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Hyaluronic Acid-based Biomimetic Hydrogels for Tissue Engineering and Medical Applications

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Abstract

Hyaluronic acid (HA), an essential component of extracellular matrix (ECM), plays an important role in various cellular activities, including migration, proliferation, and differentiation. Not only its structural and biological properties, but also properties such as biocompatibility, biodegradability, and low immunogenicity make HA a promising biomaterial for tissue engineering and regenerative medicine. HA has been widely utilized as a hydrogel to form complex polymer networks, which can be chemically modified owing to the abundance of functional groups. To closely recapitulate native tissues, many approaches have been developed through chemical modification, incorporation of various biomaterials and biomolecules based on biomimetics, and fabrication techniques. Thus, HA-based hydrogels can be designed to exhibit specific properties or functions for targeted tissues, capable of maintaining or replacing structural and biological properties. This review highlights recent efforts in developing HA-based hydrogels as ECM-mimetic scaffolds and bio-inspired functional biomaterials in the fields of tissue engineering and regenerative medicine as well as their medical applications.

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References

  1. Burdick, J. A. and G. D. Prestwich (2011) Hyaluronic acid hydrogels for biomedical applications. Adv. Mater. 23: H41–H56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Hachet, E., H. Van Den Berghe, E. Bayma, M. R. Block, and R. Auzély-Velty (2012) Design of biomimetic cell-interactive substrates using hyaluronic acid hydrogels with tunable mechanical properties. Biomacromolecules. 13: 1818–1827.

    Article  CAS  PubMed  Google Scholar 

  3. Hong, S., K. Yang, B. Kang, C. Lee, I. T. Song, E. Byun, K. I. Park, S. W. Cho, and H. Lee (2013) Hyaluronic acid catechol: a biopolymer exhibiting a pH-dependent adhesive or cohesive property for human neural stem cell engineering. Adv. Funct. Mater. 23: 1774–1780.

    Article  CAS  Google Scholar 

  4. Fisher, S. A., R. Y. Tam, and M. S. Shoichet (2014) Tissue mimetics: engineered hydrogel matrices provide biomimetic environments for cell growth. Tissue Eng. Part A. 20: 895–898.

    Article  PubMed  Google Scholar 

  5. Xu, X., A. K. Jha, D. A. Harrington, M. C. Farach-Carson, and X. Jia (2012) Hyaluronic acid-based hydrogels: from a natural polysaccharide to complex networks. Soft Matter. 8: 3280–3294.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Lam, J., N. F. Truong, and T. Segura (2014) Design of cell-matrix interactions in hyaluronic acid hydrogel scaffolds. Acta Biomater. 10: 1571–1580.

    Article  CAS  PubMed  Google Scholar 

  7. Li, H., Z. Qi, S. Zheng, Y. Chang, W. Kong, C. Fu, Z. Yu, X. Yang, and S. Pan (2019) The application of hyaluronic acid-based hydrogels in bone and cartilage tissue engineering. Adv. Mater. Sci. Eng. 2019: 3027303.

    Article  Google Scholar 

  8. Wang, T. W. and M. Spector (2009) Development of hyaluronic acid-based scaffolds for brain tissue engineering. Acta Biomater. 5: 2371–2384.

    Article  CAS  PubMed  Google Scholar 

  9. Sahana, T. G. and P. D. Rekha (2018) Biopolymers: Applications in wound healing and skin tissue engineering. Mol. Biol. Rep. 45: 2857–2867.

    Article  CAS  PubMed  Google Scholar 

  10. Kaczmarek, B., A. Sionkowska, J. Kozlowska, and A. Osyczka (2018) New composite materials prepared by calcium phosphate precipitation in chitosan/collagen/hyaluronic acid sponge cross-linked by EDC/NHS. Int. J. Biol. Macromol. 107: 247–253.

    Article  CAS  PubMed  Google Scholar 

  11. Choi, S., J. S. Lee, J. Shin, M. S. Lee, D. Kang, N. S. Hwang, H. Lee, H. S. Yang, and S. W. Cho (2020) Osteoconductive hybrid hyaluronic acid hydrogel patch for effective bone formation. J. Control. Release. 327: 571–583.

    Article  CAS  PubMed  Google Scholar 

  12. Fischer, R. L., M. G. McCoy, and S. A. Grant (2012) Electrospinning collagen and hyaluronic acid nanofiber meshes. J. Mater. Sci. Mater. Med. 23: 1645–1654.

    Article  CAS  PubMed  Google Scholar 

  13. Chen, W., S. Chen, Y. Morsi, H. El-Hamshary, M. El-Newhy, C. Fan, and X. Mo (2016) Superabsorbent 3D scaffold based on electrospun nanofibers for cartilage tissue engineering. ACS Appl. Mater. Interfaces. 8: 24415–24425.

    Article  CAS  PubMed  Google Scholar 

  14. Bauer, T. W. and G. F. Muschler (2000) Bone graft materials: an overview of the basic science. Clin. Orthop. Relat. Res. 371: 10–27.

    Article  Google Scholar 

  15. Sander, E. A., K. A. Lynch, and S. T. Boyce (2014) Development of the mechanical properties of engineered skin substitutes after grafting to full-thickness wounds. J. Biomech. Eng. 136: 051008.

    Article  PubMed  Google Scholar 

  16. Tavsanli, B. and O. Okay (2017) Mechanically strong hyaluronic acid hydrogels with an interpenetrating network structure. Eur. Polym. J. 94: 185–195.

    Article  CAS  Google Scholar 

  17. Tavsanli, B., V. Can, and O. Okay (2015) Mechanically strong triple network hydrogels based on hyaluronan and poly(N,N-dimethylacrylamide). Soft Matter. 11: 8517–8524.

    Article  CAS  PubMed  Google Scholar 

  18. Ma, X., X. Liu, P. Wang, X. Wang, R. Yang, S. Liu, Z. Ye, and B. Chi (2020) Covalently adaptable hydrogel based on hyaluronic acid and poly(γ-glutamic acid) for potential load-bearing tissue engineering. ACS Appl. Bio Mater. 3: 4036–4043.

    Article  CAS  PubMed  Google Scholar 

  19. Zhang, L., J. Hu, and K. A. Athanasiou (2009) The role of tissue engineering in articular cartilage repair and regeneration. Crit. Rev. Biomed. Eng. 37: 1–57.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Lee, C. R., A. J. Grodzinsky, and M. Spector (2001) The effects of cross-linking of collagen-glycosaminoglycan scaffolds on compressive stiffness, chondrocyte-mediated contraction, proliferation and biosynthesis. Biomaterials. 22: 3145–3154.

    Article  CAS  PubMed  Google Scholar 

  21. Bryant, S. J. and K. S. Anseth (2002) Hydrogel properties influence ECM production by chondrocytes photoencapsulated in poly(ethylene glycol) hydrogels. J. Biomed. Mater. Res. 59: 63–72.

    Article  CAS  PubMed  Google Scholar 

  22. Fahy, N., M. Alini, and M. J. Stoddart (2018) Mechanical stimulation of mesenchymal stem cells: Implications for cartilage tissue engineering. J. Orthop. Res. 36: 52–63.

    PubMed  Google Scholar 

  23. Sun, M., X. Sun, Z. Wang, S. Guo, G. Yu, and H. Yang (2018) Synthesis and properties of gelatin methacryloyl (GelMA) hydrogels and their recent applications in load-bearing tissue. Polymers. 10: 1290.

    Article  PubMed Central  CAS  Google Scholar 

  24. Feng, Q., H. Gao, H. Wen, H. Huang, Q. Li, M. Liang, Y. Liu, H. Dong, and X. Cao (2020) Engineering the cellular mechanical microenvironment to regulate stem cell chondrogenesis: Insights from a microgel model. Acta Biomater. 113: 393–406.

    Article  CAS  PubMed  Google Scholar 

  25. Wu, Y., M. J. Stoddart, K. Wuertz-Kozak, S. Grad, M. Alini, and S. J. Ferguson (2017) Hyaluronan supplementation as a mechanical regulator of cartilage tissue development under joint-kinematic-mimicking loading. J. R. Soc. Interface. 14: 20170255.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Lee, K. B. L., J. H. P. Hui, I. C. Song, L. Ardany, and E. H. Lee (2007) Injectable mesenchymal stem cell therapy for large cartilage defects—a porcine model. Stem Cells. 25: 2964–2971.

    Article  PubMed  Google Scholar 

  27. Li, L., X. Duan, Z. Fan, L. Chen, F. Xing, Z. Xu, Q. Chen, and Z. Xiang (2018) Mesenchymal stem cells in combination with hyaluronic acid for articular cartilage defects. Sci. Rep. 8: 9900.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Cho, H., H. Kim, Y. G. Kim, and K. Kim (2019) Recent clinical trials in adipose-derived stem cell mediated osteoarthritis treatment. Biotechnol. Bioprocess Eng. 24: 839–853.

    Article  CAS  Google Scholar 

  29. Toh, W. S., E. H. Lee, X. M. Guo, J. K. Y. Chan, C. H. Yeow, A. B. Choo, and T. Cao (2010) Cartilage repair using hyaluronan hydrogel-encapsulated human embryonic stem cell-derived chondrogenic cells. Biomaterials. 31: 6968–6980.

    Article  CAS  PubMed  Google Scholar 

  30. Yao, Y., P. Wang, X. Li, Y. Xu, G. Lu, Q. Jiang, Y. Sun, Y. Fan, and X. Zhang (2020) A di-self-crosslinking hyaluronan-based hydrogel combined with type I collagen to construct a biomimetic injectable cartilage-filling scaffold. Acta Biomater. 111: 197–207.

    Article  CAS  PubMed  Google Scholar 

  31. Wu, S. C., P. Y. Huang, C. H. Chen, B. Teong, J. W. Chen, C. W. Wu, J. K. Chang, and M. L. Ho (2018) Hyaluronan microenvironment enhances cartilage regeneration of human adipose-derived stem cells in a chondral defect model. Int. J. Biol. Macromol. 119: 726–740.

    Article  CAS  PubMed  Google Scholar 

  32. La Gatta, A., G. Ricci, A. Stellavato, M. Cammarota, R. Filosa, A. Papa, A. D’Agostino, M. Portaccio, I. Delfino, M. De Rosa, and C. Schiraldi (2017) Hyaluronan hydrogels with a low degree of modification as scaffolds for cartilage engineering. Int. J. Biol. Macromol. 103: 978–989.

    Article  CAS  PubMed  Google Scholar 

  33. Wang, C. Z., R. Eswaramoorthy, T. H. Lin, C. H. Chen, Y. C. Fu, C. K. Wang, S. C. Wu, G. J. Wang, J. K. Chang, and M. L. Ho (2018) Enhancement of chondrogenesis of adipose-derived stem cells in HA-PNIPAAm-CL hydrogel for cartilage regeneration in rabbits. Sci. Rep. 8: 10526.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Zhang, Y., Y. Cao, H. Zhao, L. Zhang, T. Ni, Y. Liu, Z. An, M. Liu, and R. Pei (2020) An injectable BMSC-laden enzyme-catalyzed crosslinking collagen-hyaluronic acid hydrogel for cartilage repair and regeneration. J. Mater. Chem. B. 8: 4237–4244.

    Article  CAS  PubMed  Google Scholar 

  35. Lin, H., A. M. Beck, K. Shimomura, J. Sohn, M. R. Fritch, Y. Deng, E. J. Kilroy, Y. Tang, P. G. Alexander, and R. S. Tuan (2019) Optimization of photocrosslinked gelatin/hyaluronic acid hybrid scaffold for the repair of cartilage defect. J. Tissue Eng. Regen. Med. 13: 1418–1429.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Deng, Y., A. X. Sun, K. J. Overholt, G. Z. Yu, M. R. Fritch, P. G. Alexander, H. Shen, R. S. Tuan, and H. Lin (2019) Enhancing chondrogenesis and mechanical strength retention in physiologically relevant hydrogels with incorporation of hyaluronic acid and direct loading of TGF-β. Acta Biomater. 83: 167–176.

    Article  CAS  PubMed  Google Scholar 

  37. Jooybar, E., M. J. Abdekhodaie, M. Alvi, A. Mousavi, M. Karperien, and P. J. Dijkstra (2019) An injectable platelet lysate-hyaluronic acid hydrogel supports cellular activities and induces chondrogenesis of encapsulated mesenchymal stem cells. Acta Biomater. 83: 233–244.

    Article  CAS  PubMed  Google Scholar 

  38. Gobbi, A. and G. P. Whyte (2019) Long-term clinical outcomes of one-stage cartilage repair in the knee with hyaluronic acid-based scaffold embedded with mesenchymal stem cells sourced from bone marrow aspirate concentrate. Am. J. Sports. Med. 47: 1621–1628.

    Article  PubMed  Google Scholar 

  39. Mohammadi, F., N. Tanideh, S. M. Samani, and F. Ahmadi (2019) Efficacy of a hybrid system of hyaluronic acid and collagen loaded with prednisolone and TGF-β3 for cartilage regeneration in rats. J. Drug Deliv. Sci. Technol. 51: 55–62.

    Article  CAS  Google Scholar 

  40. Park, S. H., J. Y. Seo, J. Y. Park, Y. B. Ji, K. Kim, H. S. Choi, S. Choi, J. H. Kim, B. H. Min, and M. S. Kim (2019) An injectable, click-crosslinked, cytomodulin-modified hyaluronic acid hydrogel for cartilage tissue engineering. NPG Asia Mater. 11: 30.

    Article  CAS  Google Scholar 

  41. Gu, B. K., D. J. Choi, S. J. Park, M. S. Kim, C. M. Kang, and C. H. Kim (2016) 3-dimensional bioprinting for tissue engineering applications. Biomater. Res. 20: 12.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Singh, Y. P., A. Bandyopadhyay, and B. B. Mandal (2019) 3D Bioprinting using cross-linker-free silk-gelatin bioink for cartilage tissue engineering. ACS Appl. Mater. Interfaces. 11: 33684–33696.

    Article  CAS  PubMed  Google Scholar 

  43. Gopinathan, J. and I. Noh (2018) Click chemistry-based injectable hydrogels and bioprinting inks for tissue engineering applications. Tissue Eng. Regen. Med. 15: 531–546.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Galarraga, J. H., M. Y. Kwon, and J. A. Burdick (2019) 3D bioprinting via an in situ crosslinking technique towards engineering cartilage tissue. Sci. Rep. 9: 19987.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Antich, C., J. de Vicente, G. Jiménez, C. Chocarro, E. Carrillo, E. Montañez, P. Gálvez-Martín, and J. A. Marchal (2020) Bio-inspired hydrogel composed of hyaluronic acid and alginate as a potential bioink for 3D bioprinting of articular cartilage engineering constructs. Acta Biomater. 106: 114–123.

    Article  CAS  PubMed  Google Scholar 

  46. Baroli, B. (2009) From natural bone grafts to tissue engineering therapeutics: brainstorming on pharmaceutical formulative requirements and challenges. J. Pharm. Sci. 98: 1317–1375.

    Article  CAS  PubMed  Google Scholar 

  47. Qu, H., H. Fu, Z. Han, and Y. Sun (2019) Biomaterials for bone tissue engineering scaffolds: a review. RSC Adv. 9: 26252–26262.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Mallick, S., Z. Beyene, D. K. Suman, A. Madhual, B. N. Singh, and P. Srivastava (2019) Strategies towards orthopaedic tissue engineered graft generation: Current scenario and application. Biotechnol. Bioprocess Eng. 24: 854–869.

    Article  CAS  Google Scholar 

  49. Zhou, Y., Z. Gu, J. Liu, K. Huang, G. Liu, and J. Wu (2020) Arginine based poly (ester amide)/ hyaluronic acid hybrid hydrogels for bone tissue engineering. Carbohydr. Polym. 230: 115640.

    Article  CAS  PubMed  Google Scholar 

  50. Chae, H. J., R. K. Park, H. T. Chung, J. S. Kang, M. S. Kim, D. Y. Choi, B. G. Bang, and H. R. Kim (1997) Nitric oxide is a regulator of bone remodelling. J. Pharm. Pharmacol. 49: 897–902.

    Article  CAS  PubMed  Google Scholar 

  51. Jahromi, M. T., G. Yao, and M. Cerruti (2013) The importance of amino acid interactions in the crystallization of hydroxyapatite. J. R. Soc. Interface. 10: 20120906.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Tavafoghi, M. and M. Cerruti (2016) The role of amino acids in hydroxyapatite mineralization. J. R. Soc. Interface. 13: 20160462.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Bendtsen, S. T., S. P. Quinnell, and M. Wei (2017) Development of a novel alginate-polyvinyl alcohol-hydroxyapatite hydrogel for 3D bioprinting bone tissue engineered scaffolds. J. Biomed. Mater. Res. A. 105: 1457–1468.

    Article  CAS  PubMed  Google Scholar 

  54. Nikpour, P., H. Salimi-Kenari, F. Fahimipour, S. M. Rabiee, M. Imani, E. Dashtimoghadam, and L. Tayebi (2018) Dextran hydrogels incorporated with bioactive glass-ceramic: Nanocomposite scaffolds for bone tissue engineering. Carbohydr. Polym. 190: 281–294.

    Article  CAS  PubMed  Google Scholar 

  55. Gantar, A., L. P. da Silva, J. M. Oliveira, A. P. Marques, V. M. Correlo, S. Novak, and R. L. Reis (2014) Nanoparticulate bioactive-glass-reinforced gellan-gum hydrogels for bone-tissue engineering. Mater. Sci. Eng. C. 43: 27–36.

    Article  CAS  Google Scholar 

  56. Taz, M., P. Makkar, K. M. Imran, D. W. Jang, Y. S. Kim, and B. T. Lee (2019) Bone regeneration of multichannel biphasic calcium phosphate granules supplemented with hyaluronic acid. Mater. Sci. Eng. C. 99: 1058–1066.

    Article  CAS  Google Scholar 

  57. Lee, S. J., H. Nah, D. N. Heo, K. H. Kim, J. M. Seok, M. Heo, H. J. Moon, D. Lee, J. S. Lee, S. Y. An, Y. S. Hwang, W. K. Ko, S. J. Kim, S. Sohn, S. A. Park, S. Y. Park, and I. K. Kwon (2020) Induction of osteogenic differentiation in a rat calvarial bone defect model using an in situ forming graphene oxide incorporated glycol chitosan/oxidized hyaluronic acid injectable hydrogel. Carbon. 168: 264–277.

    Article  CAS  Google Scholar 

  58. Zhang, L. T., R. M. Liu, Y. Luo, Y. J. Zhao, D. X. Chen, C. Y. Yu, and J. H. Xiao (2019) Hyaluronic acid promotes osteogenic differentiation of human amniotic mesenchymal stem cells via the TGF-β/Smad signalling pathway. Life Sci. 232: 116669.

    Article  CAS  PubMed  Google Scholar 

  59. Boeckel, D. G., P. Sesterheim, T. R. Peres, A. H. Augustin, K. M. Wartchow, D. C. Machado, G. G. Fritscher, and E. R. Teixeira (2019) Adipogenic mesenchymal stem cells and hyaluronic acid as a cellular compound for bone tissue engineering. J. Craniofac. Surg. 30: 777–783.

    Article  PubMed  Google Scholar 

  60. Zhang, Y., H. Chen, T. Zhang, Y. Zan, T. Ni, Y. Cao, J. Wang, M. Liu, and R. Pei (2019) Injectable hydrogels from enzyme-catalyzed crosslinking as BMSCs-laden scaffold for bone repair and regeneration. Mater. Sci. Eng. C. 96: 841–849.

    Article  CAS  Google Scholar 

  61. Makvandi, P., G. W. Ali, F. Della Sala, W. I. Abdel-Fattah, and A. Borzacchiello (2020) Hyaluronic acid/corn silk extract based injectable nanocomposite: A biomimetic antibacterial scaffold for bone tissue regeneration. Mater. Sci. Eng. C. 107: 110195.

    Article  CAS  Google Scholar 

  62. Price, R. D., S. Myers, I. M. Leigh, and H. A. Navsaria (2005) The role of hyaluronic acid in wound healing. Am. J. Clin. Dermatol. 6: 393–402.

    Article  PubMed  Google Scholar 

  63. Hussain, Z., H. E. Thu, H. Katas, and S. N. A. Bukhari (2017) Hyaluronic acid-based biomaterials: a versatile and smart approach to tissue regeneration and treating traumatic, surgical, and chronic wounds. Polym. Rev. 57: 594–630.

    Article  CAS  Google Scholar 

  64. Zhao, J. Y., J. K. Chai, H. F. Song, J. Zhang, M. H. Xu, and Y. D. Liang (2013) Influence of hyaluronic acid on wound healing using composite porcine acellular dermal matrix grafts and autologous skin in rabbits. Int. Wound J. 10: 562–572.

    Article  PubMed  Google Scholar 

  65. Dong, Y., M. Cui, J. Qu, X. Wang, S. H. Kwon, J. Barrera, N. Elvassore, and G. C. Gurtner (2020) Conformable hyaluronic acid hydrogel delivers adipose-derived stem cells and promotes regeneration of burn injury. Acta Biomater. 108: 56–66.

    Article  CAS  PubMed  Google Scholar 

  66. Li, W. J., C. T. Laurencin, E. J. Caterson, R. S. Tuan, and F. K. Ko (2002) Electrospun nanofibrous structure: a novel scaffold for tissue engineering. J. Biomed. Mater. Res. 60: 613–621.

    Article  CAS  PubMed  Google Scholar 

  67. Nair, L. S., S. Bhattacharyya, and C. T. Laurencin (2004) Development of novel tissue engineering scaffolds via electrospinning. Expert Opin. Biol. Ther. 4: 659–668.

    Article  CAS  PubMed  Google Scholar 

  68. Chantre, C. O., G. M. Gonzalez, S. Ahn, L. Cera, P. H. Campbell, S. P. Hoerstrup, and K. K. Parker (2019) Porous biomimetic hyaluronic acid and extracellular matrix protein nanofiber scaffolds for accelerated cutaneous tissue repair. ACS Appl. Mater. Interfaces. 11: 45498–45510.

    Article  CAS  PubMed  Google Scholar 

  69. Preston, M. and L. S. Sherman (2011) Neural stem cell niches: critical roles for the hyaluronan-based extracellular matrix in neural stem cell proliferation and differentiation. Front. Biosci. (Schol. Ed.). 3: 1165–1179.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Seidlits, S. K., J. Liang, R. D. Bierman, A. Sohrabi, J. Karam, S. M. Holley, C. Cepeda, and C. M. Walthers (2019) Peptide-modified, hyaluronic acid-based hydrogels as a 3D culture platform for neural stem/progenitor cell engineering. J. Biomed. Mater. Res. A. 107: 704–718.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Cui, F. Z., W. M. Tian, S. P. Hou, Q. Y. Xu, and I. S. Lee (2006) Hyaluronic acid hydrogel immobilized with RGD peptides for brain tissue engineering. J. Mater. Sci. Mater. Med. 17: 1393–1401.

    Article  CAS  PubMed  Google Scholar 

  72. Hou, S., Q. Xu, W. Tian, F. Cui, Q. Cai, J. Ma, and I. S. Lee (2005) The repair of brain lesion by implantation of hyaluronic acid hydrogels modified with laminin. J. Neurosci. Methods. 148: 60–70.

    Article  CAS  PubMed  Google Scholar 

  73. Patel, R., M. Santhosh, J. K. Dash, R. Karpoormath, A. Jha, J. Kwak, M. Patel, and J. H. Kim (2019) Ile-Lys-Val-ala-Val (IKVAV) peptide for neuronal tissue engineering. Polym. Adv. Technol. 30: 4–12.

    Article  CAS  Google Scholar 

  74. Thomas, R. C., P. Vu, S. P. Modi, P. E. Chung, R. C. Landis, Z. Z. Khaing, J. G. Hardy, and C. E. Schmidt (2017) Sacrificial crystal templated hyaluronic acid hydrogels as biomimetic 3D tissue scaffolds for nerve tissue regeneration. ACS Biomater. Sci. Eng. 3: 1451–1459.

    Article  CAS  PubMed  Google Scholar 

  75. Wen, Y., S. Yu, Y. Wu, R. Ju, H. Wang, Y. Liu, Y. Wang, and Q. Xu (2016) Spinal cord injury repair by implantation of structured hyaluronic acid scaffold with PLGA microspheres in the rat. Cell Tissue Res. 364: 17–28.

    Article  CAS  PubMed  Google Scholar 

  76. Zarei-Kheirabadi, M., H. Sadrosadat, A. Mohammadshirazi, R. Jaberi, F. Sorouri, F. Khayyatan, and S. Kiani (2020) Human embryonic stem cell-derived neural stem cells encapsulated in hyaluronic acid promotes regeneration in a contusion spinal cord injured rat. Int. J. Biol. Macromol. 148: 1118–1129.

    Article  CAS  PubMed  Google Scholar 

  77. Patterson, J., R. Siew, S. W. Herring, A. S. P. Lin, R. Guldberg, and P. S. Stayton (2010) Hyaluronic acid hydrogels with controlled degradation properties for oriented bone regeneration. Biomaterials. 31: 6772–6781.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Migliore, A. and M. Granata (2008) Intra-articular use of hyaluronic acid in the treatment of osteoarthritis. Clin. Interv. Aging. 3: 365–369.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Bowman, S., M. E. Awad, M. W. Hamrick, M. Hunter, and S. Fulzele (2018) Recent advances in hyaluronic acid based therapy for osteoarthritis. Clin. Transl. Med. 7: 6.

    Article  PubMed  PubMed Central  Google Scholar 

  80. Miki, D., K. Dastgheib, T. Kim, A. Pfister-Serres, K. A. Smeds, M. Inoue, D. L. Hatchell, and M. W. Grinstaff (2002) A photopolymerized sealant for corneal lacerations. Cornea. 21: 393–399.

    Article  PubMed  Google Scholar 

  81. Higashide, T. and K. Sugiyama (2008) Use of viscoelastic substance in ophthalmic surgery-focus on sodium hyaluronate. Clin. Ophthalmol. 2: 21–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Hong, Y., F. Zhou, Y. Hua, X. Zhang, C. Ni, D. Pan, Y. Zhang, D. Jiang, L. Yang, Q. Lin, Y. Zou, D. Yu, D. E. Arnot, X. Zou, L. Zhu, S. Zhang, and H. Ouyang (2019) A strongly adhesive hemostatic hydrogel for the repair of arterial and heart bleeds. Nat. Commun. 10: 2060.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. Gan, D., W. Xing, L. Jiang, J. Fang, C. Zhao, F. Ren, L. Fang, K. Wang, and X. Lu (2019) Plant-inspired adhesive and tough hydrogel based on Ag-Lignin nanoparticles-triggered dynamic redox catechol chemistry. Nat. Commun. 10: 1487.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. Ghobril, C. and M. W. Grinstaff (2015) The chemistry and engineering of polymeric hydrogel adhesives for wound closure: a tutorial. Chem. Soc. Rev. 44: 1820–1835.

    Article  CAS  PubMed  Google Scholar 

  85. Brubaker, C. E., H. Kissler, L. J. Wang, D. B. Kaufman, and P. B. Messersmith (2010) Biological performance of mussel-inspired adhesive in extrahepatic islet transplantation. Biomaterials. 31: 420–427.

    Article  CAS  PubMed  Google Scholar 

  86. Liang, Y., X. Zhao, P. X. Ma, B. Guo, Y. Du, and X. Han (2019) pH-responsive injectable hydrogels with mucosal adhesiveness based on chitosan-grafted-dihydrocaffeic acid and oxidized pullulan for localized drug delivery. J. Colloid Interface Sci. 536: 224–234.

    Article  CAS  PubMed  Google Scholar 

  87. Shin, J., J. S. Lee, C. Lee, H. J. Park, K. Yang, Y. Jin, J. H. Ryu, K. S. Hong, S. H. Moon, H. M. Chung, H. S. Yang, S. H. Um, J. W. Oh, D. I. Kim, H. Lee, and S. W. Cho (2015) Tissue adhesive catechol-modified hyaluronic acid hydrogel for effective, minimally invasive cell therapy. Adv. Funct. Mater. 25: 3814–3824.

    Article  CAS  Google Scholar 

  88. Lee, C., J. Shin, J. S. Lee, E. Byun, J. H. Ryu, S. H. Um, D. I. Kim, H. Lee, and S. W. Cho (2013) Bioinspired, calcium-free alginate hydrogels with tunable physical and mechanical properties and improved biocompatibility. Biomacromolecules. 14: 2004–2013.

    Article  CAS  PubMed  Google Scholar 

  89. Kim, K., K. Kim, J. H. Ryu, and H. Lee (2015) Chitosan-catechol: A polymer with long-lasting mucoadhesive properties. Biomaterials. 52: 161–170.

    Article  CAS  PubMed  Google Scholar 

  90. Park, H. J., Y. Jin, J. Shin, K. Yang, C. Lee, H. S. Yang, and S. W. Cho (2016) Catechol-functionalized hyaluronic acid hydrogels enhance angiogenesis and osteogenesis of human adipose-derived stem cells in critical tissue defects. Biomacromolecules. 17: 1939–1948.

    Article  CAS  PubMed  Google Scholar 

  91. Koivusalo, L., M. Kauppila, S. Samanta, V. S. Parihar, T. Ilmarinen, S. Miettinen, O. P. Oommen, and H. Skottman (2019) Tissue adhesive hyaluronic acid hydrogels for sutureless stem cell delivery and regeneration of corneal epithelium and stroma. Biomaterials. 225: 119516.

    Article  CAS  PubMed  Google Scholar 

  92. Kang, B., J. Shin, H. J. Park, C. Rhyou, D. Kang, S. J. Lee, Y. S. Yoon, S. W. Cho, and H. Lee (2018) High-resolution acoustophoretic 3D cell patterning to construct functional collateral cylindroids for ischemia therapy. Nat. Commun. 9: 5402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Zhou, D., S. Li, M. Pei, H. Yang, S. Gu, Y. Tao, D. Ye, Y. Zhou, W. Xu, and P. Xiao (2020) Dopamine-modified hyaluronic acid hydrogel adhesives with fast-forming and high tissue adhesion. ACS Appl. Mater. Interfaces. 12: 18225–18234.

    Article  CAS  PubMed  Google Scholar 

  94. Zhou, Y., L. Kang, Z. Yue, X. Liu, and G. G. Wallace (2020) Composite tissue adhesive containing catechol-modified hyaluronic acid and poly-l-lysine. ACS Appl. Bio Mater. 3: 628–638.

    Article  CAS  PubMed  Google Scholar 

  95. Cho, J. H., J. S. Lee, J. Shin, E. J. Jeon, S. An, Y. S. Choi, and S. W. Cho (2018) Ascidian-inspired fast-forming hydrogel system for versatile biomedical applications: Pyrogallol chemistry for dual modes of crosslinking mechanism. Adv. Funct. Mater. 28: 1705244.

    Article  CAS  Google Scholar 

  96. Taylor, S. W., B. Kammerer, and E. Bayer (1997) New perspectives in the chemistry and biochemistry of the tunichromes and related compounds. Chem. Rev. 97: 333–346.

    Article  CAS  PubMed  Google Scholar 

  97. Shin, J., S. Choi, J. H. Kim, J. H. Cho, Y. Jin, S. Kim, S. Min, S. K. Kim, D. Choi, and S. W. Cho (2019) Tissue tapes—phenolic hyaluronic acid hydrogel patches for off-the-shelf therapy. Adv. Funct. Mater. 29: 1903863.

    Article  CAS  Google Scholar 

  98. Yuk, H., C. E. Varela, C. S. Nabzdyk, X. Mao, R. F. Padera, E. T. Roche, and X. Zhao (2019) Dry double-sided tape for adhesion of wet tissues and devices. Nature. 575: 169–174.

    Article  CAS  PubMed  Google Scholar 

  99. Sivashanmugam, A., R. A. Kumar, M. V. Priya, S. V. Nair, and R. Jayakumar (2015) An overview of injectable polymeric hydrogels for tissue engineering. Eur. Polym. J. 72: 543–565.

    Article  CAS  Google Scholar 

  100. Kim, B. S. and C. S. Cho (2018) Injectable hydrogels for regenerative medicine. Tissue Eng. Regen. Med. 15: 511–512.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Sontyana, A. G., A. P. Mathew, K. H. Cho, S. Uthaman, and I. K. Park (2018) Biopolymeric in situ hydrogels for tissue engineering and bioimaging applications. Tissue Eng. Regen. Med. 15: 575–590.

    Article  PubMed  PubMed Central  Google Scholar 

  102. Liu, M., X. Zeng, C. Ma, H. Yi, Z. Ali, X. Mou, S. Li, Y. Deng, and N. He (2017) Injectable hydrogels for cartilage and bone tissue engineering. Bone Res. 5: 17014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Singh, A., M. Corvelli, S. A. Unterman, K. A. Wepasnick, P. McDonnell, and J. H. Elisseeff (2014) Enhanced lubrication on tissue and biomaterial surfaces through peptide-mediated binding of hyaluronic acid. Nat. Mater. 13: 988–995.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Oh, E. J., S. W. Kang, B. S. Kim, G. Jiang, I. H. Cho, and S. K. Hahn (2008) Control of the molecular degradation of hyaluronic acid hydrogels for tissue augmentation. J. Biomed. Mater. Res. A. 86: 685–693.

    Article  PubMed  CAS  Google Scholar 

  105. Won, H. R., Y. S. Kim, J. E. Won, Y. S. Shin, and C. H. Kim (2018) The application of fibrin/hyaluronic acid-poly(L-lactic-co-glycolic acid) construct in augmentation rhinoplasty. Tissue Eng. Regen. Med. 15: 223–230.

    Article  CAS  PubMed  Google Scholar 

  106. Lee, S. Y., J. H. Park, M. Yang, M. J. Baek, M. H. Kim, J. Lee, A. Khademhosseini, D. D. Kim, and H. J. Cho (2020) Ferrous sulfate-directed dual-cross-linked hyaluronic acid hydrogels with long-term delivery of donepezil. Int. J. Pharm. 582: 119309.

    Article  CAS  PubMed  Google Scholar 

  107. Waite, J. H. (2017) Mussel adhesion-essential footwork. J. Exp. Biol. 220: 517–530.

    Article  PubMed  PubMed Central  Google Scholar 

  108. Holten-Andersen, N., M. J. Harrington, H. Birkedal, B. P. Lee, P. B. Messersmith, K. Y. C. Lee, and J. H. Waite (2011) pH-induced metal-ligand cross-links inspired by mussel yield self-healing polymer networks with near-covalent elastic moduli. Proc. Natl. Acad. Sci. USA. 108: 2651–2655.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Wu, D., X. Shi, F. Zhao, S. T. F. Chilengue, L. Deng, A. Dong, D. Kong, W. Wang, and J. Zhang (2019) An injectable and tumor-specific responsive hydrogel with tissue-adhesive and nanomedicine-releasing abilities for precise locoregional chemotherapy. Acta Biomater. 96: 123–136.

    Article  CAS  PubMed  Google Scholar 

  110. Yang, M., S. Y. Lee, S. Kim, J. S. Koo, J. H. Seo, D. I. Jeong, C. Hwang, J. Lee, and H. J. Cho (2020) Selenium and dopamine-crosslinked hyaluronic acid hydrogel for chemophotothermal cancer therapy. J. Control. Release. 324: 750–764.

    Article  CAS  PubMed  Google Scholar 

  111. Chung, E. J., J. S. Choi, J. Shin, H. N. Cho, S. Kim, J. Y. Park, Y. Lee, Y. Kim, H. G. Wu, S. W. Cho, and S. K. Kwon (2020) Prevention of irradiation-induced damage to salivary glands by local delivery of adipose-derived stem cells via hyaluronic acid-based hydrogels. J. Ind. Eng. Chem. 90: 47–57.

    Article  CAS  Google Scholar 

  112. Li, Y., J. Wen, M. Qin, Y. Cao, H. Ma, and W. Wang (2017) Single-molecule mechanics of catechol-iron coordination bonds. ACS Biomater. Sci. Eng. 3: 979–989.

    Article  CAS  PubMed  Google Scholar 

  113. Guo, Z., K. Ni, D. Wei, and Y. Ren (2015) F3+-induced oxidation and coordination cross-linking in catechol-chitosan hydrogels under acidic pH conditions. RSC Adv. 5: 37377–37384.

    Article  CAS  Google Scholar 

  114. Lee, J. S., J. H. Cho, S. An, J. Shin, S. Choi, E. J. Jeon, and S. W. Cho (2019) In situ self-cross-linkable, long-term stable hyaluronic acid filler by gallol autoxidation for tissue augmentation and wrinkle correction. Chem. Mater. 31: 9614–9624.

    Article  CAS  Google Scholar 

  115. Ishii, T., T. Mori, T. Tanaka, D. Mizuno, R. Yamaji, S. Kumazawa, T. Nakayama, and M. Akagawa (2008) Covalent modification of proteins by green tea polyphenol (-)-epigallocatechin-3-gallate through autoxidation. Free Radic. Biol. Med. 45: 1384–1394.

    Article  CAS  PubMed  Google Scholar 

  116. Shin, M., J. H. Galarraga, M. Y. Kwon, H. Lee, and J. A. Burdick (2019) Gallol-derived ECM-mimetic adhesive bioinks exhibiting temporal shear-thinning and stabilization behavior. Acta Biomater. 95: 165–175.

    Article  CAS  PubMed  Google Scholar 

  117. Shin, M., K. H. Song, J. C. Burrell, D. K. Cullen, and J. A. Burdick (2019) Injectable and conductive granular hydrogels for 3D printing and electroactive tissue support. Adv. Sci. 6: 1901229.

    Article  CAS  Google Scholar 

  118. Shin, M. and H. Lee (2017) Gallol-rich hyaluronic acid hydrogels: shear-thinning, protein accumulation against concentration gradients, and degradation-resistant properties. Chem. Mater. 29: 8211–8220.

    Article  CAS  Google Scholar 

  119. Lee, F., J. E. Chung, K. Xu, and M. Kurisawa (2015) Injectable degradation-resistant hyaluronic acid hydrogels cross-linked via the oxidative coupling of green tea catechin. ACS Macro Lett. 4: 957–960.

    Article  CAS  PubMed  Google Scholar 

  120. Liu, C., K. H. Bae, A. Yamashita, J. E. Chung, and M. Kurisawa (2017) Thiol-mediated synthesis of hyaluronic acid-epigallocatechin-3-O-gallate conjugates for the formation of injectable hydrogels with free radical scavenging property and degradation resistance. Biomacromolecules. 18: 3143–3155.

    Article  CAS  PubMed  Google Scholar 

  121. Gupta, R. C., R. Lall, A. Srivastava, and A. Sinha (2019) Hyaluronic acid: molecular mechanisms and therapeutic trajectory. Front. Vet. Sci. 6: 192.

    Article  PubMed  PubMed Central  Google Scholar 

  122. An, S., E. J. Jeon, J. Jeon, and S. W. Cho (2019) A serotonin-modified hyaluronic acid hydrogel for multifunctional hemostatic adhesives inspired by a platelet coagulation mediator. Mater. Horiz. 6: 1169–1178.

    Article  CAS  Google Scholar 

  123. Liu, Y., J. Yang, Z. Luo, D. Li, J. Lu, Q. Wang, Y. Xiao, and X. Zhang (2019) Development of an injectable thiolated icariin functionalized collagen/hyaluronic hydrogel to promote cartilage formation in vitro and in vivo. J. Mater. Chem. B. 7: 2845–2854.

    Article  CAS  PubMed  Google Scholar 

  124. Yang, J., Y. Liu, L. He, Q. Wang, L. Wang, T. Yuan, Y. Xiao, Y. Fan, and X. Zhang (2018) Icariin conjugated hyaluronic acid/collagen hydrogel for osteochondral interface restoration. Acta Biomater. 74: 156–167.

    Article  CAS  PubMed  Google Scholar 

  125. Duan, Y., K. Li, H. Wang, T. Wu, Y. Zhao, H. Li, H. Tang, and W. Yang (2020) Preparation and evaluation of curcumin grafted hyaluronic acid modified pullulan polymers as a functional wound dressing material. Carbohydr. Polym. 238: 116195.

    Article  CAS  PubMed  Google Scholar 

  126. Garcia, J. M. S., A. Panitch, and S. Calve (2019) Functionalization of hyaluronic acid hydrogels with ECM-derived peptides to control myoblast behavior. Acta Biomater. 84: 169–179.

    Article  CAS  Google Scholar 

  127. Xing, D., L. Ma, and C. Gao (2017) A bioactive hyaluronic acid-based hydrogel cross-linked by Diels-Alder reaction for promoting neurite outgrowth of PC12 cells. J. Bioact. Compat. Polym. 32: 382–396.

    Article  CAS  Google Scholar 

  128. Wang, L. S., F. Lee, J. Lim, C. Du, A. C. A. Wan, S. S. Lee, and M. Kurisawa (2014) Enzymatic conjugation of a bioactive peptide into an injectable hyaluronic acid-tyramine hydrogel system to promote the formation of functional vasculature. Acta Biomater. 10: 2539–2550.

    Article  CAS  PubMed  Google Scholar 

  129. Ren, Y., H. Zhang, W. Qin, B. Du, L. Liu, and J. Yang (2020) A collagen mimetic peptide-modified hyaluronic acid hydrogel system with enzymatically mediated degradation for mesenchymal stem cell differentiation. Mater. Sci. Eng. C. 108: 110276.

    Article  CAS  Google Scholar 

  130. Zhu, M., S. Lin, Y. Sun, Q. Feng, G. Li, and L. Bian (2016) Hydrogels functionalized with N-cadherin mimetic peptide enhance osteogenesis of hMSCs by emulating the osteogenic niche. Biomaterials. 77: 44–52.

    Article  CAS  PubMed  Google Scholar 

  131. Cosgrove, B. D., K. L. Mui, T. P. Driscoll, S. R. Caliari, K. D. Mehta, R. K. Assoian, J. A. Burdick, and R. L. Mauck (2016) N-cadherin adhesive interactions modulate matrix mechanosensing and fate commitment of mesenchymal stem cells. Nat. Mater. 15: 1297–1306.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Gallagher, L. B., E. B. Dolan, J. O’Sullivan, R. Levey, B. L. Cavanagh, L. Kovarova, M. Pravda, V. Velebny, T. Farrell, F. J. O’Brien, and G. P. Duffy (2020) Pre-culture of mesenchymal stem cells within RGD-modified hyaluronic acid hydrogel improves their resilience to ischaemic conditions. Acta Biomater. 107: 78–90.

    Article  CAS  PubMed  Google Scholar 

  133. Zhang, X., P. Zhou, Y. Zhao, M. Wang, and S. Wei (2016) Peptide-conjugated hyaluronic acid surface for the culture of human induced pluripotent stem cells under defined conditions. Carbohydr. Polym. 136: 1061–1064.

    Article  CAS  PubMed  Google Scholar 

  134. Lin, Z., T. Wu, W. Wang, B. Li, M. Wang, L. Chen, H. Xia, and T. Zhang (2019) Biofunctions of antimicrobial peptide-conjugated alginate/hyaluronic acid/collagen wound dressings promote wound healing of a mixed-bacteria-infected wound. Int. J. Biol. Macromol. 140: 330–342.

    Article  CAS  PubMed  Google Scholar 

  135. Mohamed, M. F., A. Abdelkhalek, and M. N. Seleem (2016) Evaluation of short synthetic antimicrobial peptides for treatment of drug-resistant and intracellular Staphylococcus aureus. Sci. Rep. 6: 29707.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

S.A. and S.C. contributed equally to this work. The authors sincerely thank Sooyeon Kim of Yonsei University for her support in preparing the illustrations. This work was supported by the Bio & Medical Technology Development Program (2020M3A9I4038455) of the National Research Foundation of Korea (NRF) funded by the Ministry of Science and ICT (MSIT), Republic of Korea. This work was also supported by the Technology Innovation Program (Alchemist Project, 20012378) funded by the Ministry of Trade, Industry & Energy (MOTIE), Republic of Korea. The authors declare no conflict of interest.

Neither ethical approval nor informed consent was required for this study.

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  1. Department of Biotechnology, Yonsei University, Seoul, 03722, Korea

    Soohwan An, Soojeong Choi, Sungjin Min & Seung-Woo Cho

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An, S., Choi, S., Min, S. et al. Hyaluronic Acid-based Biomimetic Hydrogels for Tissue Engineering and Medical Applications. Biotechnol Bioproc E 26, 503–516 (2021). https://doi.org/10.1007/s12257-020-0343-8

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