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Tissue Engineering of a Healthy Corneal Endothelium for FECD Patients

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Current Treatment Options for Fuchs Endothelial Dystrophy

Abstract

The growing global shortage of corneal tissue for transplantation, in part exacerbated by population aging, has prompted the search for alternatives to native human corneas. Tissue engineering of a corneal endothelium appears to be a quite interesting option. The attractiveness of this approach resides in the possibility of expanding the number of cells obtained from a single donor, as one pair of donor corneas could theoretically treat hundreds of eyes. This chapter describes the key steps of corneal endothelial tissue engineering. It explains the importance of cell types, cell isolation, and expansion techniques, as well as cell quality assessment. It reviews the transplantation modalities that can be used to replace a diseased endothelium with a tissue-engineered endothelium, using or not a carrier. This chapter also covers the recent progress in corneal endothelial tissue engineering for Fuchs endothelial corneal dystrophy (FECD). Finally, it underlines the importance of new FECD models to advance our understanding of FECD pathophysiology and to develop or test new therapeutic options in order to cure or delay the progression of this disease.

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References

  1. Anshu A, Price MO, Price Jr FW. Risk of corneal transplant rejection significantly reduced with Descemet’s membrane endothelial keratoplasty. Ophthalmology. 2012;119:536–40.

    Article  PubMed  Google Scholar 

  2. Eye Bank Association of America, 2014. 2013 Eye Banking Statistical Report. Washington D.C.

    Google Scholar 

  3. Eye Bank Association of America, 2010. 2009 Eye Banking Statistical Report. Washington D.C.

    Google Scholar 

  4. Mack RJ, Mason P, Mathers WD. Obstacles to donor eye procurement and their solutions at the University of Iowa. Cornea. 1995;14:249–52.

    Article  CAS  PubMed  Google Scholar 

  5. Poinard C, Tuppin P, Loty B, Delbosc B. The French national waiting list for keratoplasty created in 1999: patient registration, indications, characteristics, and turnover. J Fr Ophtalmol. 2003;26:911–9.

    CAS  PubMed  Google Scholar 

  6. Rasouli M, Caraiscos VB, Slomovic AR. Efficacy of routine notification and request on reducing corneal transplantation wait times in Canada. Can J Ophthalmol. 2009;44:31–5.

    Article  PubMed  Google Scholar 

  7. Reinhard T, Bohringer D, Bogen A, Sundmacher R. The transplantation law: a chance to overcome the shortage of corneal grafts in germany? Transplant Proc. 2002;34:1322–4.

    Article  CAS  PubMed  Google Scholar 

  8. Price MO, Giebel AW, Fairchild KM, Price Jr FW. Descemet’s membrane endothelial keratoplasty: prospective multicenter study of visual and refractive outcomes and endothelial survival. Ophthalmology. 2009;116:2361–8.

    Article  PubMed  Google Scholar 

  9. Price MO, Gorovoy M, Benetz BA, Price Jr FW, Menegay HJ, Debanne SM, Lass JH. Descemet’s stripping automated endothelial keratoplasty outcomes compared with penetrating keratoplasty from the Cornea Donor Study. Ophthalmology. 2010;117:438–44.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Peh GS, Toh KP, Wu FY, Tan DT, Mehta JS. Cultivation of human corneal endothelial cells isolated from paired donor corneas. PLoS One. 2011;6:e28310.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Proulx S, Brunette I. Methods being developed for preparation, delivery and transplantation of a tissue-engineered corneal endothelium. Exp Eye Res. 2012;95:68–75.

    Article  CAS  PubMed  Google Scholar 

  12. Choi JS, Kim EY, Kim MJ, Khan FA, Giegengack M, D’Agostino Jr R, Criswell T, Khang G, Soker S. Factors affecting successful isolation of human corneal endothelial cells for clinical use. Cell Transplant. 2014;23:845–54.

    Article  PubMed  Google Scholar 

  13. Zaniolo K, Bostan C, Rochette Drouin O, Deschambeault A, Perron MC, Brunette I, Proulx S. Culture of human corneal endothelial cells isolated from corneas with Fuchs endothelial corneal dystrophy. Exp Eye Res. 2012;94:22–31.

    Article  CAS  PubMed  Google Scholar 

  14. Pellegrini G, Rama P, De Luca M. Vision from the right stem. Trends Mol Med. 2011;17:1–7.

    Article  PubMed  Google Scholar 

  15. McGowan SL, Edelhauser HF, Pfister RR, Whikehart DR. Stem cell markers in the human posterior limbus and corneal endothelium of unwounded and wounded corneas. Mol Vis. 2007;13:1984–2000.

    CAS  PubMed  Google Scholar 

  16. Espana EM, Sun M, Birk DE. Existence of corneal endothelial slow-cycling cells. Invest Ophthalmol Vis Sci. 2015;56:3827–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Noh JW, Kim JJ, Hyon JY, Chung ES, Chung TY, Yi K, Wee WR, Shin YJ. Stemness characteristics of human corneal endothelial cells cultured in various media. Eye Contact Lens. 2015;41:190–6.

    Article  PubMed  Google Scholar 

  18. Yamagami S, Yokoo S, Mimura T, Takato T, Araie M, Amano S. Distribution of precursors in human corneal stromal cells and endothelial cells. Ophthalmology. 2007;114:433–9.

    Article  PubMed  Google Scholar 

  19. Yokoo S, Yamagami S, Yanagi Y, Uchida S, Mimura T, Usui T, Amano S. Human corneal endothelial cell precursors isolated by sphere-forming assay. Invest Ophthalmol Vis Sci. 2005;46:1626–31.

    Article  PubMed  Google Scholar 

  20. Hara S, Hayashi R, Soma T, Kageyama T, Duncan T, Tsujikawa M, Nishida K. Identification and potential application of human corneal endothelial progenitor cells. Stem Cells Dev. 2014;23:2190–201.

    Article  CAS  PubMed  Google Scholar 

  21. Zhu C, Joyce NC. Proliferative response of corneal endothelial cells from young and older donors. Invest Ophthalmol Vis Sci. 2004;45:1743–51.

    Article  PubMed  Google Scholar 

  22. Li W, Sabater AL, Chen YT, Hayashida Y, Chen SY, He H, Tseng SC. A novel method of isolation, preservation, and expansion of human corneal endothelial cells. Invest Ophthalmol Vis Sci. 2007;48:614–20.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Zhu YT, Hayashida Y, Kheirkhah A, He H, Chen SY, Tseng SC. Characterization and comparison of intercellular adherent junctions expressed by human corneal endothelial cells in vivo and in vitro. Invest Ophthalmol Vis Sci. 2008;49:3879–86.

    Article  PubMed  Google Scholar 

  24. Ishino Y, Sano Y, Nakamura T, Connon CJ, Rigby H, Fullwood NJ, Kinoshita S. Amniotic membrane as a carrier for cultivated human corneal endothelial cell transplantation. Invest Ophthalmol Vis Sci. 2004;45:800–6.

    Article  PubMed  Google Scholar 

  25. Walshe J, Harkin DG. Serial explant culture provides novel insights into the potential location and phenotype of corneal endothelial progenitor cells. Exp Eye Res. 2014;127:9–13.

    Article  CAS  PubMed  Google Scholar 

  26. Su CC, Chen CW, Ho WT, Hu FR, Lee SH, Wang IJ. Phenotypes of trypsin- and collagenase-prepared bovine corneal endothelial cells in the presence of a selective Rho kinase inhibitor, Y-27632. Mol Vis. 2015;21:633–43.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Zhu YT, Chen HC, Chen SY, Tseng SC. Nuclear p120 catenin unlocks mitotic block of contact-inhibited human corneal endothelial monolayers without disrupting adherent junctions. J Cell Sci. 2012;125:3636–48.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Peh GS, Toh KP, Ang HP, Seah XY, George BL, Mehta JS. Optimization of human corneal endothelial cell culture: density dependency of successful cultures in vitro. BMC Res Notes. 2013;6:176.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Roy O, Leclerc VB, Bourget JM, Theriault M, Proulx S. Understanding the process of corneal endothelial morphological change in vitro. Invest Ophthalmol Vis Sci. 2015;56:1228–37.

    Article  PubMed  Google Scholar 

  30. Nakahara M, Okumura N, Kay EP, Hagiya M, Imagawa K, Hosoda Y, Kinoshita S, Koizumi N. Corneal endothelial expansion promoted by human bone marrow mesenchymal stem cell-derived conditioned medium. PLoS One. 2013;8:e69009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Okumura N, Kay EP, Nakahara M, Hamuro J, Kinoshita S, Koizumi N. Inhibition of TGF-beta signaling enables human corneal endothelial cell expansion in vitro for use in regenerative medicine. PLoS One. 2013;8:e58000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Peh GS, Chng Z, Ang HP, Cheng TY, Adnan K, Seah XY, George BL, Toh KP, Tan DT, Yam GH, Colman A, Mehta JS. Propagation of human corneal endothelial cells: a novel dual media approach. Cell Transplant. 2015;24:287–304.

    Article  PubMed  Google Scholar 

  33. Peh GS, Adnan K, George BL, Ang HP, Seah XY, Tan DT, Mehta JS. The effects of Rho-associated kinase inhibitor Y-27632 on primary human corneal endothelial cells propagated using a dual media approach. Sci Rep. 2015;5:9167.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Chen Y, Huang K, Nakatsu MN, Xue Z, Deng SX, Fan G. Identification of novel molecular markers through transcriptomic analysis in human fetal and adult corneal endothelial cells. Hum Mol Genet. 2013;22:1271–9.

    Article  CAS  PubMed  Google Scholar 

  35. Cheong YK, Ngoh ZX, Peh GS, Ang HP, Seah XY, Chng Z, Colman A, Mehta JS, Sun W. Identification of cell surface markers glypican-4 and CD200 that differentiate human corneal endothelium from stromal fibroblasts. Invest Ophthalmol Vis Sci. 2013;54:4538–47.

    Article  CAS  PubMed  Google Scholar 

  36. Ding V, Chin A, Peh G, Mehta JS, Choo A. Generation of novel monoclonal antibodies for the enrichment and characterization of human corneal endothelial cells (hCENC) necessary for the treatment of corneal endothelial blindness. MAbs. 2014;6:1439–52.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Yamaguchi M, Shima N, Kimoto M, Ebihara N, Murakami A, Yamagami S. Markers for distinguishing cultured human corneal endothelial cells from corneal stromal myofibroblasts. Curr Eye Res. 2015;40:1211–7.

    Article  CAS  PubMed  Google Scholar 

  38. Armitage WJ, Dick AD, Bourne WM. Predicting endothelial cell loss and long-term corneal graft survival. Invest Ophthalmol Vis Sci. 2003;44:3326–31.

    Article  PubMed  Google Scholar 

  39. Ehlers N. Corneal banking and grafting: the background to the Danish Eye Bank System, where corneas await their patients. Acta Ophthalmol Scand. 2002;80:572–8.

    Article  PubMed  Google Scholar 

  40. Okumura N, Kusakabe A, Hirano H, Inoue R, Okazaki Y, Nakano S, Kinoshita S, Koizumi N. Density-gradient centrifugation enables the purification of cultured corneal endothelial cells for cell therapy by eliminating senescent cells. Sci Rep. 2015;5:15005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Singh JS, Haroldson TA, Patel SP. Characteristics of the low density corneal endothelial monolayer. Exp Eye Res. 2013;115:239–45.

    Article  CAS  PubMed  Google Scholar 

  42. Srinivas SP. Dynamic regulation of barrier integrity of the corneal endothelium. Optom Vis Sci. 2010;87:E239–54.

    PubMed  PubMed Central  Google Scholar 

  43. Peh GS, Beuerman RW, Colman A, Tan DT, Mehta JS. Human corneal endothelial cell expansion for corneal endothelium transplantation: an overview. Transplantation. 2011;91:811–9.

    Article  PubMed  Google Scholar 

  44. Polisetti N, Joyce NC. The culture of limbal stromal cells and corneal endothelial cells. Methods Mol Biol. 2013;1014:131–9.

    Article  CAS  PubMed  Google Scholar 

  45. Mimura T, Yamagami S, Amano S. Corneal endothelial regeneration and tissue engineering. Prog Retin Eye Res. 2013;35:1–17.

    Article  CAS  PubMed  Google Scholar 

  46. Jumblatt MM, Maurice DM, Schwartz BD. A gelatin membrane substrate for the transplantation of tissue cultured cells. Transplantation. 1980;29:498–9.

    Article  CAS  PubMed  Google Scholar 

  47. McCulley JP, Maurice DM, Schwartz BD. Corneal endothelial transplantation. Ophthalmology. 1980;87:194–201.

    Article  CAS  PubMed  Google Scholar 

  48. Schwartz BD, McCulley JP. Morphology of transplanted corneal endothelium derived from tissue culture. Invest Ophthalmol Vis Sci. 1981;20:467–80.

    CAS  PubMed  Google Scholar 

  49. Mohay J, Lange TM, Soltau JB, Wood TO, McLaughlin BJ. Transplantation of corneal endothelial cells using a cell carrier device. Cornea. 1994;13:173–82.

    Article  CAS  PubMed  Google Scholar 

  50. Mohay J, Wood TO, McLaughlin BJ. Long-term evaluation of corneal endothelial cell transplantation. Trans Am Ophthalmol Soc. 1997;95:131–48; discussion 149–51.

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Koizumi N, Sakamoto Y, Okumura N, Okahara N, Tsuchiya H, Torii R, Cooper LJ, Ban Y, Tanioka H, Kinoshita S. Cultivated corneal endothelial cell sheet transplantation in a primate model. Invest Ophthalmol Vis Sci. 2007;48:4519–26.

    Article  PubMed  Google Scholar 

  52. Doillon CJ, Watsky MA, Hakim M, Wang J, Munger R, Laycock N, Osborne R, Griffith M. A collagen-based scaffold for a tissue engineered human cornea: physical and physiological properties. Int J Artif Organs. 2003;26:764–73.

    CAS  PubMed  Google Scholar 

  53. Griffith M, Osborne R, Munger R, Xiong X, Doillon CJ, Laycock NL, Hakim M, Song Y, Watsky MA. Functional human corneal equivalents constructed from cell lines. Science. 1999;286:2169–72.

    Article  CAS  PubMed  Google Scholar 

  54. Mimura T, Yamagami S, Yokoo S, Usui T, Tanaka K, Hattori S, Irie S, Miyata K, Araie M, Amano S. Cultured human corneal endothelial cell transplantation with a collagen sheet in a rabbit model. Invest Ophthalmol Vis Sci. 2004;45:2992–7.

    Article  PubMed  Google Scholar 

  55. Lange TM, Wood TO, McLaughlin BJ. Corneal endothelial cell transplantation using Descemet’s membrane as a carrier. J Cataract Refract Surg. 1993;19:232–5.

    Article  CAS  PubMed  Google Scholar 

  56. Wencan W, Mao Y, Wentao Y, Fan L, Jia Q, Qinmei W, Xiangtian Z. Using basement membrane of human amniotic membrane as a cell carrier for cultivated cat corneal endothelial cell transplantation. Curr Eye Res. 2007;32:199–215.

    Article  PubMed  Google Scholar 

  57. Auger FA, Rémy-Zolghadri M, Grenier G, Germain L. Review: the self-assembly approach for organ reconstruction by tissue engineering. e-biomed J Regen Med. 2000;1:75–86.

    Google Scholar 

  58. L’Heureux N, Paquet S, Labbe R, Germain L, Auger FA. A completely biological tissue-engineered human blood vessel. FASEB J Off publ Federation Am Soc Exp Biol. 1998;12:47–56.

    Google Scholar 

  59. Boulze Pankert M, Goyer B, Zaguia F, Bareille M, Perron MC, Liu X, Cameron JD, Proulx S, Brunette I. Biocompatibility and functionality of a tissue-engineered living corneal stroma transplanted in the feline eye. Invest Ophthalmol Vis Sci. 2014;55:6908–20.

    Article  PubMed  CAS  Google Scholar 

  60. Bourget JM, Proulx S. Characterization of a corneal endothelium engineered on a self-assembled stromal substitute. Exp Eye Res. 2016;145:125–9.

    Article  CAS  PubMed  Google Scholar 

  61. Jay L, Bourget JM, Goyer B, Singh K, Brunette I, Ozaki T, Proulx S. Characterization of tissue-engineered posterior corneas using second- and third-harmonic generation microscopy. PLoS One. 2015;10:e0125564.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Proulx S, d’Arc Uwamaliya J, Carrier P, Deschambeault A, Audet C, Giasson CJ, Guerin SL, Auger FA, Germain L. Reconstruction of a human cornea by the self-assembly approach of tissue engineering using the three native cell types. Mol Vis. 2010;16:2192–201.

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Aboalchamat B, Engelmann K, Bohnke M, Eggli P, Bednarz J. Morphological and functional analysis of immortalized human corneal endothelial cells after transplantation. Exp Eye Res. 1999;69:547–53.

    Article  CAS  PubMed  Google Scholar 

  64. Alvarado JA, Gospodarowicz D, Greenburg G. Corneal endothelial replacement. I. In vitro formation of an endothelial monolayer. Invest Ophthalmol Vis Sci. 1981;21:300–16.

    CAS  PubMed  Google Scholar 

  65. Amano S. Transplantation of cultured human corneal endothelial cells. Cornea. 2003;22:S66–74.

    Article  PubMed  Google Scholar 

  66. Amano S, Mimura T, Yamagami S, Osakabe Y, Miyata K. Properties of corneas reconstructed with cultured human corneal endothelial cells and human corneal stroma. Jpn J Ophthalmol. 2005;49:448–52.

    Article  PubMed  Google Scholar 

  67. Bahn CF, MacCallum DK, Lillie JH, Meyer RF, Martonyi CL. Complications associated with bovine corneal endothelial cell-lined homografts in the cat. Invest Ophthalmol Vis Sci. 1982;22:73–90.

    CAS  PubMed  Google Scholar 

  68. Bohnke M, Eggli P, Engelmann K. Transplantation of cultured adult human or porcine corneal endothelial cells onto human recipients in vitro. Part II: evaluation in the scanning electron microscope. Cornea. 1999;18:207–13.

    Article  CAS  PubMed  Google Scholar 

  69. Chen KH, Azar D, Joyce NC. Transplantation of adult human corneal endothelium ex vivo: a morphologic study. Cornea. 2001;20:731–7.

    Article  CAS  PubMed  Google Scholar 

  70. Engelmann K, Drexler D, Bohnke M. Transplantation of adult human or porcine corneal endothelial cells onto human recipients in vitro. Part I: cell culturing and transplantation procedure. Cornea. 1999;18:199–206.

    Article  CAS  PubMed  Google Scholar 

  71. Gospodarowicz D, Greenburg G. The coating of bovine and rabbit corneas denuded of their endothelium with bovine corneal endothelial cells. Exp Eye Res. 1979;28:249–65.

    Article  CAS  PubMed  Google Scholar 

  72. Gospodarowicz D, Greenburg G, Alvarado J. Transplantation of cultured bovine corneal endothelial cells to rabbit cornea: clinical implications for human studies. Proc Natl Acad Sci U S A. 1979;76:464–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Gospodarowicz D, Greenburg G, Alvarado J. Transplantation of cultured bovine corneal endothelial cells to species with nonregenerative endothelium. The cat as an experimental model. Arch Ophthalmol. 1979;97:2163–9.

    Article  CAS  PubMed  Google Scholar 

  74. Insler MS, Lopez JG. Transplantation of cultured human neonatal corneal endothelium. Curr Eye Res. 1986;5:967–72.

    Article  CAS  PubMed  Google Scholar 

  75. Insler MS, Lopez JG. Extended incubation times improve corneal endothelial cell transplantation success. Invest Ophthalmol Vis Sci. 1991;32:1828–36.

    CAS  PubMed  Google Scholar 

  76. Insler MS, Lopez JG. Heterologous transplantation versus enhancement of human corneal endothelium. Cornea. 1991;10:136–48.

    Article  CAS  PubMed  Google Scholar 

  77. Joo CK, Green WR, Pepose JS, Fleming TP. Repopulation of denuded murine Descemet’s membrane with life-extended murine corneal endothelial cells as a model for corneal cell transplantation. Graefes Arch Clin Exp Ophthalmol. 2000;238:174–80.

    Article  CAS  PubMed  Google Scholar 

  78. Jumblatt MM, Maurice DM, McCulley JP. Transplantation of tissue-cultured corneal endothelium. Invest Ophthalmol Vis Sci. 1978;17:1135–41.

    CAS  PubMed  Google Scholar 

  79. Mimura T, Amano S, Usui T, Araie M, Ono K, Akihiro H, Yokoo S, Yamagami S. Transplantation of corneas reconstructed with cultured adult human corneal endothelial cells in nude rats. Exp Eye Res. 2004;79:231–7.

    Article  CAS  PubMed  Google Scholar 

  80. Tchah H. Heterologous corneal endothelial cell transplantation–human corneal endothelial cell transplantation in Lewis rats. J Korean Med Sci. 1992;7:337–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Lynch AP, Ahearne M. Strategies for developing decellularized corneal scaffolds. Exp Eye Res. 2013;108:42–7.

    Article  CAS  PubMed  Google Scholar 

  82. Proulx S, Audet C, Uwamaliya J, Deschambeault A, Carrier P, Giasson CJ, Brunette I, Germain L. Tissue engineering of feline corneal endothelium using a devitalized human cornea as carrier. Tissue Eng Part A. 2009;15:1709–18.

    Article  CAS  PubMed  Google Scholar 

  83. Proulx S, Bensaoula T, Nada O, Audet C, d’Arc Uwamaliya J, Devaux A, Allaire G, Germain L, Brunette I. Transplantation of a tissue-engineered corneal endothelium reconstructed on a devitalized carrier in the feline model. Invest Ophthalmol Vis Sci. 2009;50:2686–94.

    Article  PubMed  Google Scholar 

  84. Haydari MN, Perron MC, Laprise S, Roy O, Cameron JD, Proulx S, Brunette I. A short-term in vivo experimental model for fuchs endothelial corneal dystrophy. Invest Ophthalmol Vis Sci. 2012;53:6343–54.

    Article  PubMed  Google Scholar 

  85. Mimura T, Yamagami S, Usui T, Seiichi, Honda N, Amano S. Necessary prone position time for human corneal endothelial precursor transplantation in a rabbit endothelial deficiency model. Curr Eye Res. 2007;32:617–23.

    Article  PubMed  Google Scholar 

  86. Mimura T, Yokoo S, Araie M, Amano S, Yamagami S. Treatment of rabbit bullous keratopathy with precursors derived from cultured human corneal endothelium. Invest Ophthalmol Vis Sci. 2005;46:3637–44.

    Article  PubMed  Google Scholar 

  87. Mimura T, Shimomura N, Usui T, Noda Y, Kaji Y, Yamgami S, Amano S, Miyata K, Araie M. Magnetic attraction of iron-endocytosed corneal endothelial cells to Descemet’s membrane. Exp Eye Res. 2003;76:745–51.

    Article  CAS  PubMed  Google Scholar 

  88. Mimura T, Yamagami S, Usui T, Ishii Y, Ono K, Yokoo S, Funatsu H, Araie M, Amano S. Long-term outcome of iron-endocytosing cultured corneal endothelial cell transplantation with magnetic attraction. Exp Eye Res. 2005;80:149–57.

    Article  CAS  PubMed  Google Scholar 

  89. Patel SV, Bachman LA, Hann CR, Bahler CK, Fautsch MP. Human corneal endothelial cell transplantation in a human ex vivo model. Invest Ophthalmol Vis Sci. 2009;50:2123–31.

    Article  PubMed  PubMed Central  Google Scholar 

  90. Moysidis SN, Alvarez-Delfin K, Peschansky VJ, Salero E, Weisman AD, Bartakova A, Raffa GA, Merkhofer Jr RM, Kador KE, Kunzevitzky NJ, Goldberg JL. Magnetic field-guided cell delivery with nanoparticle-loaded human corneal endothelial cells. Nanomedicine. 2015;11:499–509.

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Li S, Wang C, Dai Y, Yang Y, Pan H, Zhong J, Chen J. The stimulatory effect of ROCK inhibitor on bovine corneal endothelial cells. Tissue Cell. 2013;45:387–96.

    Article  CAS  PubMed  Google Scholar 

  92. Pipparelli A, Arsenijevic Y, Thuret G, Gain P, Nicolas M, Majo F. ROCK inhibitor enhances adhesion and wound healing of human corneal endothelial cells. PLoS One. 2013;8:e62095.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Okumura N, Koizumi N, Ueno M, Sakamoto Y, Takahashi H, Tsuchiya H, Hamuro J, Kinoshita S. ROCK inhibitor converts corneal endothelial cells into a phenotype capable of regenerating in vivo endothelial tissue. Am J Pathol. 2012;181:268–77.

    Article  CAS  PubMed  Google Scholar 

  94. He Y, Weng J, Li Q, Knauf HP, Wilson SE. Fuchs’ corneal endothelial cells transduced with the human papilloma virus E6/E7 oncogenes. Exp Eye Res. 1997;65:135–42.

    Article  CAS  PubMed  Google Scholar 

  95. Joyce NC. Proliferative capacity of the corneal endothelium. Prog Retin Eye Res. 2003;22:359–89.

    Article  CAS  PubMed  Google Scholar 

  96. Joyce NC, Zhu CC. Human corneal endothelial cell proliferation: potential for use in regenerative medicine. Cornea. 2004;23:S8–19.

    Article  PubMed  Google Scholar 

  97. Konomi K, Zhu C, Harris D, Joyce NC. Comparison of the proliferative capacity of human corneal endothelial cells from the central and peripheral areas. Invest Ophthalmol Vis Sci. 2005;46:4086–91.

    Article  PubMed  Google Scholar 

  98. Van Horn DL, Sendele DD, Seideman S, Buco PJ. Regenerative capacity of the corneal endothelium in rabbit and cat. Invest Ophthalmol Vis Sci. 1977;16:597–613.

    PubMed  Google Scholar 

  99. Bahn CF, Glassman RM, MacCallum DK, Lillie JH, Meyer RF, Robinson BJ, Rich NM. Postnatal development of corneal endothelium. Invest Ophthalmol Vis Sci. 1986;27:44–51.

    CAS  PubMed  Google Scholar 

  100. Bahn CF, Glassman RM, MacCallum DK, Lillie JH, Meyer RF, Robinson BJ, Rich NM. Postnatal development of corneal endothelium. Invest Ophthalmol Vis Sci. 1986;27:44–51.

    CAS  PubMed  Google Scholar 

  101. Giasson CJ, Gosselin L, Masella A, Forcier P. Does endothelial cell density correlate with corneal diameter in a group of young adults? Cornea. 2008;27:640–3.

    Article  PubMed  Google Scholar 

  102. Bahn CF, Meyer RF, MacCallum DK, Lillie JH, Lovett EJ, Sugar A, Martonyi CL. Penetrating keratoplasty in the cat. A clinically applicable model. Ophthalmology. 1982;89:687–99.

    Article  CAS  PubMed  Google Scholar 

  103. Ohno K, Nelson LR, Mitooka K, Bourne WM. Transplantation of cryopreserved human corneas in a xenograft model. Cryobiology. 2002;44:142–9.

    Article  PubMed  Google Scholar 

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Brunette, I., Proulx, S. (2017). Tissue Engineering of a Healthy Corneal Endothelium for FECD Patients. In: Cursiefen, C., Jun, A. (eds) Current Treatment Options for Fuchs Endothelial Dystrophy. Springer, Cham. https://doi.org/10.1007/978-3-319-43021-8_16

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