Long-term cultivation of human corneal endothelial cells by telomerase expression

Experimental Eye Research

Volumn 100, Issue , 2012, Pages 40-51

  Liu, Zhiping ^a   Zhuang, Jing ^a   Li, Chaoyang ^a   Wan, Pengxia ^a   Li, Naiyang ^a   Zhou, Qiang ^a   Zhou, Chenjing ^a   Huang, Zheqian ^a   Wang, Zhichong ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

Cell line; Cornea; Corneal endothelial cells; Telomerase

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); BICARBONATE SODIUM COTRANSPORTER; BICARBONATE SODIUM COTRANSPORTER MEMBER 4; CHLORIDE CHANNEL PROTEIN 3; PROTEIN ZO1; REGULATOR PROTEIN; SODIUM POTASSIUM ATPASE ALPHA1; TELOMERASE REVERSE TRANSCRIPTASE; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL 3;

ADOLESCENT; ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL JUNCTION; CELL LINEAGE; CELL POPULATION; CELL PROLIFERATION; CHROMOSOME NUMBER; CONTROLLED STUDY; CORNEA ENDOTHELIUM; CORNEA ENDOTHELIUM CELL; ENDOTHELIUM CELL; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; KARYOTYPE; LIFESPAN; MONOLAYER CULTURE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADOLESCENT; AGED; AGING; ANIMALS; APOPTOSIS; CELL CYCLE; CELL PROLIFERATION; CELLS, CULTURED; CHILD; CHLORIDE CHANNELS; DNA PRIMERS; ENDOTHELIUM, CORNEAL; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; INFANT, NEWBORN; KARYOTYPING; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, NUDE; MIDDLE AGED; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; PHOSPHOPROTEINS; PRIMARY CELL CULTURE; SODIUM-BICARBONATE SYMPORTERS; SODIUM-POTASSIUM-EXCHANGING ATPASE; TELOMERASE; TISSUE DONORS; TRANSFECTION; VOLTAGE-DEPENDENT ANION CHANNELS; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84862698260     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2012.04.013     Document Type: Article

References (85)

1. 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, 69:547-553.
2. Avisar R., Weinberger D. Corneal endothelial morphologic features in toxic anterior segment syndrome. Cornea 2010, 29:251-253.
3. Bednarz J., Teifel M., Friedl P., Engelmann K. Immortalization of human corneal endothelial cells using electroporation protocol optimized for human corneal endothelial and human retinal pigment epithelial cells. Acta Ophthalmol. Scand. 2000, 78:130-136.
4. Blake D.A., Yu H., Young D.L., Caldwell D.R. Matrix stimulates the proliferation of human corneal endothelial cells in culture. Invest. Ophthalmol. Vis. Sci. 1997, 38:1119-1129.
5. Bodnar A.G., Ouellette M., Frolkis M., Holt S.E., Chiu C.P., Morin G.B., Harley C.B., Shay J.W., Lichtsteiner S., Wright W.E. Extension of life-span by introduction of telomerase into normal human cells. Science 1998, 279:349-352.
6. Bourne W.M., Nelson L.R., Hodge D.O. Continued endothelial cell loss ten years after lens implantation. Ophthalmology 1994, 101:1014-1022. (discussion 1022-1013).
7. Burger A.M., Double J.A., Newell D.R. Inhibition of telomerase activity by cisplatin in human testicular cancer cells. Eur. J. Cancer 1997, 33:638-644.
8. Chen K.H., Azar D., Joyce N.C. Transplantation of adult human corneal endothelium ex vivo: a morphologic study. Cornea 2001, 20:731-737.
9. Dikstein S., Maurice D.M. The metabolic basis to the fluid pump in the cornea. J. Physiol. 1972, 221:29-41.
10. Egan C.A., Savre-Train I., Shay J.W., Wilson S.E., Bourne W.M. Analysis of telomere lengths in human corneal endothelial cells from donors of different ages. Invest. Ophthalmol. Vis. Sci. 1998, 39:648-653.
11. Elmore L.W., Rehder C.W., Di X., McChesney P.A., Jackson-Cook C.K., Gewirtz D.A., Holt S.E. Adriamycin-induced senescence in breast tumor cells involves functional p53 and telomere dysfunction. J. Biol. Chem. 2002, 277:35509-35515.
12. Engelmann K., Bohnke M. Growing human corneal endothelium in cell culture. Fortschr. Ophthalmol. 1989, 86:72-75.
13. Enomoto K., Mimura T., Harris D.L., Joyce N.C. Age differences in cyclin-dependent kinase inhibitor expression and rb hyperphosphorylation in human corneal endothelial cells. Invest. Ophthalmol. Vis. Sci. 2006, 47:4330-4340.
14. Fan T., Wang D., Zhao J., Wang J., Fu Y., Guo R. Establishment and characterization of a novel untransfected corneal endothelial cell line from New Zealand white rabbits. Mol. Vis. 2009, 15:1070-1078.
15. Fan T., Zhao J., Ma X., Xu X., Zhao W., Xu B. Establishment of a continuous untransfected human corneal endothelial cell line and its biocompatibility to denuded amniotic membrane. Mol. Vis. 2011, 17:469-480.
16. Feldman S.T., Gjerset R., Gately D., Chien K.R., Feramisco J.R. Expression of SV40 virus large T antigen by recombinant adenoviruses activates proliferation of corneal endothelium in vitro. J. Clin. Invest. 1993, 91:1713-1720.
17. Flint J., Craddock C.F., Villegas A., Bentley D.P., Williams H.J., Galanello R., Cao A., Wood W.G., Ayyub H., Higgs D.R. Healing of broken human chromosomes by the addition of telomeric repeats. Am. J. Hum. Genet. 1994, 55:505-512.
18. Foets B., van den Oord J., Engelmann K., Missotten L. A comparative immunohistochemical study of human corneotrabecular tissue. Graefes. Arch. Clin. Exp. Ophthalmol. 1992, 230:269-274.
19. Friberg T.R., Guibord N.M. Corneal endothelial cell loss after multiple vitreoretinal procedures and the use of silicone oil. Ophthalmic Surg. Lasers 1999, 30:528-534.
20. Fu W., Begley J.G., Killen M.W., Mattson M.P. Anti-apoptotic role of telomerase in pheochromocytoma cells. J. Biol. Chem. 1999, 274:7264-7271.
21. Furuse M., Hirase T., Itoh M., Nagafuchi A., Yonemura S., Tsukita S., Tsukita S. Occludin: a novel integral membrane protein localizing at tight junctions. J. Cell Biol. 1993, 123:1777-1788.
22. Gendron R.L., Liu C.Y., Paradis H., Adams L.C., Kao W.W. MK/T-1, an immortalized fibroblast cell line derived using cultures of mouse corneal stroma. Mol. Vis. 2001, 7:107-113.
23. Guan L.S., Li G.C., Chen C.C., Liu L.Q., Wang Z.Y. Rb-associated protein 46 (RbAp46) suppresses the tumorigenicity of adenovirus-transformed human embryonic kidney 293 cells. Int. J. Cancer 2001, 93:333-338.
24. Hande M.P., Lansdorp P.M., Natarajan A.T. Induction of telomerase activity by in vivo X-irradiation of mouse splenocytes and its possible role in chromosome healing. Mutat. Res. 1998, 404:205-214.
25. Harley C.B., Vaziri H., Counter C.M., Allsopp R.C. The telomere hypothesis of cellular aging. Exp. Gerontol. 1992, 27:375-382.
26. Hoppenreijs V.P., Pels E., Vrensen G.F., Treffers W.F. Effects of platelet-derived growth factor on endothelial wound healing of human corneas. Invest. Ophthalmol. Vis. Sci. 1994, 35:150-161.
27. Huang B., Blanco G., Mercer R.W., Fleming T., Pepose J.S. Human corneal endothelial cell expression of Na+, K+-adenosine triphosphatase isoforms. Arch. Ophthalmol. 2003, 121:840-845.
28. Huang X.Q., Wang J., Liu J.P., Feng H., Liu W.B., Yan Q., Liu Y., Sun S.M., Deng M., Gong L., Liu Y., Li D.W. hTERT extends proliferative lifespan and prevents oxidative stress-induced apoptosis in human lens epithelial cells. Invest. Ophthalmol. Vis. Sci. 2005, 46:2503-2513.
29. Johnstone E.W., Wong H.C., Coster D.J., Williams K.A. Factors affecting bovine corneal endothelial cell density in vitro. Br. J. Ophthalmol. 1996, 80:256-262.
30. Joyce N.C. Proliferative capacity of the corneal endothelium. Prog. Retin. Eye Res. 2003, 22:359-389.
31. Joyce N.C. Proliferative capacity of corneal endothelial cells. Exp. Eye Res. 2012, 95:16-23.
32. Joyce N.C., Zhu C.C. Human corneal endothelial cell proliferation: potential for use in regenerative medicine. Cornea 2004, 23:S8-S19.
33. Joyce N.C., Meklir B., Joyce S.J., Zieske J.D. Cell cycle protein expression and proliferative status in human corneal cells. Invest. Ophthalmol. Vis. Sci. 1996, 37:645-655.
34. Joyce N.C., Navon S.E., Roy S., Zieske J.D. Expression of cell cycle-associated proteins in human and rabbit corneal endothelium in situ. Invest. Ophthalmol. Vis. Sci. 1996, 37:1566-1575.
35. Joyce N.C., Harris D.L., Zieske J.D. Mitotic inhibition of corneal endothelium in neonatal rats. Invest. Ophthalmol. Vis. Sci. 1998, 39:2572-2583.
36. Jumblatt M.M., Maurice D.M., McCulley J.P. Transplantation of tissue-cultured corneal endothelium. Invest. Ophthalmol. Vis. Sci. 1978, 17:1135-1141.
37. Kim H.J., Ryu Y.H., Ahn J.I., Park J.K., Kim J.C. Characterization of immortalized human corneal endothelial cell line using HPV 16 E6/E7 on lyophilized human amniotic membrane. Korean J. Ophthalmol. 2006, 20:47-54.
38. Kondo S., Tanaka Y., Kondo Y., Hitomi M., Barnett G.H., Ishizaka Y., Liu J., Haqqi T., Nishiyama A., Villeponteau B., Cowell J.K., Barna B.P. Antisense telomerase treatment: induction of two distinct pathways, apoptosis and differentiation. FASEB J. 1998, 12:801-811.
39. Krishan A., Cabana R. Flow cytometric analysis of electronic nuclear volume and DNA content in normal mouse tissues. Cell Cycle 2004, 3:380-383.
40. Li Q.J., Ashraf M.F., Shen D.F., Green W.R., Stark W.J., Chan C.C., O'Brien T.P. The role of apoptosis in the pathogenesis of Fuchs endothelial dystrophy of the cornea. Arch. Ophthalmol. 2001, 119:1597-1604.
41. Liu J., Song G., Wang Z., Huang B., Gao Q., Liu B., Xu Y., Liang X., Ma P., Gao N., Ge J. Establishment of a corneal epithelial cell line spontaneously derived from human limbal cells. Exp. Eye Res. 2007, 84:599-609.
42. Liu Y., Ma P., Wu Z., Duan H., Ding Y., Liu Z., Wan P., Lu X., Xiang P., Ge J., Wang Z. Enhancement of long-term proliferative capacity of rabbit corneal epithelial cells by embryonic stem cell conditioned medium. Tissue Eng. Part C Methods 2009.
43. Mandal M., Kumar R. Bcl-2 modulates telomerase activity. J. Biol. Chem. 1997, 272:14183-14187.
44. Matsuda M., Inaba M., Suda T., MacRae S.M. Corneal endothelial changes associated with aphakic extended contact lens wear. Arch. Ophthalmol. 1988, 106:70-72.
45. Matsuda M., MacRae S.M., Inaba M., Manabe R. The effect of hard contact lens wear on the keratoconic corneal endothelium after penetrating keratoplasty. Am. J. Ophthalmol. 1989, 107:246-251.
46. Maurice D.M. The structure and transparency of the cornea. J. Physiol. 1957, 136:263-286.
47. Maurice D.M. The location of the fluid pump in the cornea. J. Physiol. 1972, 221:43-54.
48. McCarthy K.M., Skare I.B., Stankewich M.C., Furuse M., Tsukita S., Rogers R.A., Lynch R.D., Schneeberger E.E. Occludin is a functional component of the tight junction. J. Cell Sci. 1996, 109(Pt 9):2287-2298.
49. Melles G.R., Lander F., Rietveld F.J. Transplantation of Descemet's membrane carrying viable endothelium through a small scleral incision. Cornea 2002, 21:415-418.
50. Mimura T., Joyce N.C. Replication competence and senescence in central and peripheral human corneal endothelium. Invest. Ophthalmol. Vis. Sci. 2006, 47:1387-1396.
51. 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, 79:231-237.
52. 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, 45:2992-2997.
53. Mimura T., Yamagami S., Yokoo S., Usui T., Amano S. Selective isolation of young cells from human corneal endothelium by the sphere-forming assay. Tissue Eng. Part C Methods 2009.
54. Mimura T., Yamagami S., Yokoo S., Usui T., Amano S. Selective isolation of young cells from human corneal endothelium by the sphere-forming assay. Tissue Eng. Part C Methods 2010, 16:803-812.
55. Morales C.P., Holt S.E., Ouellette M., Kaur K.J., Yan Y., Wilson K.S., White M.A., Wright W.E., Shay J.W. Absence of cancer-associated changes in human fibroblasts immortalized with telomerase. Nat. Genet. 1999, 21:115-118.
56. Morin G.B. Recognition of a chromosome truncation site associated with alpha-thalassaemia by human telomerase. Nature 1991, 353:454-456.
57. Nitta M., Katabuchi H., Ohtake H., Tashiro H., Yamaizumi M., Okamura H. Characterization and tumorigenicity of human ovarian surface epithelial cells immortalized by SV40 large T antigen. Gynecol. Oncol. 2001, 81:10-17.
58. O'Neal M.R., Polse K.A. In vivo assessment of mechanisms controlling corneal hydration. Invest. Ophthalmol. Vis. Sci. 1985, 26:849-856.
59. Odenthal M.T., Gan I.M., Oosting J., Kijlstra A., Beekhuis W.H. Long-term changes in corneal endothelial morphology after discontinuation of low gas-permeable contact lens wear. Cornea 2005, 24:32-38.
60. Patterson M.K. Measurement of growth and viability of cells in culture. Methods Enzymol. 1979, 58:141-152.
61. Pellegrini G., Dellambra E., Paterna P., Golisano O., Traverso C.E., Rama P., Lacal P., De Luca M. Telomerase activity is sufficient to bypass replicative senescence in human limbal and conjunctival but not corneal keratinocytes. Eur. J. Cell Biol. 2004, 83:691-700.
62. Petroll W.M., Hsu J.K., Bean J., Cavanagh H.D., Jester J.V. The spatial organization of apical junctional complex-associated proteins in feline and human corneal endothelium. Curr. Eye Res. 1999, 18:10-19.
63. Pistsov M.Y., Sadovnikova E., Danilov S.M. Human corneal endothelial cells: isolation, characterization and long-term cultivation. Exp. Eye Res. 1988, 47:403-414.
64. Price F.W., Price M.O. Descemet's stripping with endothelial keratoplasty in 50 eyes: a refractive neutral corneal transplant. J. Refract. Surg. 2005, 21:339-345.
65. Robertson D.M., Li L., Fisher S., Pearce V.P., Shay J.W., Wright W.E., Cavanagh H.D., Jester J.V. Characterization of growth and differentiation in a telomerase-immortalized human corneal epithelial cell line. Invest. Ophthalmol. Vis. Sci. 2005, 46:470-478.
66. Ross A.H., Jones M.N., Nguyen D.Q., Jaycock P.D., Armitage W.J., Cook S.D., Kaye S.B., Tole D.M. Long-term topical steroid treatment after penetrating keratoplasty in patients with pseudophakic bullous keratopathy. Ophthalmology 2009, 116:2369-2372.
67. Rubio M.A., Kim S.H., Campisi J. Reversible manipulation of telomerase expression and telomere length - implications for the ionizing radiation response and replicative senescence of human cells. J. Biol. Chem. 2002, 277:28609-28617.
68. Sawada H., Konomi H., Hirosawa K. Characterization of the collagen in the hexagonal lattice of Descemet's membrane: its relation to type VIII collagen. J. Cell Biol. 1990, 110:219-227.
69. Schonthal A.H., Hwang J.J., Stevenson D., Trousdale M.D. Expression and activity of cell cycle-regulatory proteins in normal and transformed corneal endothelial cells. Exp. Eye Res. 1999, 68:531-539.
70. Senoo T., Joyce N.C. Cell cycle kinetics in corneal endothelium from old and young donors. Invest. Ophthalmol. Vis. Sci. 2000, 41:660-667.
71. Sheerin A.N., Smith S.K., Jennert-Burston K., Brook A.J., Allen M.C., Ibrahim B., Jones D., Wallis C., Engelmann K., Rhys-Williams W., Faragher R.G., Kipling D. Characterization of cellular senescence mechanisms in human corneal endothelial cells. Aging Cell 2011.
72. Stevenson B.R., Siliciano J.D., Mooseker M.S., Goodenough D.A. Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J. Cell Biol. 1986, 103:755-766.
73. Terry M.A., Ousley P.J. Deep lamellar endothelial keratoplasty in the first United States patients: early clinical results. Cornea 2001, 20:239-243.
74. Tomas-Loba A., Flores I., Fernandez-Marcos P.J., Cayuela M.L., Maraver A., Tejera A., Borras C., Matheu A., Klatt P., Flores J.M., Vina J., Serrano M., Blasco M.A. Telomerase reverse transcriptase delays aging in cancer-resistant mice. Cell 2008, 135:609-622.
75. Tsao S.W., Mok S.C., Fey E.G., Fletcher J.A., Wan T.S., Chew E.C., Muto M.G., Knapp R.C., Berkowitz R.S. Characterization of human ovarian surface epithelial cells immortalized by human papilloma viral oncogenes (HPV-E6E7 ORFs). Exp. Cell Res. 1995, 218:499-507.
76. Valtink M., Gruschwitz R., Funk R.H., Engelmann K. Two clonal cell lines of immortalized human corneal endothelial cells show either differentiated or precursor cell characteristics. Cells Tissues Organs 2008, 187:286-294.
77. van Setten G.B., Fagerholm P., Philipson B., Schultz G. Growth factors and their receptors in the anterior chamber. Absence of epidermal growth factor and transforming growth factor alpha in human aqueous humor. Ophthalmic Res. 1996, 28:361-364.
78. Whikehart D.R., Parikh C.H., Vaughn A.V., Mishler K., Edelhauser H.F. Evidence suggesting the existence of stem cells for the human corneal endothelium. Mol. Vis. 2005, 11:816-824.
79. Wilkie A.O., Lamb J., Harris P.C., Finney R.D., Higgs D.R. A truncated human chromosome 16 associated with alpha thalassaemia is stabilized by addition of telomeric repeat (TTAGGG)n. Nature 1990, 346:868-871.
80. Wilson S.E., Lloyd S.A. Epidermal growth factor and its receptor, basic fibroblast growth factor, transforming growth factor beta-1, and interleukin-1 alpha messenger RNA production in human corneal endothelial cells. Invest. Ophthalmol. Vis. Sci. 1991, 32:2747-2756.
81. Wilson S.E., Lloyd S.A., He Y.G., McCash C.S. Extended life of human corneal endothelial cells transfected with the SV40 large T antigen. Invest. Ophthalmol. Vis. Sci. 1993, 34:2112-2123.
82. Wilson S.E., Weng J., Blair S., He Y.G., Lloyd S. Expression of E6/E7 or SV40 large T antigen-coding oncogenes in human corneal endothelial cells indicates regulated high-proliferative capacity. Invest. Ophthalmol. Vis. Sci. 1995, 36:32-40.
83. Yee R.W., Matsuda M., Schultz R.O., Edelhauser H.F. Changes in the normal corneal endothelial cellular pattern as a function of age. Curr. Eye Res. 1985, 4:671-678.
84. Yoeruek E., Spitzer M.S., Tatar O., Biedermann T., Grisanti S., Luke M., Bartz-Schmidt K.U., Szurman P. Toxic effects of recombinant tissue plasminogen activator on cultured human corneal endothelial cells. Invest. Ophthalmol. Vis. Sci. 2008, 49:1392-1397.
85. Yokoi T., Seko Y., Makino H., Hatou S., Yamada M., Kiyono T., Umezawa A., Nishina H., Azuma N. Establishment of functioning human corneal endothelial cell line with high growth potential. PLoS One 2012, 7:e29677.