OVOL2 Maintains the Transcriptional Program of Human Corneal Epithelium by Suppressing Epithelial-to-Mesenchymal Transition

Cell Reports

Volumn 15, Issue 6, 2016, Pages 1359-1368

  Kitazawa, Koji ^a,b,f   Hikichi, Takafusa ^a   Nakamura, Takahiro ^b   Mitsunaga, Kanae ^a   Tanaka, Azusa ^a   Nakamura, Masahiro ^a   Yamakawa, Tatsuya ^a   Furukawa, Shiori ^a   Takasaka, Mieko ^c   Goshima, Naoki ^d   Watanabe, Akira ^a   Okita, Keisuke ^a   Kawasaki, Satoshi ^b,e   Ueno, Morio ^b   Kinoshita, Shigeru ^b   Masui, Shinji ^a,f  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^c Japan Biological Informatics Consortium   (Japan)

^d NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^e OSAKA UNIVERSITY   (Japan)

^f JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN OVOL2; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; OVOL2 PROTEIN, HUMAN;

ARTICLE; CELL LINEAGE; CONTROLLED STUDY; CORNEA EPITHELIUM; ECTODERM; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; FIBROBLAST; GENE ACTIVATION; GENE REPRESSION; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; HUMAN TISSUE; INDUCED PLURIPOTENT STEM CELL; NEURAL STEM CELL; NEUROECTODERM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MESODERM; METABOLISM;

EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; EPITHELIUM, CORNEAL; FIBROBLASTS; GENE EXPRESSION REGULATION; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MESODERM; NEURAL STEM CELLS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84964689431     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.04.020     Document Type: Article

References (33)

1. Buenrostro J.D., Giresi P.G., Zaba L.C., Chang H.Y., Greenleaf W.J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 2013, 10:1213-1218.
2. Chng Z., Teo A., Pedersen R.A., Vallier L. SIP1 mediates cell-fate decisions between neuroectoderm and mesendoderm in human pluripotent stem cells. Cell Stem Cell 2010, 6:59-70.
3. Conti L., Pollard S.M., Gorba T., Reitano E., Toselli M., Biella G., Sun Y., Sanzone S., Ying Q.L., Cattaneo E., Smith A. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol. 2005, 3:e283.
4. De Craene B., Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nat. Rev. Cancer 2013, 13:97-110.
5. Di Micco R., Fontanals-Cirera B., Low V., Ntziachristos P., Yuen S.K., Lovell C.D., Dolgalev I., Yonekubo Y., Zhang G., Rusinova E., et al. Control of embryonic stem cell identity by BRD4-dependent transcriptional elongation of super-enhancer-associated pluripotency genes. Cell Rep. 2014, 9:234-247.
6. Du Z.W., Ma L.X., Phillips C., Zhang S.C. miR-200 and miR-96 families repress neural induction from human embryonic stem cells. Development 2013, 140:2611-2618.
7. Gill J.G., Langer E.M., Lindsley R.C., Cai M., Murphy T.L., Kyba M., Murphy K.M. Snail and the microRNA-200 family act in opposition to regulate epithelial-to-mesenchymal transition and germ layer fate restriction in differentiating ESCs. Stem Cells 2011, 29:764-776.
8. Graw J. The genetic and molecular basis of congenital eye defects. Nat. Rev. Genet. 2003, 4:876-888.
9. Hanna J., Markoulaki S., Schorderet P., Carey B.W., Beard C., Wernig M., Creyghton M.P., Steine E.J., Cassady J.P., Foreman R., et al. Direct reprogramming of terminally differentiated mature B lymphocytes to pluripotency. Cell 2008, 133:250-264.
10. Hikichi T., Matoba R., Ikeda T., Watanabe A., Yamamoto T., Yoshitake S., Tamura-Nakano M., Kimura T., Kamon M., Shimura M., et al. Transcription factors interfering with dedifferentiation induce cell type-specific transcriptional profiles. Proc. Natl. Acad. Sci. USA 2013, 110:6412-6417.
11. Kao W.W., Liu C.Y., Converse R.L., Shiraishi A., Kao C.W., Ishizaki M., Doetschman T., Duffy J. Keratin 12-deficient mice have fragile corneal epithelia. Invest. Ophthalmol. Vis. Sci. 1996, 37:2572-2584.
12. Kfoury Y., Scadden D.T. Mesenchymal cell contributions to the stem cell niche. Cell Stem Cell 2015, 16:239-253.
13. Kitazawa K., Kawasaki S., Shinomiya K., Aoi K., Matsuda A., Funaki T., Yamasaki K., Nakatsukasa M., Ebihara N., Murakami A., et al. Establishment of a human corneal epithelial cell line lacking the functional TACSTD2 gene as an in vitro model for gelatinous drop-like dystrophy. Invest. Ophthalmol. Vis. Sci. 2013, 54:5701-5711.
14. Koster M.I., Roop D.R. Mechanisms regulating epithelial stratification. Annu. Rev. Cell Dev. Biol. 2007, 23:93-113.
15. Lee T.I., Young R.A. Transcriptional regulation and its misregulation in disease. Cell 2013, 152:1237-1251.
16. Lee B., Villarreal-Ponce A., Fallahi M., Ovadia J., Sun P., Yu Q.C., Ito S., Sinha S., Nie Q., Dai X. Transcriptional mechanisms link epithelial plasticity to adhesion and differentiation of epidermal progenitor cells. Dev. Cell 2014, 29:47-58.
17. Mackay D.R., Hu M., Li B., Rhéaume C., Dai X. The mouse Ovol2 gene is required for cranial neural tube development. Dev. Biol. 2006, 291:38-52.
18. Miyoshi T., Maruhashi M., Van De Putte T., Kondoh H., Huylebroeck D., Higashi Y. Complementary expression pattern of Zfhx1 genes Sip1 and deltaEF1 in the mouse embryo and their genetic interaction revealed by compound mutants. Dev. Dyn. 2006, 235:1941-1952.
19. Ordonez P., Di Girolamo N. Limbal epithelial stem cells: role of the niche microenvironment. Stem Cells 2012, 30:100-107.
20. Ouyang H., Xue Y., Lin Y., Zhang X., Xi L., Patel S., Cai H., Luo J., Zhang M., Zhang M., et al. WNT7A and PAX6 define corneal epithelium homeostasis and pathogenesis. Nature 2014, 511:358-361.
21. Ozair M.Z., Kintner C., Brivanlou A.H. Neural induction and early patterning in vertebrates. Wiley Interdiscip. Rev. Dev. Biol. 2013, 2:479-498.
22. Pellegrini G., Dellambra E., Golisano O., Martinelli E., Fantozzi I., Bondanza S., Ponzin D., McKeon F., De Luca M. p63 identifies keratinocyte stem cells. Proc. Natl. Acad. Sci. USA 2001, 98:3156-3161.
23. Perry K.J., Thomas A.G., Henry J.J. Expression of pluripotency factors in larval epithelia of the frog Xenopus: evidence for the presence of cornea epithelial stem cells. Dev. Biol. 2013, 374:281-294.
24. Schermer A., Galvin S., Sun T.T. 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.
25. Shirakihara T., Saitoh M., Miyazono K. Differential regulation of epithelial and mesenchymal markers by deltaEF1 proteins in epithelial mesenchymal transition induced by TGF-beta. Mol. Biol. Cell 2007, 18:3533-3544.
26. Stergachis A.B., Neph S., Reynolds A., Humbert R., Miller B., Paige S.L., Vernot B., Cheng J.B., Thurman R.E., Sandstrom R., et al. Developmental fate and cellular maturity encoded in human regulatory DNA landscapes. Cell 2013, 154:888-903.
27. Swamynathan S.K., Katz J.P., Kaestner K.H., Ashery-Padan R., Crawford M.A., Piatigorsky J. Conditional deletion of the mouse Klf4 gene results in corneal epithelial fragility, stromal edema, and loss of conjunctival goblet cells. Mol. Cell. Biol. 2007, 27:182-194.
28. Watanabe K., Villarreal-Ponce A., Sun P., Salmans M.L., Fallahi M., Andersen B., Dai X. Mammary morphogenesis and regeneration require the inhibition of EMT at terminal end buds by Ovol2 transcriptional repressor. Dev. Cell 2014, 29:59-74.
29. Xu J., Du Y., Deng H. Direct lineage reprogramming: strategies, mechanisms, and applications. Cell Stem Cell 2015, 16:119-134.
30. Yamben I.F., Rachel R.A., Shatadal S., Copeland N.G., Jenkins N.A., Warming S., Griep A.E. Scrib is required for epithelial cell identity and prevents epithelial to mesenchymal transition in the mouse. Dev. Biol. 2013, 384:41-52.
31. Yoshida Y., Ban Y., Kinoshita S. Tight junction transmembrane protein claudin subtype expression and distribution in human corneal and conjunctival epithelium. Invest. Ophthalmol. Vis. Sci. 2009, 50:2103-2108.
32. Zhang X., Huang C.T., Chen J., Pankratz M.T., Xi J., Li J., Yang Y., Lavaute T.M., Li X.J., Ayala M., et al. Pax6 is a human neuroectoderm cell fate determinant. Cell Stem Cell 2010, 7:90-100.
33. Zhang T., Zhu Q., Xie Z., Chen Y., Qiao Y., Li L., Jing N. The zinc finger transcription factor Ovol2 acts downstream of the bone morphogenetic protein pathway to regulate the cell fate decision between neuroectoderm and mesendoderm. J. Biol. Chem. 2013, 288:6166-6177.