Seeing through collagen: integrative pro-regenerative corneal implants for clearer future

seeing-through-collagen:-integrative-pro-regenerative-corneal-implants-for-clearer-future
Seeing through collagen: integrative pro-regenerative corneal implants for clearer future

References

  1. DelMonte, D. W. & Kim, T. Anatomy and physiology of the cornea. J. Cataract Refract. Surg. 37, 588–598 (2011).

    Google Scholar 

  2. Ludwig, P. E., Lopez, M. J. & Sevensma, K. E. Anatomy, head and neck, eye cornea (StatPearls Publishing LLC, 2017).

  3. Williams, K. A., Irani, Y. D. & Klebe, S. Novel therapeutic approaches for corneal disease. Discov. Med. 15, 291–299 (2013).

    Google Scholar 

  4. Garg, P., Krishna, P., Stratis, A. & Gopinathan, U. The value of corneal transplantation in reducing blindness. Eye 19, 1106–1114 (2005).

    Google Scholar 

  5. Tidu, A., Schanne-Klein, M.-C. & Borderie, V. M. Development, structure, and bioengineering of the human corneal stroma: a review of collagen-based implants. Exp. Eye Res. 200, 108256 (2020).

    Google Scholar 

  6. Tidke, S. C. & Tidake, P. A review of corneal blindness: causes and management. Cureus 14, 1–7 (2022).

  7. Li, Z. et al. Preventing corneal blindness caused by keratitis using artificial intelligence. Nat. Commun. 12, 3738 (2021).

    Google Scholar 

  8. Matthyssen, S., Van den Bogerd, B., Dhubhghaill, S. N., Koppen, C. & Zakaria, N. Corneal regeneration: a review of stromal replacements. Acta Biomater. 69, 31–41 (2018).

    Google Scholar 

  9. Armitage, W. J., Dick, A. D. & Bourne, W. M. Predicting endothelial cell loss and long-term corneal graft survival. Invest. Ophthalmol. Vis. Sci. 44, 3326–3331 (2003).

    Google Scholar 

  10. Faye, P. A. et al. Focus on cell therapy to treat corneal endothelial diseases. Exp. Eye Res. 204, 108462 (2021).

    Google Scholar 

  11. Beuerman, R. W. & Pedroza, L. Ultrastructure of the human cornea. Microsc. Res. Tech. 33, 320–335 (1996).

    Google Scholar 

  12. NCLC, G. M. B. Sixth layer to human cornea discovered by UK researcher. Optometry 5, 1 (2013).

    Google Scholar 

  13. West-Mays, J. A. & Dwivedi, D. J. The keratocyte: corneal stromal cell with variable repair phenotypes. Int. J. Biochem. Cell Biol. 38, 1625–1631 (2006).

    Google Scholar 

  14. Palchesko, R. N., Carrasquilla, S. D. & Feinberg, A. W. Natural biomaterials for corneal tissue engineering, repair, and regeneration. Adv. Healthc. Mater. 7, 1701434 (2018).

    Google Scholar 

  15. Chirila, T. V. An overview of the development of artificial corneas with porous skirts and the use of PHEMA for such an application. Biomaterials 22, 3311–3317 (2001).

    Google Scholar 

  16. Meek, K. M. & Knupp, C. Corneal structure and transparency. Prog. Retin. Eye Res. 49, 1–16 (2015).

    Google Scholar 

  17. Balters, L. & Reichl, S. 3D bioprinting of corneal models: a review of the current state and future outlook. J. Tissue Eng. 14, 20417314231197793 (2023).

    Google Scholar 

  18. Holland, G. et al. Artificial cornea: past, current, and future directions. Front. Med. 8, 770780 (2021).

    Google Scholar 

  19. Wong, Y. L., Liu, S. & Walkden, A. Current perspectives on corneal transplantation (Part 2). Clin. Ophthalmol. 16, 647–659 (2022).

  20. Nonpassopon, M., Niparugs, M. & Cortina, M. S. Boston type 1 keratoprosthesis: updated perspectives. Clin. Ophthalmol. 14, 1189–1200 (2020).

  21. Hicks, C. et al. Corneal replacement using a synthetic hydrogel cornea, AlphaCor™: device, preliminary outcomes and complications. Eye 17, 385–392 (2003).

    Google Scholar 

  22. Gain, P. et al. Global survey of corneal transplantation and eye banking. JAMA Ophthalmol. 134, 167–173 (2016).

    Google Scholar 

  23. Meek, K. M. Corneal collagen-its role in maintaining corneal shape and transparency. Biophys. Rev. 1, 83–93 (2009).

    Google Scholar 

  24. Merrett, K. et al. Tissue-engineered recombinant human collagen-based corneal substitutes for implantation: performance of type I versus type III collagen. Invest. Ophthalmol. Vis. Sci. 49, 3887–3894 (2008).

    Google Scholar 

  25. Sarrigiannidis, S. O. et al. A tough act to follow: collagen hydrogel modifications to improve mechanical and growth factor loading capabilities. Mater. Today Bio 10, 100098 (2021).

    Google Scholar 

  26. Everaerts, F., Torrianni, M., Hendriks, M. & Feijen, J. Quantification of carboxyl groups in carbodiimide crosslinked collagen sponges. J. Biomed. Mater. Res. A. 83, 1176–1183 (2007).

    Google Scholar 

  27. Lin, K. et al. Advanced collagen-based biomaterials for regenerative biomedicine. Adv. Funct. Mater. 29, 1804943 (2019).

    Google Scholar 

  28. Ricard-Blum, S. The collagen family. Cold Spring Harb. perspect. biol. 3, a004978 (2011).

    Google Scholar 

  29. Shoulders, M. D. & Raines, R. T. Collagen structure and stability. Annu. Rev. Biochem. 78, 929–958 (2009).

    Google Scholar 

  30. Sharma, S., Dwivedi, S., Chandra, S., Srivastava, A. & Vijay, P. Collagen: a brief analysis. J. Oral Maxillofac. Pathol. 10, 11–17 (2019).

  31. Lister, J. An address on the catgut ligature. Br. Med. J. 1, 219 (1881).

    Google Scholar 

  32. Macewen, W. Clinical lectures on some points connected with the treatment of wounds. Br. Med. J. 1, 185 (1881).

    Google Scholar 

  33. Rezvani Ghomi, E., Nourbakhsh, N., Akbari Kenari, M., Zare, M. & Ramakrishna, S. Collagen-based biomaterials for biomedical applications. J. Biomed. Mater. Res. B Appl. Biomater. 109, 1986–1999 (2021).

    Google Scholar 

  34. Chattopadhyay, S. & Raines, R. T. Collagen-based biomaterials for wound healing. Biopolymers 101, 821–833 (2014).

    Google Scholar 

  35. Khare, E. et al. Discovering design principles of collagen molecular stability using a genetic algorithm, deep learning, and experimental validation. Proc. Natl. Acad. Sci. USA 119, e2209524119 (2022).

    Google Scholar 

  36. Ramshaw, J. A., Shah, N. K. & Brodsky, B. Gly-XY tripeptide frequencies in collagen: a context for host-guest triple-helical peptides. J. Struct. Biol. 122, 86–91 (1998).

    Google Scholar 

  37. Li, P. & Wu, G. Roles of dietary glycine, proline, and hydroxyproline in collagen synthesis and animal growth. Amino acids 50, 29–38 (2018).

    Google Scholar 

  38. Olsen, D. et al. Recombinant collagen and gelatin for drug delivery. Adv. Drug Deliv. Rev. 55, 1547–1567 (2003).

    Google Scholar 

  39. Yang, C. et al. The application of recombinant human collagen in tissue engineering. Front. Bioeng. Biotechnol. 18, 103–119 (2004).

    Google Scholar 

  40. Avila Rodríguez, M. I., Rodríguez Barroso, L. G. & Sánchez, M. L. Collagen: A review on its sources and potential cosmetic applications. J. Cosmet. Dermatol. 17, 20–26 (2018).

    Google Scholar 

  41. Bell, J. et al. The hierarchical response of human corneal collagen to load. Acta Biomater. 65, 216–225 (2018).

    Google Scholar 

  42. Michelacci, Y. M. Collagens and proteoglycans of the corneal extracellular matrix. Braz. J. Med. Biol. Res. 36, 1037–1046 (2003).

    Google Scholar 

  43. Kazaili, A., Abdul-Amir Al-Hindy, H., Madine, J. & Akhtar, R. Nano-scale stiffness and collagen fibril deterioration: Probing the cornea following enzymatic degradation using peakforce-qnm afm. Sensors 21, 1629 (2021).

    Google Scholar 

  44. Funderburgh, J. L., Funderburgh, M. L. & Du, Y. Stem cells in the limbal stroma. Ocul. Surf. 14, 113–120 (2016).

    Google Scholar 

  45. Hassell, J. R. & Birk, D. E. The molecular basis of corneal transparency. Exp. Eye Res. 91, 326–335 (2010).

    Google Scholar 

  46. Müller, L. J., Pels, E. & Vrensen, G. F. The specific architecture of the anterior stroma accounts for maintenance of corneal curvature. Br. J. Ophthalmol. 85, 437–443 (2001).

    Google Scholar 

  47. Maurice, D. M. The structure and transparency of the cornea. J. Physiol. 136, 263 (1957).

    Google Scholar 

  48. Morishige, N., Takagi, Y., Chikama, T. -i, Takahara, A. & Nishida, T. Three-dimensional analysis of collagen lamellae in the anterior stroma of the human cornea visualized by second harmonic generation imaging microscopy. Invest. Ophthalmol. Vis. Sci. 52, 911–915 (2011).

    Google Scholar 

  49. Muiznieks, L. D. & Keeley, F. W. Molecular assembly and mechanical properties of the extracellular matrix: a fibrous protein perspective. Biochim. Biophys. Acta. 1832, 866–875 (2013).

    Google Scholar 

  50. Akhtar, S. et al. Ultrastructural analysis of collagen fibrils and proteoglycans in keratoconus. Acta Ophthalmol. 86, 764–772 (2008).

    Google Scholar 

  51. Meyer, M. Processing of collagen based biomaterials and the resulting materials properties. Biomed. Eng. Online 18, 24 (2019).

    Google Scholar 

  52. Abraham, L. C., Zuena, E., Perez-Ramirez, B. & Kaplan, D. L. Guide to collagen characterization for biomaterial studies. J. Biomed. Mater. Res. B Appl. Biomater. 87, 264–285 (2008).

    Google Scholar 

  53. Antman-Passig, M., Levy, S., Gartenberg, C., Schori, H. & Shefi, O. Mechanically oriented 3D collagen hydrogel for directing neurite growth. Tissue Eng. Part A 23, 403–414 (2017).

    Google Scholar 

  54. Hong, H. et al. Compressed collagen intermixed with cornea-derived decellularized extracellular matrix providing mechanical and biochemical niches for corneal stroma analogue. Mater. Sci. Eng. C. 103, 109837 (2019).

    Google Scholar 

  55. Hong, H., Park, S. M., Kim, D., Park, S. J. & Kim, D. S. Grayscale mask-assisted photochemical crosslinking for a dense collagen construct with stiffness gradient. J. Biomed. Mater. Res. B Appl. Biomater. 108, 1000–1009 (2020).

    Google Scholar 

  56. Mi, S., Chen, B., Wright, B. & Connon, C. J. Plastic compression of a collagen gel forms a much improved scaffold for ocular surface tissue engineering over conventional collagen gels. J. Biomed. Mater. Res. A 95, 447–453 (2010).

    Google Scholar 

  57. McKay, T. B., Hutcheon, A. E., Guo, X., Zieske, J. D. & Karamichos, D. Modeling the cornea in 3-dimensions: current and future perspectives. Exp. Eye Res. 197, 108127 (2020).

    Google Scholar 

  58. Brown, R. A., Wiseman, M., Chuo, C. B., Cheema, U. & Nazhat, S. N. Ultrarapid engineering of biomimetic materials and tissues: fabrication of nano-and microstructures by plastic compression. Adv. Funct. Mater. 15, 1762–1770 (2005).

    Google Scholar 

  59. Majumdar, S. et al. Cyclodextrin modulated type I collagen self-assembly to engineer biomimetic cornea implants. Adv. Funct. Mater. 28, 1804076 (2018).

    Google Scholar 

  60. Zhao, X. et al. Collagen membranes crosslinked by β-cyclodextrin polyrotaxane monoaldehyde with good biocompatibilities and repair capabilities for cornea repair. RSC Adv. 7, 28865–28875 (2017).

    Google Scholar 

  61. Chen, Y., Song, W., Zhao, X., Han, Q. & Ren, L. An antibacterial collagen membrane crosslinked by the inclusion complex of β-cyclodextrin dialdehyde and ofloxacin for bacterial keratitis. RSC Adv. 8, 18153–18162 (2018).

    Google Scholar 

  62. Wang, Y. et al. Fabrication of cyclodextrin-based hydrogels for wound healing: progress, limitations, and prospects. Chem. Mater. 35, 5723–5743 (2023).

    Google Scholar 

  63. Wu, K. et al. Glycerol modulated collagen fibril evolution and lamellar organization for biomimetic corneal substitutes construction. Small 21,1–15 (2024).

  64. Lei, M. et al. Electrical signal initiates kinetic assembly of collagen to construct optically transparent and geometry customized artificial cornea substitutes. ACS Nano. 16, 10632–10646 (2022).

    Google Scholar 

  65. Jayakrishnan, A. & Jameela, S. Glutaraldehyde as a fixative in bioprostheses and drug delivery matrices. Biomaterials 17, 471–484 (1996).

    Google Scholar 

  66. Duan, X. & Sheardown, H. Dendrimer crosslinked collagen as a corneal tissue engineering scaffold: mechanical properties and corneal epithelial cell interactions. Biomaterials 27, 4608–4617 (2006).

    Google Scholar 

  67. Huang-Lee, L. L., Cheung, D. T. & Nimni, M. E. Biochemical changes and cytotoxicity associated with the degradation of polymeric glutaraldehyde derived crosslinks. J. Biomed. Mater. Res. 24, 1185–1201 (1990).

    Google Scholar 

  68. Ayaki, M., Shimada, K., Yaguchi, S., Koide, R. & Iwasawa, A. Corneal and conjunctival toxicity of disinfectants-assessing safety for use with ophthalmic surgical instruments. Regul. Toxicol. Pharmacol. 48, 292–295 (2007).

    Google Scholar 

  69. Boyer, J. C., Taylor, L. W. & Nylander-French, L. A. Viability of cultured human skin cells treated with 1, 6-hexamethylene diisocyanate monomer and its oligomer isocyanurate in different culture media. Sci. Rep. 11, 23804 (2021).

    Google Scholar 

  70. Zeng, Y. et al. Development of high refractive and high water content polythiourethane/AA hydrogels for potential artificial cornea implants. Int. J. Polym. Mater. Polym. Biomater. 69, 580–591 (2020).

    Google Scholar 

  71. Liu, S. et al. Crosslinking of collagen using a controlled molecular weight bio-crosslinker: β-cyclodextrin polyrotaxane multi-aldehydes. RSC Adv. 5, 46088–46094 (2015).

    Google Scholar 

  72. Loth, T. et al. Gelatin-based biomaterial engineering with anhydride-containing oligomeric cross-linkers. Biomacromolecules 15, 2104–2118 (2014).

    Google Scholar 

  73. Chan, B. & So, K. F. Photochemical crosslinking improves the physicochemical properties of collagen scaffolds. J. Biomed. Mater. Res. A. 75, 689–701 (2005).

    Google Scholar 

  74. Zhao, X. et al. Collagen based film with well epithelial and stromal regeneration as corneal repair materials: improving mechanical property by crosslinking with citric acid. Mater. Sci. Eng. C. 55, 201–208 (2015).

    Google Scholar 

  75. Wollensak, G., Spoerl, E. & Seiler, T. Riboflavin/ultraviolet-A-induced collagen crosslinking for the treatment of keratoconus. Am. J. Ophthalmol. 135, 620–627 (2003).

    Google Scholar 

  76. Arbelaez, M. C., Sekito, M. B., Vidal, C. & Choudhury, S. R. Collagen cross-linking with riboflavin and ultraviolet-a light in keratoconus: one-year results. Oman J. Ophthalmol. 2, 33–38 (2009).

    Google Scholar 

  77. Kilic, C., Girotti, A., Rodriguez-Cabello, J. C. & Hasirci, V. A collagen-based corneal stroma substitute with micro-designed architecture. Biomater. Sci. 2, 318–329 (2014).

    Google Scholar 

  78. Adamiak, K. & Sionkowska, A. Current methods of collagen cross-linking. Int. J. Biol. Macromol. 161, 550–560 (2020).

    Google Scholar 

  79. Koide, M. et al. A new type of biomaterial for artificial skin: dehydrothermally cross-linked composites of fibrillar and denatured collagens. J. Biomed. Mater. Res. 27, 79–87 (1993).

    Google Scholar 

  80. Añazco, C., Riedelsberger, J., Vega-Montoto, L. & Rojas, A. Exploring the interplay between polyphenols and lysyl oxidase enzymes for maintaining extracellular matrix homeostasis. Int. J. Mol. Sci. 24, 10985 (2023).

    Google Scholar 

  81. Katarzyna, A. & Alina, S. Current methods of collagen cross-linking: review. Int. J. Biol. Macromol. 151, 550–560 (2020).

    Google Scholar 

  82. Islam, M. M. et al. Optimization of collagen chemical crosslinking to restore biocompatibility of tissue-engineered scaffolds. Pharmaceutics 13, 832 (2021).

    Google Scholar 

  83. Orban, J. M. et al. Crosslinking of collagen gels by transglutaminase. J. Biomed. Mater. Res. A 68, 756–762 (2004).

    Google Scholar 

  84. Torbet, J. et al. Orthogonal scaffold of magnetically aligned collagen lamellae for corneal stroma reconstruction. Biomaterials 28, 4268–4276 (2007).

    Google Scholar 

  85. Islam, M. M., Griffith, M. & Merrett, K. Fabrication of a human recombinant collagen-based corneal substitute using carbodiimide chemistry. Corneal Regenerative Medicine: Methods and Protocols 157–164 (Humana Press, Totowa, NJ, 2013).

  86. Wang, Y. et al. Repairing the ruptured annular fibrosus by using type I collagen combined with citric acid, EDC and NHS: an in vivo study. Eur. Spine J. 26, 884–893 (2017).

    Google Scholar 

  87. Rýglová, Š, Braun, M. & Suchý, T. Collagen and its modifications—crucial aspects with concern to its processing and analysis. Macromol. Mater. Eng. 302, 1600460 (2017).

    Google Scholar 

  88. Van Wachem, P. et al. In vivo biocompatibility of carbodiimide-crosslinked collagen matrices: effects of crosslink density, heparin immobilization, and bFGF loading. J. Biomed. Mater. Res. 55, 368–378 (2001).

    Google Scholar 

  89. Nashchekina, Y. A. et al. The effect of carbodiimide on the structural, mechanical and biological properties of collagen films. Cell Tissue Biol. 15, 586–593 (2021).

    Google Scholar 

  90. Liu, W. et al. Recombinant human collagen for tissue engineered corneal substitutes. Biomaterials 29, 1147–1158 (2008).

    Google Scholar 

  91. Ahn, J.-I. et al. Crosslinked collagen hydrogels as corneal implants: effects of sterically bulky vs. non-bulky carbodiimides as crosslinkers. Acta Biomater. 9, 7796–7805 (2013).

    Google Scholar 

  92. Sionkowska, A., Kulka-Kamińska, K., Brudzyńska, P., Lewandowska, K. & Piwowarski, Ł. The influence of various crosslinking conditions of EDC/NHS on the properties of fish collagen film. Mar. Drugs 22, 194 (2024).

    Google Scholar 

  93. Lennarz, W. J. & Lane, M. D. Encyclopedia of Biological Chemistry (Academic Press, 2013).

  94. Roy, R., Boskey, A. & Bonassar, L. J. Processing of type I collagen gels using nonenzymatic glycation. J. Biomed. Mater. Res. A 93, 843–851 (2010).

    Google Scholar 

  95. Brownlee, M. Michael Advanced protein glycosylation in diabetes and aging. Annu. Rev. Med. 46, 223–234 (1995).

    Google Scholar 

  96. Avery, N. & Bailey, A. Enzymic and non-enzymic cross-linking mechanisms in relation to turnover of collagen: relevance to aging and exercise. Scand. J. Med. Sci. Sports 15, 231–240 (2005).

    Google Scholar 

  97. Xu, Q. et al. Collagen-and hyaluronic acid-based hydrogels and their biomedical applications. Mater. Sci. Eng. R Rep. 146, 100641 (2021).

    Google Scholar 

  98. Hu, X. et al. Prosthetic heart valves for transcatheter aortic valve replacement. BMEMat 1, e12026 (2023).

    Google Scholar 

  99. Koh, L. B. et al. Epoxy cross-linked collagen and collagen-laminin peptide hydrogels as corneal substitutes. J. Funct. Biomater. 4, 162–177 (2013).

    Google Scholar 

  100. Chan, K. L. et al. Crosslinking of collagen scaffolds promotes blood and lymphatic vascular stability. J. Biomed. Mater. Res. A 102, 3186–3195 (2014).

    Google Scholar 

  101. Výborný, K. et al. Genipin and EDC crosslinking of extracellular matrix hydrogel derived from human umbilical cord for neural tissue repair. Sci. Rep. 9, 10674 (2019).

    Google Scholar 

  102. Neves, M. I. L. et al. Study of the reaction between genipin and amino acids, dairy proteins, and milk to form a blue colorant ingredient. Food Res. Int. 157, 111240 (2022).

    Google Scholar 

  103. Singha, N. et al. Unusual confinement properties of a water insoluble small peptide hydrogel. Chem. Sci. 10, 5920–5928 (2019).

    Google Scholar 

  104. Cumming, M. H., Leonard, A. R., LeCorre-Bordes, D. S. & Hofman, K. Intra-fibrillar citric acid crosslinking of marine collagen electrospun nanofibres. Int. J. Biol. Macromol. 114, 874–881 (2018).

    Google Scholar 

  105. Sargeant, T. D., Desai, A. P., Banerjee, S., Agawu, A. & Stopek, J. B. An in situ forming collagen-PEG hydrogel for tissue regeneration. Acta Biomater. 8, 124–132 (2012).

    Google Scholar 

  106. Zhu, J. Bioactive modification of poly (ethylene glycol) hydrogels for tissue engineering. Biomaterials 31, 4639–4656 (2010).

    Google Scholar 

  107. Chun, Y. H. et al. In vivo biocompatibility evaluation of in situ-forming polyethylene glycol-collagen hydrogels in corneal defects. Sci. Rep. 11, 23913 (2021).

    Google Scholar 

  108. Fernandes-Cunha, G. M. et al. In situ-forming collagen hydrogel crosslinked via multi-functional PEG as a matrix therapy for corneal defects. Sci. Rep. 10, 16671 (2020).

    Google Scholar 

  109. Li, H.-C. et al. Synthetic crosslinker based on amino-yne click to enhance the suture tension of collagen-based corneal repair materials. ACS Appl. Polym. Mater. 4, 4495–4507 (2022).

    Google Scholar 

  110. Phelps, E. A. et al. Maleimide cross-linked bioactive PEG hydrogel exhibits improved reaction kinetics and cross-linking for cell encapsulation and in-situ delivery. Adv. Mater. 24, 64 (2012).

    Google Scholar 

  111. Lei, X. et al. Mechanical and optical properties of reinforced collagen membranes for corneal regeneration through polyrotaxane cross-linking. ACS Appl. Bio Mater. 2, 3861–3869 (2019).

    Google Scholar 

  112. Antoine, E. E., Vlachos, P. P. & Rylander, M. N. Review of collagen I hydrogels for bioengineered tissue microenvironments: characterization of mechanics, structure, and transport. Tissue Eng. Part B Rev. 20, 683–696 (2014).

    Google Scholar 

  113. Dragan, E. S. Design and applications of interpenetrating polymer network hydrogels. A review. Chem. Eng. J. 243, 572–590 (2014).

    Google Scholar 

  114. Zhang, Q. et al. High refractive index inorganic-organic interpenetrating polymer network (IPN) hydrogel nanocomposite toward artificial cornea implants. ACS Macro Lett. 1, 876–881 (2012).

    Google Scholar 

  115. Dhand, A. P., Galarraga, J. H. & Burdick, J. A. Enhancing biopolymer hydrogel functionality through interpenetrating networks. Trends Biotechnol. 39, 519–538 (2021).

    Google Scholar 

  116. Formisano, N. et al. Mechanical properties of bioengineered corneal stroma. Adv. Healthc. Mater. 10, 2100972 (2021).

    Google Scholar 

  117. Luo, Y., Li, G., Chen, L. & Hong, F. F. Preparation and evaluation of bacterial nanocellulose/hyaluronic acid composite artificial cornea for application of corneal transplantation. Biomacromolecules 24, 201–212 (2022).

    Google Scholar 

  118. Chen, F., Le, P., Lai, K., Fernandes-Cunha, G. M. & Myung, D. Simultaneous interpenetrating polymer network of collagen and hyaluronic acid as an in situ-forming corneal defect filler. Chem. Mater. 32, 5208–5216 (2020).

    Google Scholar 

  119. Yang, X. et al. Photo-crosslinked GelMA/collagen membrane loaded with lysozyme as an antibacterial corneal implant. Int. J. Biol. Macromol. 191, 1006–1016 (2021).

    Google Scholar 

  120. Liu, W. et al. Collagen-phosphorylcholine interpenetrating network hydrogels as corneal substitutes. Biomaterials 30, 1551–1559 (2009).

    Google Scholar 

  121. Hayes, S. et al. The structural and optical properties of type III human collagen biosynthetic corneal substitutes. Acta Biomater. 25, 121–130 (2015).

    Google Scholar 

  122. Islam, M. M. et al. Crosslinker-free collagen gelation for corneal regeneration. Sci. Rep. 12, 9108 (2022).

    Google Scholar 

  123. Fagerholm, P. et al. A biosynthetic alternative to human donor tissue for inducing corneal regeneration: 24-month follow-up of a phase 1 clinical study. Sci. Transl. Med. 2, 46ra61 (2010).

    Google Scholar 

  124. Sun, X., Yang, X., Song, W. & Ren, L. Construction and evaluation of collagen-based corneal grafts using polycaprolactone to improve tension stress. ACS Omega 5, 674–682 (2020).

    Google Scholar 

  125. Dellatolas, I. et al. Local mechanism governs global reinforcement of nanofiller-hydrogel composites. ACS nano 17, 20939–20948 (2023).

    Google Scholar 

  126. Lee, K.-Y., Aitomäki, Y., Berglund, L. A., Oksman, K. & Bismarck, A. On the use of nanocellulose as reinforcement in polymer matrix composites. Compos. Sci. Technol. 105, 15–27 (2014).

    Google Scholar 

  127. Qin, L., Gao, H., Xiong, S., Jia, Y. & Ren, L. Preparation of collagen/cellulose nanocrystals composite films and their potential applications in corneal repair. J. Mater. Sci. Mater. Med. 31, 1–11 (2020).

    Google Scholar 

  128. Xu, W. et al. PCL scaffold combined with rat tail collagen type I to reduce keratocyte differentiation and prevent corneal stroma fibrosis after injury. Exp. Eye Res. 217, 108936 (2022).

    Google Scholar 

  129. Chen, Z. et al. Biomimetic corneal stroma using electro-compacted collagen. Acta Biomater. 113, 360–371 (2020).

    Google Scholar 

  130. Nurković, J. S., Vojinović, R. & Dolićanin, Z. Corneal stem cells as a source of regenerative cell-based therapy. Stem Cells Int 2020, 8813447 (2020).

    Google Scholar 

  131. Daniels, J. T., Dart, J. K., Tuft, S. J. & Khaw, P. T. Corneal stem cells in review. Wound Repair Regen. 9, 483–494 (2001).

    Google Scholar 

  132. Volatier, T., Cursiefen, C. & Notara, M. Current advances in corneal stromal stem cell biology and therapeutic applications. Cells 13, 163 (2024).

    Google Scholar 

  133. Ghezzi, C. E., Marelli, B., Omenetto, F. G., Funderburgh, J. L. & Kaplan, D. L. 3D functional corneal stromal tissue equivalent based on corneal stromal stem cells and multi-layered silk film architecture. PLoS ONE 12, e0169504 (2017).

    Google Scholar 

  134. Jiwlawat, N. et al. Micropatterned substrates with physiological stiffness promote cell maturation and Pompe disease phenotype in human induced pluripotent stem cell-derived skeletal myocytes. Biotechnol. Bioeng. 116, 2377–2392 (2019).

    Google Scholar 

  135. Bhattacharjee, P., Cavanagh, B. L. & Ahearne, M. Influence of micropatterned substrates on keratocyte phenotype. Sci. Rep. 10, 6679 (2020).

    Google Scholar 

  136. Xiong, S. et al. Microgrooved collagen-based corneal scaffold for promoting collective cell migration and antifibrosis. RSC Adv. 9, 29463–29473 (2019).

    Google Scholar 

  137. Wu, J., Du, Y., Watkins, S. C., Funderburgh, J. L. & Wagner, W. R. The engineering of organized human corneal tissue through the spatial guidance of corneal stromal stem cells. Biomaterials 33, 1343–1352 (2012).

    Google Scholar 

  138. Wilson, S. L. et al. Chemical and topographical effects on cell differentiation and matrix elasticity in a corneal stromal layer model. Adv. Funct. Mater. 22, 3641–3649 (2012).

    Google Scholar 

  139. Kong, B. et al. Recombinant human collagen hydrogels with hierarchically ordered microstructures for corneal stroma regeneration. Chem. Eng. J. 428, 131012 (2022).

    Google Scholar 

  140. Cabrera-Aguas, M., Khoo, P. & Watson, S. Presumed microbial keratitis cases resulting in evisceration and enucleation in Sydney, Australia. Ocul. Immunol. Inflamm. 31, 1–7 (2021).

  141. Liu, Y., Ren, L., Long, K., Wang, L. & Wang, Y. Preparation and characterization of a novel tobramycin-containing antibacterial collagen film for corneal tissue engineering. Acta Biomater. 10, 289–299 (2014).

    Google Scholar 

  142. Cabrera-Aguas, M., Khoo, P. & Watson, S. Infectious keratitis: a review. Clin. Exp. Ophthalmol. 50, 543–562 (2022).

    Google Scholar 

  143. Riau, A. K. et al. Collagen-based artificial corneal scaffold with anti-infective capability for prevention of perioperative bacterial infections. ACS Biomater. Sci. Eng. 1, 1324–1334 (2015).

    Google Scholar 

  144. Magnier, F. et al. Preventive treatment of allograft rejection after endothelial keratoplasty: a systematic review and meta-analysis. Acta Ophthalmol. 100, e1061–e1073 (2022).

    Google Scholar 

  145. Rana, D. et al. Collagen-based hydrogels for the eye: a comprehensive review. Gels 9, 643 (2023).

    Google Scholar 

  146. Karamichos, D. & Hjortdal, J. Keratoconus: tissue engineering and biomaterials. J. Funct. Biomater. 5, 111–134 (2014).

    Google Scholar 

  147. Coster, D., Jessup, C. & Williams, K. Mechanisms of corneal allograft rejection and regional immunosuppression. Eye 23, 1894–1897 (2009).

    Google Scholar 

  148. Vora, G. K. & Ciolino, J. B. Corneal allograft reaction associated with nonocular inflammation. Digit. j. ophthalmol. 20, 29 (2014).

    Google Scholar 

  149. Xeroudaki, M. et al. A double-crosslinked nanocellulose-reinforced dexamethasone-loaded collagen hydrogel for corneal application and sustained anti-inflammatory activity. Acta Biomater. 172, 234–248 (2023).

    Google Scholar 

  150. Patra, H. K. et al. Rational nanotoolbox with theranostic potential for medicated pro-regenerative corneal implants. Adv. Funct. Mater. 29, 1903760 (2019).

    Google Scholar 

  151. Calladine, D., Ward, M. & Packard, R. Adherent ocular bandage for clear corneal incisions used in cataract surgery. J. Cataract Refract. Surg. 36, 1839–1848 (2010).

    Google Scholar 

  152. Rosenquist, J. et al. An injectable, shape-retaining collagen hydrogel cross-linked using thiol-maleimide click chemistry for sealing corneal perforations. ACS Appl. Mater. Interfaces 15, 34407–34418 (2023).

    Google Scholar 

  153. Lee, H. J., Fernandes-Cunha, G. M., Na, K.-S., Hull, S. M. & Myung, D. Bio-orthogonally crosslinked, in situ forming corneal stromal tissue substitute. Adv. Funct. Mater. 7, 1800560 (2018).

    Google Scholar 

  154. Miyashita, H. et al. Collagen-immobilized poly (vinyl alcohol) as an artificial cornea scaffold that supports a stratified corneal epithelium. J. Biomed. Mater. Res. B Appl. Biomater. 76, 56–63 (2006).

    Google Scholar 

  155. Jang, J.-W. et al. Scaffold characteristics, fabrication methods, and biomaterials for the bone tissue engineering. Int. J. Precis. Eng. Manuf. 24, 511–529 (2023).

    Google Scholar 

  156. Kong, B. et al. Fiber reinforced GelMA hydrogel to induce the regeneration of corneal stroma. Nat. Commun. 11, 1435 (2020).

    Google Scholar 

  157. Zhang, N., Yan, H. & Wen, X. Tissue-engineering approaches for axonal guidance. Brain Res. Rev. 49, 48–64 (2005).

    Google Scholar 

  158. Curtis, A. & Wilkinson, C. Topographical control of cells. Biomaterials 18, 1573–1583 (1997).

    Google Scholar 

  159. Ye, J. et al. Chitosan-modified, collagen-based biomimetic nanofibrous membranes as selective cell adhering wound dressings in the treatment of chemically burned corneas. J. Mater. Chem. B. 2, 4226–4236 (2014).

    Google Scholar 

  160. Baradaran-Rafii, A., Biazar, E. & Heidari-Keshel, S. Cellular response of limbal stem cells on PHBV/gelatin nanofibrous scaffold for ocular epithelial regeneration. Int. J. Polym. Mater. Polym. Biomater. 64, 879–887 (2015).

    Google Scholar 

  161. Zeugolis, D. I. et al. Electro-spinning of pure collagen nano-fibres–just an expensive way to make gelatin? Biomaterials 29, 2293–2305 (2008).

    Google Scholar 

  162. Zhao, G., Zhang, X., Lu, T. J. & Xu, F. Recent advances in electrospun nanofibrous scaffolds for cardiac tissue engineering. Adv. Funct. Mater. 25, 5726–5738 (2015).

    Google Scholar 

  163. Boote, C., Dennis, S., Huang, Y., Quantock, A. J. & Meek, K. M. Lamellar orientation in human cornea in relation to mechanical properties. J. Struct. Biol. 149, 1–6 (2005).

    Google Scholar 

  164. Phu, D., Wray, L. S., Warren, R. V., Haskell, R. C. & Orwin, E. J. Effect of substrate composition and alignment on corneal cell phenotype. Tissue Eng. Part A. 17, 799–807 (2011).

    Google Scholar 

  165. Wu, Z., Kong, B., Liu, R., Sun, W. & Mi, S. Engineering of corneal tissue through an aligned PVA/collagen composite nanofibrous electrospun scaffold. Nanomaterials 8, 124 (2018).

    Google Scholar 

  166. Isaacson, A., Swioklo, S. & Connon, C. J. 3D bioprinting of a corneal stroma equivalent. Exp. Eye Res. 173, 188–193 (2018).

    Google Scholar 

  167. Haring, A. P., Sontheimer, H. & Johnson, B. N. Microphysiological human brain and neural systems-on-a-chip: potential alternatives to small animal models and emerging platforms for drug discovery and personalized medicine. Stem Cell Rev. Rep. 13, 381–406 (2017).

    Google Scholar 

  168. Hagenbuchner, J., Nothdurfter, D. & Ausserlechner, M. J. 3D bioprinting: novel approaches for engineering complex human tissue equivalents and drug testing. Essays Biochem 65, 417–427 (2021).

    Google Scholar 

  169. Ozbolat, I. T. Scaffold-based or scaffold-free bioprinting: competing or complementing approaches? J. Nanotechnol. Eng. Med. 6, 024701 (2015).

    Google Scholar 

  170. Daly, A. C., Prendergast, M. E., Hughes, A. J. & Burdick, J. A. Bioprinting for the biologist. Cell 184, 18–32 (2021).

    Google Scholar 

  171. Ang, M. & Mehta, J. S. Deep anterior lamellar keratoplasty as an alternative to penetrating keratoplasty. Ophthalmology 118, 2306–2307 (2011).

    Google Scholar 

  172. Gao, Y., Li, C., Bu, P., Zhang, L. & Bouchard, C. S. Infectious interface keratitis (IIK) following lamellar keratoplasty: a literature review. Ocul. Surf. 17, 635–643 (2019).

    Google Scholar 

  173. Grossniklaus, H. E. Deep lamellar keratoplasty: surgical techniques for anterior lamellar keratoplasty with and without baring of Descemet’s membrane. Am. J. Ophthalmol. 134, 480 (2002).

    Google Scholar 

  174. Zhao, X., Song, W., Liu, S. & Ren, L. Corneal regeneration by utilizing collagen-based materials. Sci. China Chem. 59, 1548–1553 (2016).

    Google Scholar 

  175. Fagerholm, P. et al. Stable corneal regeneration four years after implantation of a cell-free recombinant human collagen scaffold. Biomaterials 35, 2420–2427 (2014).

    Google Scholar 

  176. Xu, S., Zhou, S., Mao, B., Chen, J. & Zhang, Z. Cornea-stroma-mimicking films derived from cellulose nanocrystal templating fibrous collagen as therapeutic contact lenses. ACS Sustain. Chem. Eng. 7, 12248–12260 (2019).

    Google Scholar 

  177. Zeng, Y., Yang, J., Huang, K., Lee, Z. & Lee, X. A comparison of biomechanical properties between human and porcine cornea. J. Biomech. 34, 533–537 (2001).

    Google Scholar 

  178. Menovsky, T., Beek, J. F. & van Gemert, M. J. Effect of the CO2 milliwatt laser on tensile strength of microsutures. Lasers Surg. Med. 20, 64–68 (1997).

    Google Scholar 

  179. Patel, S., Marshall, J. & Fitzke, F. W. Refractive index of the human corneal epithelium and stroma. J. Refract Surg. 11, 100–141 (1995).

  180. Goodarzi, H., Jadidi, K., Pourmotabed, S., Sharifi, E. & Aghamollaei, H. Preparation and in vitro characterization of cross-linked collagen–gelatin hydrogel using EDC/NHS for corneal tissue engineering applications. Int. J. Biol. Macromol. 126, 620–632 (2019).

    Google Scholar 

  181. Rafat, M. et al. PEG-stabilized carbodiimide crosslinked collagen–chitosan hydrogels for corneal tissue engineering. Biomaterials 29, 3960–3972 (2008).

    Google Scholar 

  182. Xu, Y. et al. Biomimetic convex implant for corneal regeneration through 3D printing. Adv. Sci. 10, 2205878 (2023).

    Google Scholar 

  183. Kong, B. et al. Cornea-Inspired ultrasound-responsive adhesive hydrogel patches for keratitis treatment. Adv. Funct. Mater. 34, 2310544 (2024).

    Google Scholar 

  184. Duarte Campos, D. F. et al. Corneal bioprinting utilizing collagen-based bioinks and primary human keratocytes. J. Biomed. Mater. Res. A 107, 1945–1953 (2019).

    Google Scholar 

  185. Buznyk, O. et al. Bioengineered corneas grafted as alternatives to human donor corneas in three high-risk patients. Clin. Transl. Sci. 8, 558–562 (2015).

    Google Scholar 

  186. Islam, M. M. et al. Biomaterials-enabled cornea regeneration in patients at high risk for rejection of donor tissue transplantation. NPJ Regen. Med. 3, 1–10 (2018).

  187. Rafat, M. et al. Bioengineered corneal tissue for minimally invasive vision restoration in advanced keratoconus in two clinical cohorts. Nat. Biotechnol. 41, 70–81 (2022).

    Google Scholar 

Download references