AccScience Publishing / IJB / Volume 10 / Issue 4 / DOI: 10.36922/ijb.3258
Submit to IJB
Cite this article
95
Download
934
Views
Journal Browser
Volume | Year
Issue
Search
Forthcoming Issue
Current Issue
View All
News and Announcements
View All
RESEARCH ARTICLE

3D printing collagen type IV for corneal endothelium transplantation

Morgan Overmass1,2 ,  Huasheng Huang1,2 ,  Li Wen2,3 ,  Zhi Chen4 ,  Sepidar Sayyar4,5 ,  Constantinos Petsoglou1,3 ,  Gordon Wallace4,5 ,  Gerard Sutton2,3,6 ,  Jingjing You1,2*
Show Less
1 School of Medical Sciences, Faculty of Medicine and Health, University of Sydney, Sydney, Australia
2 Save Sight Institute, Sydney Medical School, University of Sydney, Sydney, Australia
3 NSW Tissue Bank, Sydney, Australia
4 ARC Centre of Excellence for Electromaterial Science, Intelligent Polymer Research Institute, AIIM, Innovation Campus, University of Wollongong, Wollongong, Australia
5 Australian National Fabrication Facility – Materials Node, Innovation Campus, University of Wollongong, Wollongong, Australia
6 Vision Eye Institute, Chatswood, New South Wales, Australia
IJB 2024, 10(4), 3258 https://doi.org/10.36922/ijb.3258
Submitted: 25 March 2024 | Accepted: 9 May 2024 | Published: 21 June 2024
(This article belongs to the Special Issue Biomimetic and bioinspired printed structures)
© 2024 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
Download PDF
Cite
XML
Abstract

Collagen type IV (Col-IV) is a critical matrix protein component in the basement membrane. In the cornea, it is the key contributor to the formation of Descemet’s membrane — the layer for corneal endothelial cells to reside on. Currently, endothelial keratopathy, which uses the healthy donor corneal endothelium layer as a transplanted tissue, is the gold standard surgery to cure corneal blindness caused by endothelial dysfunction. However, its use is being limited by the shortage of donor corneas. Bioengineering Descemet’s membrane is an alternative to overcome the tissue shortage. In this study, we developed a printable Col-IV ink to construct a Col-IV membrane. We demonstrated that the printed Col-IV membrane has a seven times higher corneal endothelial cell attachment over other matrix proteins (e.g., Col-I, laminin, and chondroitin) and a significantly faster healing rate compared to Col-I. The human endothelial cells cultured on the Col-IV membrane retained their hexagonal shapes, expressed typical endothelial markers ZO-1 and Na+/K+-ATPase, and retained the ability to deposit laminin. As this collagen subtype is prevalent in the basement membranes of all body tissues, our work suggests an important role for Col-IV as a printable biomaterial in tissue engineering in general.

Keywords
Collagen type IV
Bioprinting
Corneal endothelium
Basement mem¬brane
Printable biomaterial
Endothelium transplant
Funding
We acknowledge the funding support from the NHMRC Idea Grant (GNT1181415), Australian Research Council (ARC) Centre of Excellence Scheme (CE140100012), and Sydney Eye Hospital Foundation.
Conflict of interest
The authors declare the following financial interests/ personal relationships, which may be considered as potential competing interests: the printable Col-IV biomaterial (PCT/AU2022/050247) was also patented with M.O., G.W., G.S., and J.Y. being inventors. The bioengineered endothelium construction was patented (PCT/AU2022/050248) with M.O., S.H., L.W., C.P., G.S., and J.Y. being inventors.
References
  1. Copes F, Pien N, Van Vlierberghe S, Boccafoschi F, Mantovani D. Collagen-based tissue engineering strategies for vascular medicine. Front Bioeng Biotechnol. 2019;7:166. doi: 10.3389/fbioe.2019.00166
  2. Song Y, Overmass M, Fan J, et al. Application of Collagen I and IV in bioengineering transparent ocular tissues. Review. Frontiers in Surgery. 2021-August-26 2021;8(344). doi: 10.3389/fsurg.2021.639500
  3. Dean A, Van Agtmael T. Collagen IV-related diseases and therapies. In: Ruggiero F, ed. The Collagen Superfamily and Collagenopathies. Switzerland: Springer International Publishing; 2021:143-197.
  4. De Santis MM, Wagner DE. Collagen IV: a critical new starting point for engineering upper airways. Eur Respir J. Jun 2020;55(6). doi: 10.1183/13993003.01130-2020
  5. Soh YQ, Kocaba V, Pinto M, Mehta JS. Fuchs endothelial corneal dystrophy and corneal endothelial diseases: East meets West. Eye (Lond). Mar 2020;34(3):427-441. doi: 10.1038/s41433-019-0497-9
  6. Deng SX, Lee WB, Hammersmith KM, et al. Descemet membrane endothelial keratoplasty: safety and outcomes: a report by the American Academy of Ophthalmology. Ophthalmology. Feb 2018;125(2):295-310. doi: 10.1016/j.ophtha.2017.08.015
  7. Gain P, Jullienne R, He Z, et al. Global survey of corneal transplantation and eye banking. JAMA Ophthalmology. 2016;134(2):167-173. doi: 10.1001/jamaophthalmol.2015.4776
  8. Parekh M, Romano V, Hassanin K, et al. Biomaterials for corneal endothelial cell culture and tissue engineering. Journal of Tissue Engineering. 2021/01/01 2021;12:2041731421990536. doi: 10.1177/2041731421990536
  9. de Oliveira RC, Murillo S, Saikia P, Wilson SE. The efficacy of topical HGF on corneal fibrosis and epithelial healing after scar-producing PRK Injury in Rabbits. Translational Vision Science & Technology. 2020;9(4):29-29. doi: 10.1167/tvst.9.4.29
  10. Català P, Thuret G, Skottman H, et al. Approaches for corneal endothelium regenerative medicine. Prog Retin Eye Res. Mar 2022;87:100987. doi: 10.1016/j.preteyeres.2021.100987
  11. Palchesko RN, Funderburgh JL, Feinberg AW. Engineered basement membranes for regenerating the corneal endothelium. Adv Healthc Mater. Nov 2016;5(22): 2942-2950. doi: 10.1002/adhm.201600488
  12. Sorkio AE, Vuorimaa-Laukkanen EP, Hakola HM, et al. Biomimetic collagen I and IV double layer Langmuir- Schaefer films as microenvironment for human pluripotent stem cell derived retinal pigment epithelial cells. Biomaterials. May 2015;51:257-269. doi: 10.1016/j.biomaterials.2015.02.005
  13. Gatseva A, Sin YY, Brezzo G, Van Agtmael T. Basement membrane collagens and disease mechanisms. Essays Biochem. Sep 13 2019;63(3):297-312. doi: 10.1042/ebc20180071
  14. Hospodiuk M, Dey M, Sosnoski D, Ozbolat IT. The bioink: a comprehensive review on bioprintable materials. Biotechnology Advances. 2017/03/01/ 2017;35(2):217-239. doi: 10.1016/j.biotechadv.2016.12.006
  15. Song Y, Hua S, Sayyar S, et al. Corneal bioprinting using a high concentration pure collagen I transparent bioink. Bioprinting. 2022/12/01/ 2022;28:e00235. doi: 10.1016/j.bprint.2022.e00235
  16. Chung JHY, Naficy S, Yue Z, et al. Bio-ink properties and printability for extrusion printing living cells. 10.1039/ C3BM00012E. Biomaterials Science. 2013;1(7):763-773. doi: 10.1039/C3BM00012E
  17. Ouyang L, Yao R, Zhao Y, Sun W. Effect of bioink properties on printability and cell viability for 3D bioplotting of embryonic stem cells. Biofabrication. 2016/09/16 2016;8(3):035020. doi: 10.1088/1758-5090/8/3/035020
  18. Dickman MM, van Maris MPFHL, van Marion FW, et al. Surface metrology and 3-dimensional confocal profiling of femtosecond laser and mechanically dissected ultrathin endothelial lamellae. Investigative Ophthalmology & Visual Science. 2014;55(8):5183-5190. doi: 10.1167/iovs.14-14309
  19. Petsoglou C, Wen L, Hoque M, et al. Effects of human platelet lysate on the growth of cultured human corneal endothelial cells. Experimental Eye Research. 2021/07/01/ 2021;208:108613. doi: 10.1016/j.exer.2021.108613
  20. Davidenko N, Hamaia S, Bax DV, et al. Selecting the correct cellular model for assessing of the biological response of collagen-based biomaterials. Acta Biomater. Jan 2018;65: 88-101. doi: 10.1016/j.actbio.2017.10.035
  21. Engelmann K, Bohnke M, Friedl P. Isolation and long-term cultivation of human corneal endothelial cells. Invest Ophthalmol Vis Sci. Nov 1988;29(11):1656-62.
  22. Ng WL, Shkolnikov V. Optimizing cell deposition for inkjet-based bioprinting. IJB. 2024;0(0). doi: 10.36922/ijb.2135
  23. Kim HS, Lee DY, Park JH, Kim JH, Hwang JH, Jung HI. Optimization of electrohydrodynamic writing technique to print collagen. Experimental Techniques. 2007/07/01 2007;31(4):15-19. doi: 10.1111/j.1747-1567.2007.00154.x
  24. Sakai S, Kamei H, Mori T, et al. Visible light-induced hydrogelation of an alginate derivative and application to stereolithographic bioprinting using a visible light projector and acid red. Biomacromolecules. 2018/02/12 2018;19(2):672-679. doi: 10.1021/acs.biomac.7b01827
  25. Vetter JM, Butsch C, Faust M, et al. Irregularity of the posterior corneal surface after curved interface femtosecond laser-assisted versus microkeratome-assisted descemet stripping automated endothelial keratoplasty. Cornea. 2013;32(2)
  26. Chen Z, You J, Liu X, et al. Biomaterials for corneal bioengineering. Biomed Mater. Mar 6 2018;13(3):032002. doi: 10.1088/1748-605X/aa92d2
  27. Zhu YT, Tighe S, Chen SL, John T, Kao WY, Tseng SC. Engineering of human corneal endothelial grafts. Curr Ophthalmol Rep. Sep 2015;3(3):207-217. doi: 10.1007/s40135-015-0077-5
  28. Chen J, Li Z, Zhang L, et al. Descemet’s membrane supports corneal endothelial cell regeneration in rabbits. Sci Rep. Aug 1 2017;7(1):6983. doi: 10.1038/s41598-017-07557-2
  29. Vercammen H, Miron A, Oellerich S, et al. Corneal endothelial wound healing: understanding the regenerative capacity of the innermost layer of the cornea. Translational Research. 2022/10/01/ 2022;248:111-127. doi: 10.1016/j.trsl.2022.05.003
  30. Walenda G, Hemeda H, Schneider RK, Merkel R, Hoffmann B, Wagner W. Human platelet lysate gel provides a novel three dimensional-matrix for enhanced culture expansion of mesenchymal stromal cells. Tissue Eng Part C Methods. Dec 2012;18(12):924-34. doi: 10.1089/ten.TEC.2011.0541
  31. Naito M, Funaki C, Hayashi T, et al. Substrate-bound fibrinogen, fibrin and other cell attachment-promoting proteins as a scaffold for cultured vascular smooth muscle cells. Atherosclerosis. Oct 1992;96(2-3):227-34. doi: 10.1016/0021-9150(92)90069-s
  32. Madathil BK, Anil Kumar PR, Kumary TV. N-Isopropylacrylamide-co-glycidylmethacrylate as a thermoresponsive substrate for corneal endothelial cell sheet engineering. Biomed Research International. 2014/06/09 2014;2014:450672. doi: 10.1155/2014/450672
  33. Khalili M, Zarebkohan A, Dianat-Moghadam H, Panahi M, Andre H, Alizadeh E. Corneal endothelial cell sheet bioengineering from neural crest cell-derived adipose stem cells on novel thermo-responsive elastin-mimetic dendrimers decorated with RGD. Chemical Engineering Journal. 2022/02/01/ 2022;429:132523. doi: 10.1016/j.cej.2021.132523
  34. Last JA, Thomasy SM, Croasdale CR, Russell P, Murphy CJ. Compliance profile of the human cornea as measured by atomic force microscopy. Micron. Dec 2012;43(12):1293-8. doi: 10.1016/j.micron.2012.02.014
  35. Singh M, Jonnalagadda S. Advances in bioprinting using additive manufacturing. Eur J Pharm Sci. Feb 15 2020;143:105167. doi: 10.1016/j.ejps.2019.105167
  36. Yu C, Guan G, Glas S, Wang L, Li Z, Turng L-S. A biomimetic basement membrane consisted of hybrid aligned nanofibers and microfibers with immobilized collagen IV and laminin for rapid endothelialization. Bio-Design and Manufacturing. 2021/06/01 2021;4(2):171-189. doi: 10.1007/s42242-020-00111-6
  37. Luo X, Han C, Yang P, et al. The co-deposition coating of collagen IV and laminin on hyaluronic acid pattern for better biocompatibility on cardiovascular biomaterials. Colloids and Surfaces B: Biointerfaces. 2020/12/01/ 2020;196:111307. doi: 10.1016/j.colsurfb.2020.111307
  38. Lin SL, Christen MO. Polycaprolactone-based dermal filler complications: A retrospective study of 1111 treatments. J Cosmet Dermatol. Aug 2020;19(8):1907-1914. doi: 10.1111/jocd.13518
  39. Ostberg A, Törnqvist G. Management of detachment of Descemet’s membrane caused by injection of hyaluronic acid. Ophthalmic Surg. Dec 1989;20(12):885-6.
  40. Zhang K, Li JA, Deng K, Liu T, Chen JY, Huang N. The endothelialization and hemocompatibility of the functional multilayer on titanium surface constructed with type IV collagen and heparin. Colloids Surf B Biointerfaces. Aug 1 2013;108:295-304. doi: 10.1016/j.colsurfb.2012.12.053

 

 

Share
Back to top
International Journal of Bioprinting, Electronic ISSN: 2424-8002 Print ISSN: 2424-7723, Published by AccScience Publishing
We use cookies on our website to ensure you get the best experience.
Read more about our cookies here
Accept