Serial analysis of gene expression (SAGE) in the rat limbal and central corneal epithelium

Investigative Ophthalmology and Visual Science

Volumn 47, Issue 9, 2006, Pages 3801-3810

  Adachi, Wakako ^a   Ulanovsky, Hagit ^a,b   Li, Yan ^a   Norman, Barbara ^a   Davis, Janine ^a   Piatigorsky, Joram ^a  

^a NATIONAL EYE INSTITUTE   (United States)

^b UNIVERSITY OF HAIFA   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKERATIN; CYTOKERATIN K15; CYTOKERATIN K4; DISULFIDE; GENE PRODUCT; MARAPSIN; MEMBRANE SPANNING FOUR DOMAIN SUBFAMILY A 8B PROTEIN; MESOTHELIN; PROTEINASE; SERINE PROTEINASE; UNCLASSIFIED DRUG; WDNM1 LIKE PROTEIN; EYE PROTEIN;

ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CONJUNCTIVA EPITHELIUM; CORNEA EPITHELIUM; CORNEA LIMBUS; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; IN SITU HYBRIDIZATION; MALE; METABOLISM; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SERIAL ANALYSIS OF GENE EXPRESSION; WISTAR RAT; ANIMAL; CYTOLOGY; GENE EXPRESSION; GENETIC MARKER; GENETICS; METHODOLOGY; STEM CELL;

ANIMALS; EPITHELIUM, CORNEAL; EYE PROTEINS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC MARKERS; IN SITU HYBRIDIZATION; LIMBUS CORNEAE; MALE; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STEM CELLS;

EID: 33749120517     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: 10.1167/iovs.06-0216     Document Type: Article

References (98)

1. Hay ED. Development of the vertebrate cornea. Int Rev Cytol. 1979;63:263-322.
2. Hanna C, O'Brien JE. Cell production and migration in the epithelial layer of the cornea. Arch Ophthalmol. 1960;64:536-539.
3. Lemp MA, Mathers WD. Corneal epithelial cell movement in humans. Eye. 1989;3:438-445.
4. Beebe DC, Masters BR. Cell lineage and the differentiation of corneal epithelial cells. Invest Ophthalmol Vis Sci. 1996;37:1815-1825.
5. Norman B, Davis J, Piatigorsky J. Postnatal gene expression in the normal mouse cornea by SAGE. Invest Ophthalmol Vis Sci. 2004;45:429-440.
6. Birger Y, Davis J, Furusawa T, Rand E, Piatigorsky J, Bustin M. A role for chromosomal protein HMGN1 in corneal maturation. Differentiation. 2006;74;19-29.
7. Schermer A, Galvin S, Sun TT. Differentiation-related expression of a major 64K corneal keratin in vivo and in culture suggests limbal location of corneal epithelial stem cells. J Cell Biol. 1986;103:49-62.
8. Cotsarelis G, Cheng SZ, Dong G, Sun TT, Lavker RM. Existence of slow-cycling limbal epithelial basal cells that can be preferentially stimulated to proliferate: implications on epithelial stem cells. Cell. 1989;57:201-209.
9. Lavker RM, Dong G, Cheng SZ, Kudoh K, Cotsarelis G, Sun TT. Relative proliferative rates of limbal and corneal epithelia; implications of corneal epithelial migration, circadian rhythm, and suprabasally located DNA-synthesizing keratinocytes. Invest Ophthalmol Vis Sci. 1991;32:1864-1875.
10. Wolosin JM, Xiong X, Schutte M, Stegman Z, Tieng A. Stem cells and differentiation stages in the limbo-corneal epithelium. Prog Retin Eye Res., 2000;19:223-255.
11. Lavker RM, Sun TT. Epidermal stem cells: properties, markers, and location. Proc Natl Acad Sci USA. 2000;97:13473-13475.
12. Wolosin JM, Budak MT, Akinci MA. Ocular surface epithelial and stem cell development. Int J Dev Biol. 2004;48:981-991.
13. Lavker RM, Sun TT. Epithelial stem cells: the eye provides a vision. Eye. 2003;17:937-942.
14. Lavker RM, Tseng SC, Sun TT. Corneal epithelial stem cells at the limbus: looking at some old problems from a new angle. Exp Eye Res. 2004;78:433-446.
15. Collinson JM, Morris L, Reid AI, et al. Clonal analysis of patterns of growth, stem cell activity, and cell movement during the development and maintenance of the murine corneal epithelium. Dev Dyn. 2002;224:432-440.
16. Nagasaki T, Zhao J. Centripetal movement of corneal epithelial cells in the normal adult mouse. Invest Ophthalmol Vis Sci. 2003;44:558-566.
17. Kenyon KR, Tseng SC. Limbal autograft transplantation for ocular surface disorders. Ophthalmology. 1989;96:709-722; discussion 722-723.
18. Tseng SC. Concept and application of limbal stem cells. Eye. 1989;3:141-157.
19. Pellegrini G, Traverso CE, Franzi AT, Zingirian M, Cancedda R, De Luca M. Long-term restoration of damaged corneal surfaces with autologous cultivated corneal epithelium. Lancet. 1997;349:990-993.
20. Rama P, Bonini S, Lambiase A, et al. Autologous fibrin-cultured limbal stem cells permanently restore the corneal surface of patients with total limbal stem cell deficiency. Transplantation. 2001;72:1478-1485.
21. Espana EM, Di Pascuale M, Grueterich M, Solomon A, Tseng SC. Keratolimbal allograft in corneal reconstruction. Eye. 2004;18:406-417.
22. De Luca M, Pellegrini G. The importance of epidermal stem cells in keratinocyte-mediated gene therapy. Gene Ther. 1997;4:381-383.
23. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105-111.
24. Miller SJ, Lavker RM, Sun TT. Interpreting epithelial cancer biology in the context of stem cells: tumor properties and therapeutic implications. Biochim Biophys Acta. 2005;1756:25-52.
25. Waring III GO, Roth AM, Ekins MB. Clinical and pathologic description of 17 cases of corneal intraepithelial neoplasia. Am J Ophthalmol. 1984;97:547-559.
26. Lehrer MS, Sun TT, Lavker RM. Strategies of epithelial repair: modulation of stem cell and transit amplifying cell proliferation. J Cell Sci. 1998;111:2867-2875.
27. Wu RL, Zhu G, Galvin S, et al. Lineage-specific and differentiation- dependent expression of K12 keratin in rabbit corneal/limbal epithelial cells: cDNA cloning and northern blot analysis. Differentiation. 1994;55:137-144.
28. Chen WY, Mui MM, Kao WW, Liu CY, Tseng SC. Conjunctival epithelial cells do not transdifferentiate in organotypic cultures: expression of K12 keratin is restricted to corneal epithelium. Curr Eye Res. 1994;13:765-778.
29. Kays WT, Piatigorsky J. Aldehyde dehydrogenase class 3 expression: identification of a cornea-preferred gene promoter in transgenic mice. Proc Natl Acad Sci USA. 1997;94:13594-13599.
30. Matic M, Petrov IN, Chen S, Wang C, Dimitrijevich SD, Wolosin JM. Stem cells of the corneal epithelium lack connexins and metabolite transfer capacity. Differentiation. 1997;61:251-260.
31. Espana EM, Kawakita T, Romano A, et al. Stromal niche controls the plasticity of limbal and corneal epithelial differentiation in a rabbit model of recombined tissue. Invest Ophthalmol Vis Sci. 2003;44:5130-5135.
32. Sun L, Sun TT, Lavker RM. CLED: a calcium-linked protein associated with early epithelial differentiation. Exp Cell Res. 2000;259:96-106.
33. Sun L, Ryan DG, Zhou M, Sun TT, Lavker RM. EEDA: A protein associated with an early stage of stratified epithelial differentiation. J Cell Physiol. 2006;206:103-111.
34. Chen Z, de Paiva CS, Luo L, Kretzer FL, Pflugfelder SC, Li DQ. Characterization of putative stem cell phenotype in human limbal epithelia. Stem Cells. 2004;22:355-366.
35. Zhou S, Schuetz JD, Bunting KD, et al. 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. 2001;7:1028-1034.
36. Budak MT, Alpdogan OS, Zhou M, Lavker RM, Akinci MA, Wolosin JM. Ocular surface epithelia contain ABCG2-dependent side population cells exhibiting features associated with stem cells. J Cell Sci. 2005;118:1715-1724.
37. de Paiva CS, Chen Z, Corrales RM, Pflugfelder SC, Li DQ. ABCG2 transporter identifies a population of clonogenic human limbal epithelial cells. Stem Cells. 2005;23:63-73.
38. Kim HS, Jun Song X, 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.
39. 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.
40. Li DQ, Chen Z, Song XJ, de Paiva CS, Kim HS, Pflugfelder SC. Partial enrichment of a population of human limbal epithelial cells with putative stem cell properties based on collagen type IV adhesiveness. Exp Eye Res. 2005;80:581-590.
41. Chung EH, Bukusoglu G, Zieske JD. Localization of corneal epithelial stem cells in the developing rat. Invest Ophthalmol Vis Sci. 1992;33:2199-2206.
42. Pellegrini G, Dellambra E, Golisano O, et al. p63 identifies keratinocyte stem cells. Proc Natl Acad Sci USA. 2001;98:3156-3161.
43. Di Iorio E, Barbaro V, Ruzza A, Ponzin D, Pellegrini G, De Luca M. Isoforms of DeltaNp63 and the migration of ocular limbal cells in human corneal regeneration. Proc Natl Acad Sci USA. 2005;102:9523-9528.
44. Moore JE, McMullen CB, Mahon G, Adamis AP. The corneal epithelial stem cell. DNA Cell Biol. 2002;21:443-451.
45. Dua HS, Joseph A, Shanmuganathan VA, Jones RE. Stem cell differentiation and the effects of deficiency. Eye. 2003;17:877-885.
46. Hsueh YJ, Wang DY, Cheng CC, Chen JK. Age-related expressions of p63 and other keratinocyte stem cell markers in rat cornea. J Biomed Sci. 2004;11:641-651.
47. Kawasaki S, Tanioka H, Yamasaki K, Connon CJ, Kinoshita S. Expression and tissue distribution of p63 isoforms in human ocular surface epithelia. Exp Eye Res. 2006;82:293-299.
48. Velculescu VE, Zhang L, Vogelstein B, Kinzler KW. Serial analysis of gene expression. Science. 1995;270:484-487.
49. Siddiqui AS, Khattra J, Delaney AD, et al. A mouse atlas of gene expression: large-scale digital gene-expression profiles from precisely defined developing C57BL/6J mouse tissues and cells. Proc Natl Acad Sci USA. 2005;102:18485-18490.
50. Liu CY, Zhu G, Westerhausen-Larson A, et al. Cornea-specific expression of K12 keratin during mouse development. Curr Eye Res. 1993;12:963-974.
51. Liu JJ, Kao WW, Wilson SE. Corneal epithelium-specific mouse keratin K12 promoter. Exp Eye Res. 1999;68:295-301.
52. Boehlke CS, Yuan C, Kao WW, Huang AJ. Cytokeratin 12 in human ocular surface epithelia is the antigen reactive with a commercial anti-Galpha q antibody. Mol Vis. 2004;10:867-873.
53. Cooper DL, Baptist EW, Enghild JJ, Isola NR, Klintworth GK. Bovine corneal protein 54K (BCP54) is a homologue of the tumor-associated (class 3) rat aldehyde dehydrogenase (RATALD). Gene. 1991;98:201-207.
54. Abedinia M, Pain T, Algar EM, Holmes RS. Bovine corneal aldehyde dehydrogenase: the major soluble corneal protein with a possible dual protective role for the eye. Exp Eye Res. 1990;51:419-426.
55. Nees DW, Wawrousek EF, Robison WG Jr, Piatigorsky J. Structurally normal corneas in aldehyde dehydrogenase 3a1-deficient mice. Mol Cell Biol. 2002;22:849-855.
56. Sax CM, Salamon C, Kays WT, et al. Transketolase is a major protein in the mouse cornea. J Biol Chem. 1996;271:33568-33574.
57. Okazaki Y, Furuno M, Kasukawa T, et al. Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature 2002;420:563-573.
58. Hulo N, Bairoch A, Bulliard V, et al. The PROSITE database. Nucleic Acids Res. 2006;34:D227-D230.
59. Dear TN, Kefford RF. The WDNM1 gene product is a novel member of the 'four-disulphide core' family of proteins. Biochem Biophys Res Commun. 1991;176:247-254.
60. Kaplan N, Sasson O, Inbar U, et al. ProtoNet 4.0: a hierarchical classification of one million protein sequences. Nucleic Acids Res. 2005;33:D216-D218.
61. Nakai K, Horton P. PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci. 1999;24:34-36.
62. Morrison BW, Leder P. neu and ras initiate murine mammary tumors that share genetic markers generally absent in c-myc and int-2-initiated tumors. Oncogene. 1994;9:34l7-3426.
63. Tanifuji-Terai N, Terai K, Hayashi Y, Chikama T, Kao WW. Expression of keratin 12 and maturation of corneal epithelium during development and postnatal growth. Invest Ophthalmol Vis Sci. 2006;47:545-551.
64. Yew DT, Sha O, Li WW, Lam TT, Lorke DE. Proliferation and apoptosis in the epithelium of the developing human cornea and conjunctiva. Life Sci. 2001;68:2987-3003.
65. Tseng H, Matsuzaki K, Lavker RM. Basonuclin in murine corneal and lens epithelia correlates with cellular maturation and proliferative ability. Differentiation. 1999;65:221-227.
66. Westfall MD, Pietenpol JA. p63: Molecular complexity in development and cancer. Carcinogenesis. 2004;25:857-864.
67. Dai X, Segre JA. Transcriptional control of epidermal specification and differentiation. Curr Opin Genet Dev. 2004;14:485-491.
68. Koster MI, Kim S, Mills AA, DeMayo FJ, Roop DR. p63 is the molecular switch for initiation of an epithelial stratification program. Genes Dev. 2004;18:126-131.
69. Koster MI, Kim S, Roop DR. P63 deficiency: a failure of lineage commitment or stem cell maintenance? J Investig Dermatol Symp Proc. 2005;10:118-123.
70. Kurpakus MA, Stock EL, Jones JC. Expression of the 55-kD/64-kD corneal keratins in ocular surface epithelium. Invest Ophthalmol Vis Sci. 1990;31:448-456.
71. Sun TT, Lavker RM. Corneal epithelial stem cells: past, present, and future. J Investig Dermatol Symp Proc. 2004;9:202-207.
72. Kawasaki S, Tanioka H, Yamasaki K, Yokoi N, Komuro A, Kinoshita S. Clusters of corneal epithelial cells reside ectopically in human conjunctival epithelium. Invest Ophthalmol Vis Sci. 2006;47:1359-1367.
73. Vantrappen L, Geboes K, Missotten L, Maudgal PC, Desmet V. Lymphocytes and Langerhans cells in the normal human cornea. Invest Ophthalmol Vis Sci. 1985;26:220-225.
74. Yamagami S, Usui T, Amano S, Ebihara N. Bone marrow-derived cells in mouse and human cornea. Cornea. 2005;24:S71-S74.
75. Yamagami S, Yokoo S, Usui T, Yamagami H, Amano S, Ebihara N. Distinct populations of dendritic cells in the normal human donor corneal epithelium. Invest Ophthalmol Vis Sci. 2005;46:4489-4494.
76. Lyle S, Christofidou-Solomidou M, Liu Y, Elder DE, Albelda S, Cotsarelis G. The C8/144B monoclonal antibody recognizes cytokeratin 15 and defines the location of human hair follicle stem cells. J Cell Sci. 1998;111:3179-3188.
77. Lyle S, Christofidou-Solomidou M, Liu Y, Elder DE, Albelda S, Cotsarelis G. Human hair follicle bulge cells are biochemically distinct and possess an epithelial stem cell phenotype. J Investig Dermatol Symp Proc. 1999;4:296-301.
78. Liu Y, Lyle S, Yang Z, Cotsarelis G. Keratin 15 promoter targets putative epithelial stem cells in the hair follicle bulge. J Invest Dermatol. 2003;121:963-968.
79. Aldaz CM, Hu Y, Daniel R, Gaddis S, Kittrell F, Medina D. Serial analysis of gene expression in normal p53 null mammary epithelium. Oncogene. 2002;21:6366-6376.
80. Robinson GW, McKnight RA, Smith GH, Hennighausen L. Mammary epithelial cells undergo secretory differentiation in cycling virgins but require pregnancy for the establishment of terminal differentiation. Development. 1995;121:2079-2090.
81. Howe LR, Watanabe O, Leonard J, Brown AM. Twist is up-regulated in response to Wnt1 and inhibits mouse mammary cell differentiation. Cancer Res. 2003;63:1906-1913.
82. Dear TN, Ramshaw IA, Kefford RF. Differential expression of a novel gene, WDNM1, in nonmetastatic rat mammary adenocarcinoma cells. Cancer Res. 1988;48:5203-5209.
83. Kluger HM, Kluger Y, Gilmore-Hebert M, et al. cDNA microarray analysis of invasive and tumorigenic phenotypes in a breast cancer model. Lab Invest. 2004;84:320-331.
84. Chang K, Pastan I. Molecular cloning of mesothelin, a differentiation antigen present on mesothelium, mesotheliomas, and ovarian cancers. Proc Natl Acad Sci USA. 1996;93:136-140.
85. Hassan R, Laszik ZG, Lerner M, Raffeld M, Postier R, Brackett D. Mesothelin is overexpressed in pancreaticobiliary adenocarcinomas but not in normal pancreas and chronic pancreatitis. Am J Clin Pathol. 2005;124:838-845.
86. Hassan R, Remaley AT, Sampson ML, et al. Detection and quantitation of serum mesothelin, a tumor marker for patients with mesothelioma and ovarian cancer. Clin Cancer Res. 2006;12:447-453.
87. Vang R, Gown AM, Barry TS, Wheeler DT, Ronnett BM. Ovarian atypical proliferative (borderline) mucinous tumors: gastrointestinal and seromucinous (endocervical-like) types are immunophenotypically distinctive. Int J Gynecol Pathol. 2006;25:83-89.
88. Wong GW, Yasuda S, Madhusudhan MS, et al. Human tryptase epsilon (PRSS22), a new member of the chromosome 16p13.3 family of human serine proteases expressed in airway epithelial cells. J Biol Chem. 2001;276:49169-49182.
89. Hooper JD, Nicol DL, Dickinson JL, et al. Testisin, a new human serine proteinase expressed by premeiotic testicular germ cells and lost in testicular germ cell tumors. Cancer Res. 1999;59:3199-3205.
90. Benaud CM, Oberst M, Dickson RB, Lin CY. Deregulated activation of matriptase in breast cancer cells. Clin Exp Metastasis. 2002;19:639-649.
91. Hollenberg MD, Houle S. Proteinases as hormone-like signal messengers. Swiss Med Wkly. 2005;135:425-432.
92. Comoglio PM, Trusolino L. Cancer: the matrix is now in control. Nat Med. 2005;11:1156-1159.
93. Sivak JM, Fini ME. MMPs in the eye: emerging roles for matrix metalloproteinases in ocular physiology. Prog Retin Eye Res. 2002;21:1-14.
94. Wilson SE, Netto M, Ambrosio R Jr. Corneal cells: chatty in development, homeostasis, wound healing, and disease. Am J Ophthalmol. 2003;136:530-536.
95. Nagase H, Visse R, Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res. 2006;69;562-573.
96. Lee SL, Dickson RB, Lin CY. Activation of hepatocyte growth factor and urokinase/plasminogen activator by matriptase, an epithelial membrane serine protease. J Biol Chem. 2000;275:36720-36725.
97. Lee MS, Kiyomiya K, Benaud C, Dickson RB, Lin CY. Simultaneous activation and hepatocyte growth factor activator inhibitor 1-mediated inhibition of matriptase induced at activation foci in human mammary epithelial cells. Am J Physiol. 2005;288:C932-C94l.
98. Sueoka K, Nawata S, Nakagawa T, et al. Tumor-associated serpin, squamous cell carcinoma antigen stimulates matrix metalloproteinase-9 production in cervical squamous cell carcinoma cell lines. Int J Oncol. 2005;27:1345-1353.