Successful Consecutive Expansion of Limbal Explants Using a Biosafe Culture Medium under Feeder Layer-Free Conditions

References

• Notara M, Alatza A, Gilfillan J, Harris AR, Levis HJ, Schrader S, et al. In sickness and in health: corneal epithelial stem cell biology, pathology and therapy. Exp Eye Res 2010;90:188–195.
   PubMed Web of Science ®Google Scholar
• O’Callaghan AR, Daniels JT. Concise review: limbal epithelial stem cell therapy: controversies and challenges. Stem Cells 2011;29:1923–1932.
   PubMed Web of Science ®Google Scholar
• Ordonez P, Di Girolamo N. Limbal epithelial stem cells: role of the niche microenvironment. Stem Cells 2012;30:100–107.
   PubMed Web of Science ®Google Scholar
• Dua HS, Saini JS, Azuara-Blanco A, Gupta P. Limbal stem cell deficiency: concept, aetiology, clinical presentation, diagnosis and management. Indian J Ophthalmol 2000;48:83–92.
   PubMedGoogle Scholar
• Baylis O, Figueiredo F, Henein C, Lako M, Ahmad S. 13 years of cultured limbal epithelial cell therapy: a review of the outcomes. J Cell Biochem 2011;112:993–1002.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Ma L. Systematic review and meta-analysis on transplantation of ex vivo cultivated limbal epithelial stem cell on amniotic membrane in limbal stem cell deficiency. Cornea 2015;34:592–600.
   PubMed Web of Science ®Google Scholar
• Green H. Cyclic AMP in relation to proliferation of the epidermal cell: a new view. Cell 1978;15:801–811.
   PubMed Web of Science ®Google Scholar
• Schwab IR, Johnson NT, Harkin DG. Inherent risks associated with manufacture of bioengineered ocular surface tissue. Arch Ophthalmol 2006;124:1734–1740.
   PubMed Web of Science ®Google Scholar
• Cao XG, Li XX, Bao YZ, Xing NZ, Chen Y. Responses of human lens epithelial cells to quercetin and DMSO. Invest Ophthalmol Vis Sci 2007;48:3714–3718.
   PubMed Web of Science ®Google Scholar
• Akkok CA, Holte MR, Tangen JM, Ostenstad B, Bruserud O. Hematopoietic engraftment of dimethyl sulfoxide-depleted autologous peripheral blood progenitor cells. Transfusion 2009;49:354–361.
   PubMed Web of Science ®Google Scholar
• Caselli D, Tintori V, Messeri A, Frenos S, Bambi F, Arico M. Respiratory depression and somnolence in children receiving dimethylsulfoxide and morphine during hematopoietic stem cells transplantation. Haematologica 2009;94:152–153.
   PubMed Web of Science ®Google Scholar
• Kruse FE, Tseng SC. Serum differentially modulates the clonal growth and differentiation of cultured limbal and corneal epithelium. Invest Ophthalmol Vis Sci 1993;34:2976–2989.
   PubMed Web of Science ®Google Scholar
• Di Girolamo N, Bosch M, Zamora K, Coroneo MT, Wakefield D, Watson SL. A contact lens-based technique for expansion and transplantation of autologous epithelial progenitors for ocular surface reconstruction. Transplantation 2009;87:1571–1578.
   PubMed Web of Science ®Google Scholar
• Mariappan I, Maddileti S, Savy S, Tiwari S, Gaddipati S, Fatima A, et al. In vitro culture and expansion of human limbal epithelial cells. Nat Protoc 2010;5:1470–1479.
   PubMed Web of Science ®Google Scholar
• Albert R, Vereb Z, Csomos K, Moe MC, Johnsen EO, Olstad OK, et al. Cultivation and characterization of cornea limbal epithelial stem cells on lens capsule in animal material-free medium. PLoS One 2012;7:e47187.
   PubMed Web of Science ®Google Scholar
• Pathak M, Cholidis S, Haug K, Shahdadfar A, Moe MC, Nicolaissen B, et al. Clinical transplantation of ex vivo expanded autologous limbal epithelial cells using a culture medium with human serum as single supplement: a retrospective case series. Acta Ophthalmol 2013;91:769–775.
   PubMed Web of Science ®Google Scholar
• Zakaria N, Possemiers T, Dhubhghaill SN, Leysen I, Rozema J, Koppen C, et al. Results of a phase I/II clinical trial: standardized, non-xenogenic, cultivated limbal stem cell transplantation. J Transl Med 2014;3;12:58. doi: 10.1186/1479-5876-12-58.
   Web of Science ®Google Scholar
• Shahdadfar A, Haug K, Pathak M, Drolsum L, Olstad OK, Johnsen EO, et al. Ex vivo expanded autologous limbal epithelial cells on amniotic membrane using a culture medium with human serum as single supplement. Exp Eye Res 2012;97:1–9.
   PubMed Web of Science ®Google Scholar
• Lopez-Paniagua M, Nieto-Miguel T, de la Mata A, Galindo S, Herreras JM, Corrales RM, et al. Consecutive expansion of limbal epithelial stem cells from a single limbal biopsy. Curr Eye Res 2013;38:537–549.
   PubMed Web of Science ®Google Scholar
• Kim HS, Jun SX, de Paiva CS, Chen Z, Pflugfelder SC, Li DQ. Phenotypic characterization of human corneal epithelial cells expanded ex vivo from limbal explant and single cell cultures. Exp Eye Res 2004;79:41–49.
   PubMed Web of Science ®Google Scholar
• Espana EM, Romano AC, Kawakita T, Di Pascuale M, Smiddy R, Tseng SC. Novel enzymatic isolation of an entire viable human limbal epithelial sheet. Invest Ophthalmol Vis Sci 2003;44:4275–4281.
   PubMed Web of Science ®Google Scholar
• Hernandez Galindo EE, Theiss C, Steuhl KP, Meller D. Gap junctional communication in microinjected human limbal and peripheral corneal epithelial cells cultured on intact amniotic membrane. Exp Eye Res 2003;76:303–314.
   PubMed Web of Science ®Google Scholar
• Ebato B, Friend J, Thoft RA. Comparison of limbal and peripheral human corneal epithelium in tissue culture. Invest Ophthalmol Vis Sci 1988;29:1533–1537.
   PubMed Web of Science ®Google Scholar
• Shortt AJ, Secker GA, Rajan MS, Meligonis G, Dart JK, Tuft SJ, et al. Ex vivo expansion and transplantation of limbal epithelial stem cells. Ophthalmology 2008;115:1989–1997.
   PubMed Web of Science ®Google Scholar
• Kolli S, Ahmad S, Lako M, Figueiredo F. Successful clinical implementation of corneal epithelial stem cell therapy for treatment of unilateral limbal stem cell deficiency. Stem Cells 2010;28:597–610.
   PubMed Web of Science ®Google Scholar
• Rama P, Matuska S, Paganoni G, Spinelli A, De LM, Pellegrini G. Limbal stem-cell therapy and long-term corneal regeneration. N Engl J Med 2010;363:147–155.
   PubMed Web of Science ®Google Scholar
• Ramirez BE, Sánchez A, Herreras JM, Fernández I, García-Sancho J, Nieto-Miguel T, et al. Stem cell therapy for corneal epithelium regeneration following good manufacturing and clinical procedures. Biomed Res Int 2015;2015:408495. doi: 10.1155/2015/408495.
   PubMed Web of Science ®Google Scholar
• Lindberg K, Brown ME, Chaves HV, Kenyon KR, Rheinwald JG. In vitro propagation of human ocular surface epithelial cells for transplantation. Invest Ophthalmol Vis Sci 1993;34:2672–2679.
   PubMed Web of Science ®Google Scholar
• Stasi K, Goings D, Huang J, Herman L, Pinto F, Addis RC, et al. Optimal isolation and xeno-free culture conditions for limbal stem cell function. Invest Ophthalmol Vis Sci 2014;20:375–386.
   Web of Science ®Google Scholar
• Takagi R, Yamato M, Murakami D, Kondo M, Yang J, Ohki T, et al. Preparation of keratinocyte culture medium for the clinical applications of regenerative medicine. J Tissue Eng Regen Med 2011;5:63–73.
   Web of Science ®Google Scholar
• Ghoubay-Benallaoua D, Pecha F, Goldschmidt P, Fialaire-Legendre A, Chaumeil C, Laroche L, et al. Effects of isoproterenol and cholera toxin on human limbal epithelial cell cultures. Curr Eye Res 2012;37:644–653.
   PubMed Web of Science ®Google Scholar
• Gill DM. Mechanism of action of cholera toxin. Adv Cyclic Nucleotide Res 1977;8:85–118.
   PubMedGoogle Scholar
• Formanek M, Millesi W, Willheim M, Scheiner O, Kornfehl J. Optimized growth medium for primary culture of human oral keratinocytes. Int J Oral Maxillofac Surg 1996;25:157–160.
   PubMed Web of Science ®Google Scholar
• Hanslick JL, Lau K, Noguchi KK, Olney JW, Zorumski CF, Mennerick S, et al. Dimethyl sulfoxide (DMSO) produces widespread apoptosis in the developing central nervous system. Neurobiol Dis 2009;34:1–10.
   PubMed Web of Science ®Google Scholar
• Barnes D, Sato G. Methods for growth of cultured cells in serum-free medium. Anal Biochem 1980;102:255–270.
   PubMed Web of Science ®Google Scholar
• Gronbaek H, Frystyk J, Orskov H, Flyvbjerg A. Effect of sodium selenite on growth, insulin-like growth factor-binding proteins and insulin-like growth factor-I in rats. J Endocrinol 1995;145:105–112.
   PubMed Web of Science ®Google Scholar
• Nakamura T, Ang LP, Rigby H, Sekiyama E, Inatomi T, Sotozono C, et al. The use of autologous serum in the development of corneal and oral epithelial equivalents in patients with Stevens-Johnson syndrome. Invest Ophthalmol Vis Sci 2006;47:909–916.
   PubMed Web of Science ®Google Scholar
• Vemuganti GK, Kashyap S, Sangwan VS, Singh S. Ex-vivo potential of cadaveric and fresh limbal tissues to regenerate cultured epithelium. Indian J Ophthalmol 2004;52:113–120.
   PubMedGoogle Scholar
• Notara M, Shortt AJ, O’Callaghan AR, Daniels JT. The impact of age on the physical and cellular properties of the human limbal stem cell niche. Age (Dordr) 2013;35:289–300.
   PubMed Web of Science ®Google Scholar
• Moll R, Divo M, Langbein L. The human keratins: biology and pathology. Histochem Cell Biol 2008;129:705–733.
   PubMed Web of Science ®Google Scholar
• Ma DH, Tsai RJ, Chu WK, Kao CH, Chen JK. Inhibition of vascular endothelial cell morphogenesis in cultures by limbal epithelial cells. Invest Ophthalmol Vis Sci 1999;40:1822–1828.
   PubMed Web of Science ®Google Scholar
• Higa K, Shimmura S, Miyashita H, Shimazaki J, Tsubota K. Melanocytes in the corneal limbus interact with K19-positive basal epithelial cells. Exp Eye Res 2005;81:218–223.
   PubMed Web of Science ®Google Scholar
• Chen W, Hara K, Tian Q, Zhao K, Yoshitomi T. Existence of small slow-cycling Langerhans cells in the limbal basal epithelium that express ABCG2. Exp Eye Res 2007;84:626–634.
   PubMed Web of Science ®Google Scholar
• Ryan DG, Taliana L, Sun L, Wei ZG, Masur SK, Lavker RM. Involvement of S100A4 in stromal fibroblasts of the regenerating cornea. Invest Ophthalmol Vis Sci 2003;44:4255–4262.
   PubMed Web of Science ®Google Scholar
• Schlotzer-Schrehardt U, Kruse FE. Identification and characterization of limbal stem cells. Exp Eye Res 2005;81:247–264.
   PubMed Web of Science ®Google Scholar
• Nieto-Miguel T, Calonge M, de la Mata A, Lopez-Paniagua M, Galindo S, de la Paz MF, et al. A comparison of stem cell-related gene expression in the progenitor-rich limbal epithelium and the differentiating central corneal epithelium. Mol Vis 2011;17:2102–2117.
   PubMed Web of Science ®Google Scholar
• Li W, Hayashida Y, He H, Kuo CL, Tseng SC. The fate of limbal epithelial progenitor cells during explant culture on intact amniotic membrane. Invest Ophthalmol Vis Sci 2007;48:605–613.
   PubMed Web of Science ®Google Scholar
• Selver OB, Barash A, Ahmed M, Wolosin JM. ABCG2-dependent dye exclusion activity and clonal potential in epithelial cells continuously growing for 1 month from limbal explants. Invest Ophthalmol Vis Sci 2011;52:4330–4337.
   PubMed Web of Science ®Google Scholar
• Du Y, Funderburgh ML, Mann MM, SundarRaj N, Funderburgh JL. Multipotent stem cells in human corneal stroma. Stem Cells 2005;23:1266–1275.
   PubMed Web of Science ®Google Scholar
• Kawakita T, Espana EM, He H, Li W, Liu CY, Tseng SC. Intrastromal invasion by limbal epithelial cells is mediated by epithelial-mesenchymal transition activated by air exposure. Am J Pathol 2005;167:381–393.
   PubMed Web of Science ®Google Scholar
• Tan EK, He H, Tseng SC. Epidermal differentiation and loss of clonal growth potential of human limbal basal epithelial progenitor cells during intrastromal invasion. Invest Ophthalmol Vis Sci 2011;52:4534–4545.
   PubMed Web of Science ®Google Scholar
• Ma X, Shimmura S, Miyashita H, Yoshida S, Kubota M, Kawakita T, et al. Long-term culture and growth kinetics of murine corneal epithelial cells expanded from single corneas. Invest Ophthalmol Vis Sci 2009;50:2716–2721.
   PubMed Web of Science ®Google Scholar