Epithelial stem cells of the eye surface

Cell Proliferation

Volumn 40, Issue 4, 2007, Pages 445-461

  Revoltella, R P ^a   Papini, S ^a   Rosellini, A ^a   Michelini, M ^a  

^a CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKERATIN;

AUTOCRINE EFFECT; CELL DIFFERENTIATION; CELL GROWTH; CELL RENEWAL; CELL SURVIVAL; CELL ULTRASTRUCTURE; CONJUNCTIVA; CORNEA; CORNEA LIMBUS; CORNEA TRANSPLANTATION; CYTOARCHITECTURE; HUMAN; PARACRINE SIGNALING; PROGENY; REVIEW; STEM CELL TRANSPLANTATION; STROMA CELL;

ADULT; CELL CULTURE TECHNIQUES; CONJUNCTIVA; EPITHELIAL CELLS; EPITHELIUM, CORNEAL; HUMANS; KERATINS; LIMBUS CORNEAE; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 34447296758     PISSN: 09607722     EISSN: 13652184     Source Type: Journal    
DOI: 10.1111/j.1365-2184.2007.00450.x     Document Type: Review

References (117)

1. Alison MR (2003) Tissue-based stem cells: ABC transporter proteins take centre stage. J. Pathol. 200, 553 560.
2. Ambati BK, Nozaki M, Singh N, Takeda A, Jani PD, Suthar T, Albuquerque RJ, Richter E, Sakurai E, Newcomb MT, Kleinman ME, Caldwell RB, Lin Q, Ogura Y, Orecchia A, Samuelson DA, Agnew DW, St Leger J, Green WR, Mahasreshti PJ, Curiel DT, Kwan D, Marsh H, Ikeda S, Leiper LJ, Collinson JM, Bogdanovich S, Khurana TS, Shibuya M, Baldwin ME, Ferrara N, Gerber HP, De Falco S, Witta J, Baffi JZ, Raisler BJ, Ambati J (2006) Corneal avascularity is due to soluble VEGF receptor-1. Nature 7114, 993 997.
3. Barrandon Y, Green H (1987) Three clonal types of keratinocyte with different capacities for multiplication. Proc. Natl. Acad. Sci. USA 84, 2302 2306.
4. Budak MT, Alpdogan OS, Zhou M, Lavker RM, Akinci MA, Wolosin JM (2005) Ocular surface epithelia contain ABCG2-dependent side population cells exhibiting features associated with stem cells. J. Cell Sci. 118, 1715 1724.
5. Buschke W (1949) Morphologic changes in cells of corneal epithelium in wound healing. Arch. Ophthalmol. 41, 306 316.
6. Challen GA, Little MH (2006) A side order of stem cells: the SP phenotype. Stem Cells 24, 3 12.
7. Chen W, Ishikawa M, Yamaki K, Sakuragi S (2003) Wistar rat palpebral conjunctiva contains more slow-cycling stem cells that have larger proliferative capacity: implication for conjunctival epithelial homeostasis. Jpn. J. Ophthalmol. 47, 119 128.
8. Chen Z, depaiva CS, Luo L, Ketzer FL, Pflugfelder SC, Li DQ (2004) Characterization of putative stem cell phenotype in human limbal epithelia. Stem Cells 22, 355 366.
9. Clatworthy JP, Subramanian V (2001) Stem cells and the regulation of proliferation, differentiation and patterning in the intestinal epithelium: emerging insights from gene expression patterns, transgenic and gene ablation studies. Mech. Dev. 101, 3 9.
10. Compton CC, Gill JM, Bradford DA, Regauer S, Gallico GG, O'Connor NE (1989) Skin regenerated from cultured epithelial autografts on full-thickness burn wounds from 6 days to 5 years after grafting. A light, electron microscopic and immunohistochemical study. Lab. Invest. 60, 600 612.
11. Cooper D, Sun TT (1986) Monoclonal antibody analysis of bovine epithelial keratins. Specific pairs as defined by coexpression. J. Biol. Chem. 261, 4646 4654.
12. Cotsarelis G, Cheng SZ, Dong G, Sun TT (1989) Existence of slow-cycling limbal epithelial basal cells that can be preferentially stimulated to proliferate: implications on epithelial stem cells. Cell 57, 201 209.
13. Cursiefen C, Chen L, Saint-Geniez M, Hamrah P, Jin Y, Rashid S, Pytowski B, Persaud K, Wu Y, Streilein JW, Dana R (2006) Nonvascular VEGF receptor 3 expression by corneal epithelium maintains avascularity and vision. Proc. Natl. Acad. Sci. USA 103, 11405 11410.
14. Daniels JT, Dart JK, Tuft SJ, Khaw PT (2001) Corneal stem cells in press. Wound Repair Regen 9, 483 494.
15. De Luca M, Albanese E, Bondanza S, Megna M, Ugozzoli L, Molina F, Cancedda R, Santi PL, Bormioli M, Stella M, Magliacani G (1989) Multicentre experience in the treatment of burns with autologous and allogenic cultured epithelium, fresh or preserved in a frozen state. Burns 15, 303 309.
16. De Saint Jean M, Baudouin C, Di Nolfo M, Roman S, Lozato P, Warnet JM, Brignole F (2004) Comparison of morphological and functional characteristics of primary-cultured human conjunctival epithelium and of Wong-Kilbourne derivative of Chang conjunctival cell line. Exp. Eye Res. 78, 257 274.
17. Dietlein TS, Jacobi PC, Paulsson M, Smyth N, Krieglstein G (1997) Vielfalt der laminin-isoformen in der limbusregion des auges. Klin. Monatsbl. Augenheilkd. 211, 188 191.
18. Di Iorio E, Barbaro V, Ruzza A, Ponzin D, Pellegrini G, De Luca M (2005) Isoforms of ΔNp63 and the migration of ocular limbal cells in human corneal regeneration. Proc. Natl. Acad. Sci. USA 102, 9523 9528.
19. Dogru M, Asano-Kato N, Tanaka M, Igarashi A, Shimmura S, Shimazaki J, Okada N, Takano Y, Fukagawa K, Tsubota K, Fujishima H (2005) Ocular surface and MUC5AC alterations in atopic patients with corneal shield ulcers. Curr. Eye Res. 30, 897 908.
20. Dravida S, Pal R, Khanna A, Tipnis SP, Ravindran G, Khan F (2005) The transdifferentiation potential of limbal fibroblast-like cells. Brain Res. Dev. Brain Res. 160, 239 251.
21. Dua HS, Shanmuganathan VA, Powell-Richards AO, Tighe PJ, Joseph A (2005) Limbal epithelial crypts: a novel anatomical structure and a putative limbal stem cell niche. Br. J. Ophthalmol. 89, 529 532.
22. Espana EM, Kawakita T, Romano A, di Pasquale M, Smiddy R, Liu C, Tseng SCG (2003) Stromal niche controls the plasticity of limbal and corneal epithelial differentiation in a rabbit model of recombined tissue. Invest. Ophtalmol. Vis Sci. 44, 5130 5135.
23. Fini ME, Stramer BM (2005) How the cornea heals: cornea-specific repair mechanisms affecting surgical outcomes. Cornea 24 (8 Suppl S2 S11.
24. Fuchs EV, Coppock SM, Green H, Cleveland DW (1981) Two distinct classes of keratin genes and their evolutionary significance. Cell 27, 75 84.
25. Fukuda K, Chikama T, Nakamura M, Nishida T (1999) Differential distribution of subchains of the basement membrane components type IV collagen and laminin among the amniotic membrane, cornea, and conjunctiva. Cornea 18, 73 79.
26. Gabison E, Chang JH, Hernandez-Quintela E, Javier J, Lu PC, Ye H, Kure T, Kato T, Azar DT (2004) Anti-angiogenic role of angiostatin during corneal wound healing. Exp. Eye Res. 78, 579 589.
27. Gerdes J, Lemke H, Baisch H, Wacker HH, Schwab U, Stein H (1984) Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J. Immunol. 133, 1710 1715.
28. Gipson IK (1989) The epithelial basement membrane zone of the limbus. Eye 3, 132 140.
29. Gomes JA, Romano A, Santos MS, Dua HS (2005) Amniotic membrane use in ophthalmology. Curr. Opin. Ophthalmol. 16, 233 240.
30. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC (1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J. Exp. Med. 183, 1797 1806.
31. Goodell MA, McKinney-Freeman S, Camargo FD (2005) Isolation and characterization of side population cells. Methods Mol. Biol. 290, 343 352.
32. Green H (1980) The keratinocyte as differentiated cell type. Harvey Lect. 74, 101 139.
33. Gritti A, Vescovi AL, Galli R (2002) Adult neural stem cells: plasticity and developmental potential. J. Physiol. (Paris) 96, 81 90.
34. Grove JE, Bruscia E, Krause DS (2004) Plasticity of bone marrow-derived stem cells. Stem Cells 22, 487 500.
35. Grueterich M, Espana EM, Touhami A, Ti SE, Tseng SC (2002) Phenotypic study of a case with successful transplantation of ex vivo expanded human limbal epithelium for unilateral total limbal stem cell deficiency. Ophthalmology 109, 1547 1552.
36. Grueterich M, Espana EM, Tseng SC (2003) Ex vivo expansion of limbal epithelial stem cells: amniotic membrane serving as a stem cell niche. Surv. Ophthalmol. 48, 631 646.
37. Hanto DW, Hopt UT, Hoffman R, Simmons RL (1982) Lymphocyte recruitment, regional blood flow, and vascular permeability at sites of allogeneic cellular interactions. J. Immunol. 129, 2437 2443.
38. Hatzfeld M, Franke WW (1985) Pair formation and promiscuity of cytokeratins: formation in vitro of heterotypic complexes and intermediate-sized filaments by homologous and heterologous recombinations of purified polypeptides. J. Cell Biol. 101, 1826 1841.
39. He YG, McCulley JP (1991) Growing human corneal epithelium on collagen shield and subsequent transfer to denuded cornea in vitro. Curr. Eye Res. 10, 851 863.
40. Holland EJ, Schwartz GS (1996) The evolution of epithelial transplantation for severe ocular surface disease and a proposed classification system. Cornea 15, 549 556.
41. Inatomi T, Nakamura T, Koizumi N, Sotozono C, Kinoshita S (2005) Current concepts and challenges in ocular surface reconstruction using cultivated mucosal epithelial transplantation. Cornea 24 (8 Suppl S32 S38.
42. Kawakita T, Espana EM, He H, Li W, Liu CY, Tseng SC (2005) Intrastromal invasion by limbal epithelial cells is mediated by epithelial-mesenchymal transition activated by air exposure. Am. J. Pathol. 167, 381 393.
43. Kinoshita S, Koizumi N, Nakamura T (2004) Transplantable cultivated mucosal epithelial sheet for ocular surface reconstruction. Exp. Eye Res. 78, 483 491.
44. Kivela T, Uusitalo M (1998) Structure, development and function of cytoskeletal elements in non-neuronal cells of the human eye. Prog. Retin. Eye Res. 17, 385 428.
45. Kolega J, Manabe M, Sun T-T (1989) Basement membrane heterogeneity and variation in corneal epithelial differentiation. Differentiation 42, 54 63.
46. Kruse FE, Tseng SC (1994) Retinoic acid regulates clonal growth and differentiation of cultured limbal and peripheral corneal epithelium. Invest. Ophthalmol. Vis. Sci. 35, 2405 2420.
47. Kruse FE, Volcker HE (1997) Stem cells, wound healing, growth factors, and angiogenesis in the cornea. Curr. Opin. Ophthalmol. 8, 46 54.
48. Kunimoto DY, Sharma S, Reddy MK, Gopinathan U, Jyothi J, Miller D, Rao GN (1998) Microbial keratitis in children. Ophthalmology 105, 252 257.
49. Kure T, Chang JH, Kato T, Hernandez-Quintela E, Ye H, Lu PC, Matrisian LM, Gatinel D, Shapiro S, Gosheh F, Azar DT (2003) Corneal neovascularization after excimer keratectomy wounds in matrilysin-deficient mice. Invest. Ophthalmol. Vis. Sci. 44, 137 144.
50. Lajtha LG (1979) Stem cell concepts. Differentiation 14, 23 34.
51. Lakshmipathy U, Verfaillie C (2005) Stem cell plasticity. Blood Rev. 19, 29 38.
52. Lavker RM, Tseng SC, Sun TT (2004) Corneal epithelial stem cells at the limbus: looking at some old problems from a new angle. Exp. Eye Res. 78, 433 446.
53. Le Blank K, Ringden O (2006) Mesenchymal stem cells: properties and role in clinical bone marrow transplantation. Curr. Opin. Immunol. 18, 586 591.
54. Leighton J (1992) Structural biology of epithelial tissue in histophysiologic gradient culture. In Vitro Cell. Dev. Biol. 28A, 482 492.
55. Li DQ, Tseng SCG (1995) Three pattern of cytokine expression potentially involved in epithelial fibroblast interactions of human ocular surface. J. Cell. Physiol. 163, 61 79.
56. Limb GA, Daniels JT, Cambrey AD, Secker GA, Shortt AJ, Lawrence JM, Khaw P (2006) Current prospects for adult stem cell-based therapies in ocular repair and regeneration. Curr. Eye Res. 31, 381 390.
57. Liu L, Sheardown H (2005) Glucose permeable poly (dimethyl siloxane) poly (N-isopropyl acrylamide) interpenetrating networks as ophthalmic biomaterials. Biomaterials 26, 233 244.
58. Ljubimov AV, Burgeson RE, Butkowsky RJ, Michael AF, Sun T (1995) Human corneal basement membrane heterogeneity: topographical differences in the expression of type 4 collagen and laminin isoforms. Lab. Invest. 72, 461 472.
59. Mann I (1944) Study of epithelial regeneration in living eye. Br. J. Ophthalmol. 28, 26 40.
60. Margolis L, Hatfill S, Chuaqui R, Vocke C, Emmert-Buck M, Linehan WM, Duray PH (1999) Long term organ culture of human prostate tissue in a NASA-designed rotating wall bioreactor. J. Urol. 161, 290 297.
61. Matouskova E, Bucek S, Vogtova D, Vesely P, Chaloupkova A, Broz L, Singernova H, Pavlikova Konigova R (1997) Treatment of burns and donor sites with human allogeneic keratinocytes grown on acellular pig dermis. Br. J. Dermatol. 136, 901 907.
62. Maumenee A, Scholz R (1948) Histopathology of the ocular lesion produced by sulphur and nitrogen mustards. Bull. Johns Hopkins Hosp 82, 121 147.
63. McAteer JA, Davis JM (2002) Basic cell culture technique and the maintenance of cell lines. In: Davis JM, ed. Basic Cell Culture - A Practical Approach, 2nd edn, pp. 93 148. London: Oxford University Press.
64. Meller D, Dabul V, Tseng SC (2002) Expansion of conjunctival epithelial progenitor cells on amniotic membrane. Exp. Eye Res. 74, 537 545.
65. Michelini M, Rosellini A, Simoncini T, Papini S, Revoltella RP (2004) A three-dimensional organotypic culture of the human uterine exocervix for studying mucosal epithelial differentiation and migrating leukocytes. Differentiation 72, 138 149.
66. Michelini M, Rosellini A, Mandys V, Simoncini T, Revoltella RP (2005) Cytoarchitecture modifications of the human uterine endocervical mucosa in long-term three-dimensional organotypic culture. Pathol. Res. Pract. 201, 679 689.
67. Miller SJ, Lavker RM, Sun TT (1997) Keratinocyte stem cells of cornea, skin, and hair follicle. In: Potten C, ed. Stem Cells, p. 331 362. New York: Academic Press.
68. Moll R, Franke WW, Schiller DL, Geiger B, Krepler R (1982) The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells. Cell 31, 11 24.
69. Moore JE, McMullen CB, Mahon G, Adamis AP (2002) The corneal epithelial stem cell. DNA Cell Biol. 21, 443 451.
70. van Muijen GN, Ruiter DJ, Franke WW, Achtstatter T, Haasnoot WH, Ponec M, Warnaar SO (1986) Cell type heterogeneity of cytokeratin expression in complex epithelia and carcinomas as demonstrated by monoclonal antibodies specific for cytokeratins nos. 4 and 13. Exp. Cell Res. 162, 97 113.
71. Nakamura T, Inatomi T, Sotozono C, Amemiya T, Kanamura N, Kinoshita S (2004) Transplantation of cultivated autologous oral mucosal epithelial cells in patients with severe ocular surface disorders. Br. J. Ophthalmol. 88, 1280 1284.
72. Nielsen K, Birkenkamp-Demtroder K, Ehlers N, Orntoft TF (2003) Identification of differentially expressed genes in keratoconus epithelium analyzed on microarrays. Invest. Ophthalmol. Vis. Sci. 44, 2466 2476.
73. O'Guin WM, Galvin S, Schermer A, Sun TT (1987) Patterns of keratin expression define distinct pathways of epithelial development and differentiation. Curr. Top. Dev. Biol. 22, 97 125.
74. Pajoohesh-Ganji A, Stepp MA (2005) In search of markers for the stem cells of the corneal epithelium. Biol. Cell 97, 265 276.
75. Paladino G, Marino C, La Terra Mule S, Civiale C, Rusciano D, Enea V (2004) Cytokeratin expression in primary epithelial cell culture from bovine conjunctiva. Tissue Cell 36, 323 332.
76. Papini S, Cecchetti D, Campani D, Fitzgerald W, Grivel JC, Chen S, Margolis L, Revoltella RP (2003) Isolation and clonal analysis of human epidermal keratinocyte stem cells in long-term culture. Stem Cells 21, 481 494.
77. Papini S, Rosellini A, Campani D, Dematteis A, Selli C, Revoltella RP (2004) Selective growth of epithelial basal cells from human prostate in a three-dimensional organ culture. Prostate 59, 383 392.
78. Papini S, Rosellini A, Nardi M, Giannarini C, Revoltella RP (2005) Selective growth and expansion of human corneal epithelial basal stem cells in a three-dimensional-organ culture. Differentiation 73, 61 68.
79. Pellegrini G, Dellambra E, Golisano O, Martinelli E, Fantozzi I, Bondanza S, Ponzin D, McKeon F, De Luca M (2001) p63 identifies keratinocyte stem cells. Proc. Natl. Acad. Sci. USA 98, 3156 3161.
80. Pellegrini G, Traverso CE, Franzi AT, Zingirian M, Cancedda R, De Luca M (1997) Long-term restoration of damaged corneal surfaces with autologous cultivated corneal epithelium. Lancet 349, 990 993.
81. Pellegrini G, Golisano O, Paterna P, Lambiase A, Bonini S, Rama P, De Luca M (1999) Location and clonal analysis of stem cells and their differentiated progeny in the human ocular surface. J. Cell. Biol. 145, 769 782.
82. Potten CS, Morris RJ (1988) Epithelial stem cells in vivo. J. Cell Sci. 10 (Suppl 45 62.
83. Rama P, Bonini S, Lambiase A, Golisano O, Paterna P, De Luca M, Pellegrini G (2001) Autologous fibrin-cultured limbal stem cells permanently restore the corneal surface of patients with total limbal stem cell deficiency. Transplantation 72, 1478 1485.
84. Ramaesh K, Dhillon B (2003) Ex vivo expansion of corneal limbal epithelial/stem cells for corneal surface reconstruction. Eur. J. Ophthalmol. 13, 515 524.
85. Rosellini A, Papini S, Giannarini C, Nardi M, Revoltella RP (2007) Three-dimensional organotypic culture to investigate human conjunctival epithelial precursor cells and their progeny within their natural microenvironment. Int. J. Dev. Biol. forthcoming.
86. Santos MS, Gomes JA, Hofling-Lima AL, Rizzo LV, Romano AC, Belfort R Jr. (2005) Survival analysis of conjunctival limbal grafts and amniotic membrane transplantation in eyes with total limbal stem cell deficiency. Am. J. Ophthalmol. 140, 223 230.
87. Schlötzer-Schrehardt U, Kruse FE (2005) Identification and characterization of limbal stem cells. Exp. Eye Res. 81, 247 264.
88. Schmidt NJ (1988) Cell culture procedures for diagnostic virology. In: Schmidt NJ, Emmons RW, eds. Diagnostic Procedures for Viral, Rickettsial and Chlamydial Infections, 6th edn, pp. 51 100. Washington, DC: American Public Health Association Inc.
89. Schwab IR, Reyes M, Isseroff RR (2000) Successful transplantation of bioengineered tissue replacements in patients with ocular surface disease. Cornea 19, 421 426.
90. Shanmuganathan VA, Foster T, Kulkarni BB, Hopkinson A, Gray T, Powe DG, Lowe J, Dua HS (2006) Morphological characteristics of the limbal epithelial crypt. Br. J. Ophthalmol. 91, 514 519.
91. Signoretti S, Waltregny D, Dilks J, Isaac B, Lin D, Garraway L, Yang A, Montironi R, McKeon F, Loda M (2000) p63 is a prostate basal cell marker and is required for prostate development. Am. J. Pathol. 157, 1769 1775.
92. Song E, Yang W, Cui ZH, Dong Y, Sui DM, Guan XK, Ma YL (2005) Transplantation of human limbal cells cultivated on amniotic membrane for reconstruction of rat corneal epithelium after alkaline burn. Chin. Med. J. (Engl.) 118, 927 935.
93. Sosnova M, Bradl M, Forrester JV (2005) CD 34+ corneal stromal cells are bone-marrow derived and express hemopoietic stem cell markers. Stem Cells 23, 507 515.
94. Stark HJ, Willhauck MJ, Mirancea N, Boehnke K, Nord I, Breitkreutz D, Pavesio A, Boukamp P, Fusenig NE (2004) Authentic fibroblast matrix in dermal equivalents normalises epidermal histogenesis and dermoepidermal junction in organotypic co-culture. Eur. J. Cell Biol. 83, 631 645.
95. Suda T, Arai F, Shimmura S (2005) Regulation of stem cells in the niche. Cornea 24 (8 Suppl S12 S17.
96. Sudha B, Madhavan HN, Sitalakshmi G, Malathi J, Krishnakumar S, Mori Y, Yoshioka H, Abraham S (2006) Cultivation of human corneal limbal stem cells in Mebiol gel (R) - A thermo-reversible gelation polymer. Indian J. Med. Res. 124, 655 664.
97. Sun TT, Lavker RM (2004) Corneal epithelial stem cells: past, present, and future. J. Investig. Dermatol. Symp. Proc. 9, 202 207.
98. Tanifuji-Terai N, Terai K, Hayashi Y, Chikama T, Kao WW (2006) Expression of keratin 12 and maturation of corneal epithelium during development and postnatal growth. Invest. Ophthalmol. Vis. Sci. 47, 545 551.
99. Tsubota K, Satake Y, Kaido M, Shinozaki N, Shimmura S, Bissen-Miyajima H, Shimazaki J (1999) Treatment of severe ocular-surface disorders with corneal epithelial stem-cell transplantation. N. Engl. J. Med. 340, 1697 1703.
100. Tuori A, Uusitalo H, Burgeson RE, Terttunen J, Virtanen I (1996) The immunohistochemical composition of the human corneal basement membrane. Cornea 15, 286 294.
101. Vascotto SG, Griffith M (2006) Localization of candidate stem and progenitor cell markers within the human cornea, limbus and bulbar conjunctiva in vivo and in cell culture. Anat. Rec. Part A Discov. Mol. Cell. Evol. Biol. 288, 921 931.
102. Watanabe K, Nishida K, Yamato M, Umemoto T, Sumide T, Yamamoto K, Maeda N, Watanabe H, Okano T, Tano Y (2004) Human limbal epithelium contains side population cells expressing the ATP-binding cassette transporter ABCG2. FEBS Lett. 565, 6 10.
103. Watt FM (1989) Terminal differentiation of epidermal keratinocytes. Curr. Opin. Cell Biol. 1, 1107 1115.
104. Wei ZG, Cotsarelis G, Sun TT, Lavker RM (1995) Label-retaining cells are preferentially located in fornical epithelium: implication on conjunctival epithelial homeostasis. Invest. Ophthalmol. Vis. Sci. 36, 236 246.
105. Wirtschafter JD, Ketcham JM, Weinstock RJ, Tabesh T, Mcloon LK (1999) Mucocutaneous junction as the major source of replacement palpebral conjunctival epithelial cells. Invest. Ophthalmol. Vis. Sci. 40, 3138 3146.
106. Wolosin JM, Wang Y (1995) Alpha-2,3 sialylation differentiate the limbal and corneal epithelial cell phenotypes. Invest. Ophthalmol. Vis. Sci. 36, 2277 2286.
107. Wolosin JM, Xiong X, Schutte M, Stegman Z, Tieng A (2000) Stem cells and differentiation stages in the limbo-corneal epithelium. Prog. Retin. Eye Res. 19, 223 255.
108. Wolosin JM, Budak MT, Akinci MA (2004) Ocular surface epithelial and stem cell development. Int. J. Dev. Biol. 48, 981 991.
109. Yoshioka H, Cushman JA, Mori Y (1994a) Synthetic hydrogel with thermoreversible gelation 3: an NMR study of the Sol-Gel transition. Polym. Adv. Tech. 5, 122 126.
110. Yoshioka H, Mikami M, Mori Y, Tsuchida E (1994b) A synthetic hydrogel with thermoreversible gelation 1: preparation and rheological properties. J. Macromol. Sci. A31, 113 121.
111. Yoshioka H, Mori Y, Shimizu M (2003) Separation and recovery of DNA fragments by electrophoresis through a thermoreversible hydrogel composed of poly (ethylene oxide) and poly (propylene oxide). Anal. Biochem. 323, 218 222.
112. Yoshizawa M, Feinberg SE, Marcelo CL, Elner VM (2004) Ex vivo produced human conjunctiva and oral mucosa equivalents grown in a serum-free culture system. J. Oral Maxillofac. Surg. 62, 980 988.
113. Zhang XZ, Yang YY, Chung TS (2002) The influence of cold treatment on properties of temperature-sensitive poly (N-isopropylacrylamide) hydrogels. J. Colloid Interface Sci. 246, 105 111.
114. Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J, Morris JJ, Lagutina I, Grosveld GC, Osawa M, Nakauchi H, Sorrentino BP (2001) The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat. Med. 7, 1028 1034.
115. Zieske JD, Wasson M (1993) Regional variation in distribution of EGF receptor in developing and adult corneal epithelium. J. Cell Sci. 106, 145 152.
116. Zieske JD, Bukusoglu G, Yankauckas MA (1992) Characterization of a potential marker of corneal epithelial stem cells. Invest. Ophthalmol. Vis. Sci. 33, 143 152.
117. Zieske JD, Takahashi H, Hutcheon AE, Dalbone AC (2000) Activation of epidermal growth factor receptor during corneal epithelial migration. Invest. Ophthalmol. Vis. Sci. 41, 1346 1355.