. Agrawal, B. H. Lee, H. Y. Chua, K. Y. Low, B. C. Lau, M. Machluf, and S. Venkatraman, Biomed. Microdevices 17, 16 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  42. S. V. Murphy and A. Atala, Nat. Biotechnol. 32, 773 (2014).

    Article  CAS  PubMed  Google Scholar 

  43. S. V. Murphy, A. Skardal, and A. Atala, J. Biomed. Mater. Res. 101, 272 (2013).

    Article  Google Scholar 

  44. L. Trachsel, C. Johnbosco, T. Lang, E. M. Benetti, and M. Zenobi-Wong, Biomacromolecules 20, 4502 (2019).

    Article  CAS  PubMed  Google Scholar 

  45. K. Jürgensen, D. Aeschlimann, V. Cavin, M. Genge, and E. Hunziker, J. Bone Jt. Surg., Am. Vol. 79, 185 (1997).

    Article  Google Scholar 

  46. M. H. Kim, J. Lee, J. N. Lee, H. Lee, and W. H. Park, Acta Biomater. 123, 254 (2021).

    Article  CAS  PubMed  Google Scholar 

  47. J. J. Sperinde and L. G. Griffith, Macromolecules 33, 5476 (2000).

    Article  CAS  Google Scholar 

  48. H. Y. Jung, P. Le Thi, K.-H. Bo, J. W. Bae, and K. D. Park, Carbohydr. Polym. 261, 117810 (2021).

  49. H. Zheng, S. Wang, L. Zhou, X. He, Z. Cheng, F. Cheng, Z. Liu, X. Wang, Y. Chen, and Q. Zhang, Chem. Eng. J. 404, 126439 (2021).

  50. C. Hu, L. Long, J. Cao, S. Zhang, and Y. Wang, Chem. Eng. J. 411, 128564 (2021).

  51. Z. Ahmadian, A. Correia, M. Hasany, P. Figueiredo, F. Dobakhti, M. R. Eskandari, S. H. Hosseini, R. Abiri, S. Khorshid, and J. Hirvonen, Adv. Healthcare Mater. 10, 2001122 (2021).

  52. F. Rizzo and N. S. Kehr, Adv. Healthcare Mater. 10, 2001341 (2021).

  53. S. Kobayashi, H. Uyama, and S. Kimura, Chem. Rev. 101, 3793 (2001).

    Article  CAS  PubMed  Google Scholar 

  54. L. S. M. Teixeira, J. Feijen, C. A. van Blitterswijk, P. J. Dijkstra, and M. Karperien, Biomaterials 33, 1281 (2012).

    Article  PubMed  Google Scholar 

  55. D. Eyrich, F. Brandl, B. Appel, H. Wiese, G. Maier, M. Wenzel, R. Staudenmaier, A. Goepferich, and T. Blunk, Biomaterials 28, 55 (2007).

    Article  CAS  PubMed  Google Scholar 

  56. H. Hall, T. Baechi, and J. A. Hubbell, Microvasc. Res. 62, 315 (2001).

    Article  CAS  PubMed  Google Scholar 

  57. G. M. Peretti, J.-W. Xu, L. J. Bonassar, C. H. Kirchhoff, M. J. Yaremchuk, and M. A. Randolph, Tissue Eng. 12, 1151 (2006).

    Article  CAS  PubMed  Google Scholar 

  58. J. J. Sperinde and L. G. Griffith, Macromolecules 30, 5255 (1997).

    Article  CAS  Google Scholar 

  59. B. H. Hu and P. Messersmith, Orthod. Craniofacial Res. 8, 145 (2005).

    Article  Google Scholar 

  60. C. W. Yung, W. E. Bentley, and T. A. Barbari, J. Biomed. Mater. Res. 95, 25 (2010).

    Article  Google Scholar 

  61. C. Yung, L. Wu, J. Tullman, G. Payne, W. Bentley, and T. Barbari, J. Biomed. Mater. Res. 83, 1039 (2007).

    Article  CAS  Google Scholar 

  62. M. K. McHale, L. A. Setton, and A. Chilkoti, Tissue Eng. 11, 1768 (2005).

    Article  CAS  PubMed  Google Scholar 

  63. M. E. R. Jones and P. B. Messersmith, Biomaterials 28, 5215 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. T. Chen, D. A. Small, M. K. McDermott, W. E. Bentley, and G. F. Payne, Biomacromolecules 4, 1558 (2003).

    Article  CAS  PubMed  Google Scholar 

  65. L.-Q. Wu, W. E. Bentley, and G. F. Payne, Int. J. Artif. Organs 34, 215 (2011).

    Article  CAS  PubMed  Google Scholar 

  66. H. Yamamoto, S. Kuno, A. Nagai, A. Nishida, S. Yamauchi, and K. Ikeda, Int. J. Biol. Macromol.12, 305 (1990).

    Article  CAS  PubMed  Google Scholar 

  67. T. Chen, H. D. Embree, E. M. Brown, M. M. Taylor, and G. F. Payne, Biomaterials 24, 2831 (2003).

    Article  CAS  PubMed  Google Scholar 

  68. T. Chen, H. D. Embree, L. Q. Wu, and G. F. Payne, Biopolymers 64, 292 (2002).

    Article  CAS  PubMed  Google Scholar 

  69. K. Yamada, T. Chen, G. Kumar, O. Vesnovsky, L. T. Topoleski, and G. F. Payne, Biomacromolecules 1, 252 (2000).

    Article  CAS  PubMed  Google Scholar 

  70. A. Demolliens, C. Boucher, Y. Durocher, M. Jolicoeur, M. D. Buschmann, and G. De Crescenzo, Bioconjugate Chem. 19, 1849 (2008).

    Article  CAS  Google Scholar 

  71. A. Anghileri, R. Lantto, K. Kruus, C. Arosio, and G. Freddi, J. Biotechnol. 127, 508 (2007).

    Article  CAS  PubMed  Google Scholar 

  72. G. Freddi, A. Anghileri, S. Sampaio, J. Buchert, P. Monti, and P. Taddei, J. Biotechnol. 125, 281 (2006).

    Article  CAS  PubMed  Google Scholar 

  73. D. Mishra, B. Bhunia, I. Banerjee, P. Datta, S. Dhara, and T. K. Maiti, Mater. Sci. Eng., C 31, 1295 (2011).

    Article  CAS  Google Scholar 

  74. A. K. Joshi, L. Zhang, V. S. Rangan, and S. Smith, J. Biol. Chem. 278, 33142 (2003).

    Article  CAS  PubMed  Google Scholar 

  75. K. A. Mosiewicz, K. Johnsson, and M. P. Lutolf, J. Am. Chem. Soc. 132, 5972 (2010).

    Article  CAS  PubMed  Google Scholar 

  76. S. E. D’Souza, M. H. Ginsberg, and E. F. Plow, Trends Biochem. Sci. 16, 246 (1991).

    Article  PubMed  Google Scholar 

  77. H. Ton-That, G. Liu, S. K. Mazmanian, K. F. Faull, and O. Schneewind, Proc. Natl. Acad. Sci. U. S. A. 96, 12424 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. H. Mao, S. A. Hart, A. Schink, and B. A. Pollok, J. Am. Chem. Soc. 126, 2670 (2004).

    Article  CAS  PubMed  Google Scholar 

  79. E. Cambria, K. Renggli, C. C. Ahrens, C. D. Cook, C. Kroll, A. T. Krueger, B. Imperiali, and L. G. Griffith, Biomacromolecules 16, 2316 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. C. R. Kothapalli and A. Ramamurthi, J. Tissue Eng. Regener. Med. 3, 655 (2009).

    Article  CAS  Google Scholar 

  81. W. Kong, C. Lyu, H. Liao, and Y. Du, Biomed. Mater. 16, 062005 (2021).

  82. E. L. Bakota, L. Aulisa, K. M. Galler, and J. D. Hartgerink, Biomacromolecules 12, 82 (2010).

    Article  PubMed  Google Scholar 

  83. H. M. Kagan and W. Li, J. Cell Biochem. 88, 660 (2003).

    Article  CAS  PubMed  Google Scholar 

  84. Y.-K. I. Lau, A. M. Gobin, and J. L. West, Ann. Biomed. Eng. 34, 1239 (2006).

    Article  PubMed  Google Scholar 

  85. J. J. Hwang and S. I. Stupp, J. Biomater. Sci., Polym. Ed. 11, 1023 (2000).

    Article  CAS  Google Scholar 

  86. S. E. Grieshaber, T. Nie, C. Yan, S. Zhong, S. S. Teller, R. J. Clifton, D. J. Pochan, K. L. Kiick, and X. Jia, Macromol. Chem. Phys. 212, 229 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Y. Gao, Y. Kuang, Z.-F Guo, Z. Guo, I. J. Krauss, and B. Xu, J. Am. Chem. Soc. 131, 13576 (2009).

    Article  CAS  PubMed  Google Scholar 

  88. Z. Yang, G. Liang, and B. Xu, Acc. Chem. Res. 41, 315 (2008).

    Article  CAS  PubMed  Google Scholar 

  89. Z. Yang, H. Gu, D. Fu, P. Gao, J. K. Lam, and B. Xu, Adv. Mater. 16, 1440 (2004).

    Article  CAS  Google Scholar 

  90. S. Toledano, R. J. Williams, V. Jayawarna, and R. V. Ulijn, J. Am. Chem. Soc. 128, 1070 (2006).

    Article  CAS  PubMed  Google Scholar 

  91. Z. Yang, P.-L. Ho, G. Liang, K. H. Chow, Q. Wang, Y. Cao, Z. Guo, and B. Xu, J. Am. Chem. Soc. 129, 266 (2007).

    Article  CAS  PubMed  Google Scholar 

  92. Z. Yang, G. Liang, Z. Guo, Z. Guo, and B. Xu, Angew. Chem. Int. Ed. 8216 (2007).

    Google Scholar 

  93. Z. Yang, G. Liang, L. Wang, and B. Xu, J. Am. Chem. Soc. 128, 3038 (2006).

    Article  CAS  PubMed  Google Scholar 

  94. R. J. Williams, R. J. Mart, and R. V. Ulijn, J. Pept. Sci. 94, 107 (2010).

    Article  CAS  Google Scholar 

  95. R. J. Williams, A. M. Smith, R. Collins, N. Hodson, A. K. Das, and R. V. Ulijn, Nat. Nanotechnol. 4, 19 (2009).

    Article  CAS  PubMed  Google Scholar 

  96. Z. A. Schnepp, R. Gonzalez-McQuire, and S. Mann, Adv. Mater. 18, 1869 (2006).

    Article  CAS  Google Scholar 

  97. D. Yuan, J. Shi, X. Du, Y. Huang, Y. Gao, and B. Xu, J. Mater. Chem. B 4, 1318 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. H. Toda, M. Yamamoto, H. Uyama, and Y. Tabata, Acta Biomater. 29, 215 (2016)

    Article  CAS  PubMed  Google Scholar 

  99. B. J. Ryan, N. Carolan, and C. Ó’Fágáin, Trends Biotechnol. 24, 355 (2006).

    Article  CAS  PubMed  Google Scholar 

  100. S. Sakai, M. Khanmohammadi, A. B. Khoshfetrat, and M. Taya, Carbohydr. Polym. 111, 404 (2014).

    Article  CAS  PubMed  Google Scholar 

  101. N. Q. Tran, Y. K. Joung, E. Lih, K. M. Park, and K. D. Park, Biomacromolecules 11, 617 (2010).

    Article  CAS  PubMed  Google Scholar 

  102. S. J. Sofia, A. Singh, and D. L. Kaplan, J. Macromol. Sci., Part A: Pure Appl. Chem. 39, 1151 (2002).

    Article  Google Scholar 

  103. M. Kurisawa, J. E. Chung, Y. Y. Yang, S. J. Gao, and H. Uyama, Chem. Commun. 14, 4312 (2005).

    Article  Google Scholar 

  104. S. Bagheri, Z. Bagher, S. Hassanzadeh, S. Simorgh, S. K. Kamrava, V. T. Nooshabadi, R. Shabani, M. Jalessi, and M. Khanmohammadi, J. Biomed. Mater. Res., Part A 109, 649 (2021).

    CAS  Google Scholar 

  105. M. Khanmohammadi, S. Sakai, and M. Taya, Int. J. Biol. Macromol. 104, 204 (2017).

    Article  CAS  PubMed  Google Scholar 

  106. M. Khanmohammadi, S. Sakai, and M. Taya, Int. J. Biol. Macromol. 97, 308 (2017).

    Article  CAS  PubMed  Google Scholar 

  107. R. Jin, C. Hiemstra, Z. Zhong, and J. Feijen, Biomaterials 28, 2791 (2007).

    Article  CAS  PubMed  Google Scholar 

  108. S. Sakai, Y. Yamada, T. Zenke, and K. Kawakami, J. Mater. Chem. 19, 230 (2009).

    Article  CAS  Google Scholar 

  109. A. B. Khoshfetrat, M. Khanmohammadi, S. Sakai, and M. Taya, Int. J. Biol. Macromol. 92, 892 (2016).

    Article  CAS  PubMed  Google Scholar 

  110. S. Sakai, Y. Liu, E. J. Mah, and M. Taya, Biofabrication 5, 015012 (2013).

  111. V. Kuzmenko, D. Hägg, G. Toriz, and P. Gatenholm, Carbohydr. Polym. 102, 862 (2014).

    Article  CAS  PubMed  Google Scholar 

  112. Y. Ogushi, S. Sakai, and K. Kawakami, J. Biosci. Bioeng. 104, 30 (2007).

    Article  CAS  PubMed  Google Scholar 

  113. K. M. Park, Y. M. Shin, Y. K. Joung, H. Shin, and K. D. Park, Biomacromolecules 11, 706 (2010).

    Article  CAS  PubMed  Google Scholar 

  114. Y. Sun, Z. Deng, Y. Tian, and C. Lin, J. Appl. Polym. Sci. 127, 40 (2013).

    Article  CAS  Google Scholar 

  115. F. Lee, K. H. Bae, and M. Kurisawa, Biomed. Mater. 11, 014101 (2015).

  116. Y. Liu, S. Sakai, S. Kawa, and M. Taya, Anal, Chem. 86, 11592 (2014).

    Article  CAS  Google Scholar 

  117. S. Sakai and M. Taya, ACS Macro Lett. 3, 972 (2014).

    Article  CAS  Google Scholar 

  118. A. Darr and A. Calabro, J. Mater. Sci.: Mater. Med. 20, 33 (2009).

    CAS  Google Scholar 

  119. F. Lee, J. E. Chung, and M. Kurisawa, J. Controlled Release 134, 186 (2009).

    Article  CAS  Google Scholar 

  120. R. Jin, L. S. M. Teixeira, P. J. Dijkstra, C. A. van Blitterswijk, M. Karperien, and J. Feijen, J. Controlled Release 152, 186 (2011).

    Article  CAS  Google Scholar 

  121. K. S. Kim, S. J. Park, J.-A. Yang, J.-H. Jeon, S. H. Bhang, B.-S. Kim, and S. K. Hahn, Acta Biomater. 7, 666 (2011).

    Article  CAS  PubMed  Google Scholar 

  122. N. C. Veitch, Phytochemistry 65, 249 (2004).

    Article  CAS  PubMed  Google Scholar 

  123. H. Musso, Angew. Chem., Int. Ed. 2, 723 (1963).

    Article  Google Scholar 

  124. F. Lee, J. E. Chung, and M. Kurisawa, Soft Matter. 4, 880 (2008).

    Article  CAS  PubMed  Google Scholar 

  125. A. Schmidt, J. T. Schumacher, J. Reichelt, H.-J. Hecht, and U. Bilitewski, Anal. Chem. 74, 3037 (2002).

    Article  CAS  PubMed  Google Scholar 

  126. Q. Huang, Q. Huang, R. A. Pinto, K. Griebenow, R. Schweitzer-Stenner, and W. J. Weber, J. Am. Chem. Soc. 127, 1431 (2005).

    Article  CAS  PubMed  Google Scholar 

  127. T. Kudanga, G. S. Nyanhongo, G. M. Guebitz, and S. Burton, Enzyme Microb. Technol. 48, 195 (2011).

    Article  CAS  PubMed  Google Scholar 

  128. L. Wang, B. Xu, Y. Nong, P. Wang, Y. Yu, C. Deng, J. Yuan, and Q, Wang, Int. J. Biol. Macromol. 160, 795 (2020).

    Article  CAS  PubMed  Google Scholar 

  129. D. Huber, G. Tegl, M. Baumann, E. Sommer, E. G. Gorji, N. Borth, G. Schleining, G. S. Nyanhongo, and G. M. Guebitz, Carbohydr. Polym. 157, 814 (2017).

    Article  CAS  PubMed  Google Scholar 

  130. K. M. Park and S. Gerecht, Nat. Commun. 5, 4075 (2014).

    Article  CAS  PubMed  Google Scholar 

  131. M. Kurisawa, F. Lee, L.-S. Wang, and J. E. Chung, J. Mater. Chem. 20, 5371 (2010).

    Article  CAS  Google Scholar 

  132. K. Engberg and C. W. Frank, Biomed. Mater. 6, 055006 (2011).

  133. P. van de Wetering, A. T. Metters, R. G. Schoenmakers, and J. A. Hubbell, J. Controlled Release 102, 619 (2005).

    Article  CAS  Google Scholar 

  134. J. B. Leach and C. E. Schmidt, Biomaterials 26, 125 (2005).

    Article  CAS  PubMed  Google Scholar 

  135. K. Xu, F. Lee, S. J. Gao, J. E. Chung, H. Yano, and M. Kurisawa, J. Controlled Release 166, 203 (2013).

    Article  CAS  Google Scholar 

  136. S. E. Sakiyama-Elbert and J. A. Hubbell, J. Controlled Release 65, 389 (2000).

    Article  CAS  Google Scholar 

  137. J. H. Choi, J. Y. Jang, Y. K. Joung, M. H. Kwon, and K. D. Park, J. Controlled Release 147, 420 (2010).

    Article  CAS  Google Scholar 

  138. R. DeVolder, E. Antoniadou, and H. Kong, J. Controlled Release 172, 30 (2013).

    Article  CAS  Google Scholar 

  139. M. Dehghan-Niri, M. Tavakol, E. Vasheghani-Farahani, and F. Ganji, J. Biomater. Appl. 29, 1343 (2015).

    Article  CAS  PubMed  Google Scholar 

  140. A. J. Engler, S. Sen, H. L. Sweeney, and D. E. Discher, Cell 126, 677 (2006).

    Article  CAS  PubMed  Google Scholar 

  141. K. Ghosh and D. E. Ingber, Adv. Drug. Delivery Rev. 59, 1306 (2007).

    Article  CAS  Google Scholar 

  142. J. W. Bae, J. H. Choi, Y. Lee, and K. D. Park, J. Tissue Eng. Regener. Med. 9, 1225 (2015).

    Article  CAS  Google Scholar 

  143. L.-S. Wang, J. Boulaire, P. P. Chan, J. E. Chung, and M. Kurisawa, Biomaterials 31, 8608 (2010).

    Article  CAS  PubMed  Google Scholar 

  144. T. C. Lim, W. S. Toh, L.-S. Wang, M. Kurisawa, and M. Spector, Biomaterials 33, 3446 (2012).

    Article  CAS  PubMed  Google Scholar 

  145. R. K. Sharma, Q. Zhou, and P. A. Netland, Brain Res. 1243, 19 (2008).

    Article  CAS  PubMed  Google Scholar 

  146. B. C. White, J. M. Sullivan, D. J. DeGracia, B. J. O’Neil, R. W. Neumar, L. I. Grossman, J. A. Rafols, and G. S. Krause, J. Neurol. Sci 179, 1 (2000).

    Article  CAS  PubMed  Google Scholar 

  147. L.-S. Wang, C. Du, W. S. Toh, A. C. Wan, S. J. Gao, and M. Kurisawa, Biomaterials 35, 2207 (2014).

    Article  CAS  PubMed  Google Scholar 

  148. W. S. Toh, T. C. Lim, M. Kurisawa, and M. Spector, Biomaterials 33, 3835 (2012).

    Article  CAS  PubMed  Google Scholar 

  149. A. A. Amini and L. S. Nair, Adv. Healthcare Mater. 3, 897 (2014).

    Article  CAS  Google Scholar 

  150. K.-C. Kuo, R.-Z. Lin, H.-W. Tien, P.-Y. Wu, Y.-C. Li, J. M. Melero-Martin, and Y.-C. Chen, Acta Biomater. 27, 151 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. S. Sakai, Y. Liu, M. Sengoku, and M. Taya, Biomaterials 53, 494 (2015).

    Article  CAS  PubMed  Google Scholar 

  152. A. Morelli, M. Betti, D. Puppi, C. Bartoli, M. Gazzarri, and F. Chiellini, Macromol. Chem. Phys. 217, 581 (2016).

    Article  CAS  Google Scholar 

  153. M. Wartenberg, F. Dönmez, F. C. Ling, H. Acker, J. Hescheler, and H. Sauer, FASEB J. 15, 995 (2001).

    CAS  PubMed  Google Scholar 

  154. F. Hirschhaeuser, H. Menne, C. Dittfeld, J. West, W. Mueller-Klieser, and L. A. Kunz-Schughart, J. Biotechnol. 148, 3 (2010).

    Article  CAS  PubMed  Google Scholar 

  155. L. De Ridder, M. Cornelissen, and D. De Ridder, Crit. Rev. Oncol. Hematol. 36, 107 (2000).

    Article  CAS  PubMed  Google Scholar 

  156. W. D. Spotnitz and S. Burks, Transfusion 48, 1502 (2008).

    Article  PubMed  Google Scholar 

  157. S. Liu, X. Liu, Y. Ren, P. Wang, Y. Pu, R. Yang, X. Wang, X. Tan, Z. Ye, and V. Maurizot, ACS Appl. Mater. Interfaces 12, 27876 (2020).

    Article  CAS  PubMed  Google Scholar 

  158. C. Vauthier, C. Dubernet, E. Fattal, H. Pinto-Alphandary, and P. Couvreur, Adv. Drug Delivery Rev. 55, 519 (2003).

    Article  CAS  Google Scholar 

  159. E. Lih, J. S. Lee, K. M. Park, and K. D. Park, Acta Biomater. 8, 3261 (2012).

    Article  CAS  PubMed  Google Scholar 

  160. R. Jayakumar, M. Prabaharan, P. S. Kumar, S. Nair, and H. Tamura, Biotechnol. Adv. 29, 322 (2011).

    Article  CAS  PubMed  Google Scholar 

  161. N. Q. Tran, Y. K. Joung, E. Lih, and K. D. Park, Biomacromolecules 12, 2872 (2011).

    Article  CAS  PubMed  Google Scholar 

  162. M. Kurisawa, J. E. Chung, H. Uyama, and S. Kobayashi, Biomacromolecules 4, 1394 (2003).

    Article  CAS  PubMed  Google Scholar 

  163. S. Zavada, N. McHardy, and T. Scott, J. Mater. Chem. B 2, 2598 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. S. R. Zavada, T. Battsengel, and T. F. Scott, Int. J. Biol. Macromol. 17, 195 (2016).

    Google Scholar 

  165. Q. Wei, J. Duan, G. Ma, W. Zhang, Q. Wang, and Z. Hu, J. Mater. Chem. B 7, 2220 (2019).

    Article  CAS  PubMed  Google Scholar 

  166. J. A. Akkara, J. Wang, D.-P. Yang, and K. E. Gonsalves, Macromolecules 33, 2377 (2000).

    Article  CAS  Google Scholar 

  167. S. Sakai, K. Moriyama, K. Taguchi, and K. Kawakami, Biomacromolecules 11, 2179 (2010).

    Article  CAS  PubMed  Google Scholar 

  168. C. Pierach, I. Bossenmaier, R. Cardinal, M. Weimer, and C. Watson, Klin Wochenschr. 58, 829 (1980).

    Article  CAS  PubMed  Google Scholar 

  169. D. M. Bissell, J. Hepatol. 6, 1 (1988).

    Article  CAS  PubMed  Google Scholar 

  170. M. Kohri, H. Fukushima, T. Taniguchi, and T. Nakahira, Polym. J. 42, 952 (2010).

    Article  CAS  Google Scholar 

  171. S. Nagarajan, R. Nagarajan, F. Bruno, L. A. Samuelson, and J. Kumar, Green Chem. 11, 334 (2009).

    Article  CAS  Google Scholar 

  172. E. Byun, J. H. Ryu, and H. Lee, Chem. Commun. 50, 2869 (2014).

    Article  CAS  Google Scholar 

  173. J. W. Bae, B. Y. Kim, E. Lih, J. H. Choi, Y. Lee, and K. D. Park, Chem. Commun. 50, 13710 (2014).

    Article  CAS  Google Scholar 

  174. A. M. Gardner, F.-H. Xu, C. Fady, F. J. Jacoby, D. C. Duffey, Y. Tu, and A. Lichtenstein, Free Radicals Biol. Med. 22, 73 (1997).

    Article  CAS  Google Scholar 

  175. M. Gülden, A. Jess, J. Kammann, E. Maser, and H. Seibert, Free Radicals Biol. Med. 49, 1298 (2010).

    Article  Google Scholar 

  176. S. Sakai, K. Ueda, E. Gantumur, M. Taya, and M. Nakamura, Macromol. Rapid Commun. 39, 1700534 (2018).

  177. J. Shi, X. Du, Y. Huang, J. Zhou, D. Yuan, D. Wu, Y. Zhang, R. Haburcak, I. R. Epstein, and B. Xu, J. Am. Chem. Soc. 137, 26 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  178. K. N. Plunkett, K. L. Berkowski, and J. S. Moore, Biomacromolecules 6, 632 (2005).

    Article  CAS  PubMed  Google Scholar 

  179. Y. Xie, R. Huang, W. Qi, Y. Wang, R. Su, and Z. He, J. Mater. Chem. B 4, 844 (2016).

    Article  CAS  PubMed  Google Scholar 

  180. H. Liu, Y. Li, Z. Lyu, Y. Wan, X. Li, H. Chen, H. Chen, and X. Li, J. Mater. Chem. B 2, 8303 (2014).

    Article  CAS  PubMed  Google Scholar 

  181. V. Jayawarna, M. Ali, T. A. Jowitt, A. F. Miller, A. Saiani, J. E. Gough, and R. V. Ulijn, Adv. Mater. 18, 611 (2006).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Chemistry, Kharazmi University, P. O. Box 15719-14911, Tehran, Iran

    Elham Badali

  2. Skull Base Research Center, The Five Senses Institute, Hazrat Rasoul Akram Hospital, Iran University of Medical Sciences (IUMS), Tehran, Iran

    Mahshid Hosseini, Maryam Mohajer, Sajad Hassanzadeh & Mehdi Khanmohammadi

  3. Department of Tissue Engineering, Faculty of Advanced Medical Sciences, Tabriz University of Medical Sciences, Tabriz, Iran

    Sepideh Saghati

  4. Department of Chemistry, Ångström Laboratory, Uppsala University, Uppsala, Sweden

    Jöns Hilborn

Authors
  1. Elham Badali
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mahshid Hosseini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maryam Mohajer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sajad Hassanzadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sepideh Saghati
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jöns Hilborn
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mehdi Khanmohammadi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

E.B., M.M., M.H., and S.S. contributed to the reports’ primary draft preparation and review. E.B. and S.H. worked on the schematic figures of reactions. M.H., J.H., and M.Kh. committed to data analysis and editing the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Mehdi Khanmohammadi.

Ethics declarations

The authors declare that they have no conflicts of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Elham Badali, Hosseini, M., Mohajer, M. et al. Enzymatic Crosslinked Hydrogels for Biomedical Application. Polym. Sci. Ser. A 63 (Suppl 1), S1–S22 (2021). https://doi.org/10.1134/S0965545X22030026

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0965545X22030026

Search

Navigation