Pax6 Downregulation Mediates Abnormal Lineage Commitment of the Ocular Surface Epithelium in Aqueous-Deficient Dry Eye Disease

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Chen, Ying Ting ^a   Chen, Feeling Y T ^a   Vijmasi, Trinka ^a   Stephens, Denise N ^a   Gallup, Marianne ^a   McNamara, Nancy A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKERATIN 10; CYTOKERATIN 12; INTERLEUKIN 1 RECEPTOR; TRANSCRIPTION FACTOR PAX6;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNITY; AUTOREACTIVITY; CD4+ T LYMPHOCYTE; CELL LINEAGE; CELL SPECIFICITY; CONTROLLED STUDY; CORNEA EPITHELIUM; DISEASE COURSE; DOWN REGULATION; EYE DEVELOPMENT; IMMUNE DEFICIENCY; IMMUNOREACTIVITY; KERATINIZING SQUAMOUS METAPLASIA; KERATOCONJUNCTIVITIS SICCA; KNOCKOUT MOUSE; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; OCULAR SURFACE DISEASE; PATHOGENESIS; PHENOTYPE; PROTEIN DEPLETION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SQUAMOUS CELL METAPLASIA;

ANIMALS; AUTOIMMUNE DISEASES; CD4-POSITIVE T-LYMPHOCYTES; CELL LINEAGE; CORNEA; DOWN-REGULATION; DRY EYE SYNDROMES; EPITHELIUM; EYE; EYE PROTEINS; GENE KNOCKDOWN TECHNIQUES; HOMEODOMAIN PROTEINS; HUMANS; MICE; MUCOUS MEMBRANE; PAIRED BOX TRANSCRIPTION FACTORS; PHENOTYPE; RECEPTORS, INTERLEUKIN-1; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION;

EID: 84885462442     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077286     Document Type: Article

References (35)

1. Li W, Hayashida Y, Chen YT, He H, Tseng DY, et al. (2008) Air exposure induced squamous metaplasia of human limbal epithelium. Invest Ophthalmol Vis Sci 49: 154-162. doi:10.1167/iovs.07-0883. PubMed: 18172087.
2. Sun TT, (2006) Altered phenotype of cultured urothelial and other stratified epithelial cells: implications for wound healing. Am J Physiol Renal Physiol 291: F9-21. doi:10.1152/ajprenal.00035.2006. PubMed: 16609152.
3. Tseng SC, (1985) Staging of conjunctival squamous metaplasia by impression cytology. Ophthalmology 92: 728-733. PubMed: 3897935.
4. Chen YT, Lazarev S, Bahrami AF, Noble LB, Chen FY, et al. (2012) Interleukin-1 receptor mediates the interplay between CD4(+) T cells and ocular resident cells to promote keratinizing squamous metaplasia in Sjogren's syndrome. Lab Invest; J Tech Methods Pathol.
5. Chen YT, Li S, Nikulina K, Porco T, Gallup M, et al. (2009) Immune profile of squamous metaplasia development in autoimmune regulator-deficient dry eye. Mol Vis 15: 563-576. PubMed: 19365590.
6. Chen YT, Nikulina K, Lazarev S, Bahrami AF, Noble LB, et al. (2010) Interleukin-1 as a phenotypic immunomodulator in keratinizing squamous metaplasia of the ocular surface in Sjogren's syndrome. Am J Pathol 177: 1333-1343. doi:10.2353/ajpath.2010.100227. PubMed: 20696775.
7. DeVoss J, Hou Y, Johannes K, Lu W, Liou GI, et al. (2006) Spontaneous autoimmunity prevented by thymic expression of a single self-antigen. J Exp Med 203: 2727-2735. doi:10.1084/jem.20061864. PubMed: 17116738.
8. DeVoss JJ, LeClair NP, Hou Y, Grewal NK, Johannes KP, et al. (2010) An autoimmune response to odorant binding protein 1a is associated with dry eye in the aire-deficient mouse. J Immunol 184: 4236-4246. doi:10.4049/jimmunol.0902434. PubMed: 20237294.
9. Li S, Nikulina K, DeVoss J, Wu AJ, Strauss EC, et al. (2008) Small proline-rich protein 1B (SPRR1B) is a biomarker for squamous metaplasia in dry eye disease. Invest Ophthalmol Vis Sci 49: 34-41. doi:10.1167/iovs.07-0685. PubMed: 18172072.
10. Collinson JM, Chanas SA, Hill RE, West JD, (2004) Corneal development, limbal stem cell function, and corneal epithelial cell migration in the Pax6(+/-) mouse. Invest Ophthalmol Vis Sci 45: 1101-1108. doi:10.1167/iovs.03-1118. PubMed: 15037575.
11. Shiraishi A, Converse RL, Liu CY, Zhou F, Kao CW, et al. (1998) Identification of the cornea-specific keratin 12 promoter by in vivo particle-mediated gene transfer. Invest Ophthalmol Vis Sci 39: 2554-2561. PubMed: 9856765.
12. Koroma BM, Yang JM, Sundin OH, (1997) The Pax-6 homeobox gene is expressed throughout the corneal and conjunctival epithelia. Invest Ophthalmol Vis Sci 38: 108-120. PubMed: 9008636.
13. Li W, Chen YT, Hayashida Y, Blanco G, Kheirkah A, et al. (2008) Down-regulation of Pax6 is associated with abnormal differentiation of corneal epithelial cells in severe ocular surface diseases. J Pathol 214: 114-122. doi:10.1002/path.2256. PubMed: 18027901.
14. Whitcher JP, Shiboski CH, Shiboski SC, Heidenreich AM, Kitagawa K, et al. (2010) A simplified quantitative method for assessing keratoconjunctivitis sicca from the Sjogren's Syndrome International Registry. Am J Ophthalmol 149: 405-415. doi:10.1016/j.ajo.2009.09.013. PubMed: 20035924.
15. Anderson MS, Venanzi ES, Klein L, Chen Z, Berzins SP, et al. (2002) Projection of an immunological self shadow within the thymus by the aire protein. Science 298: 1395-1401. doi:10.1126/science.1075958. PubMed: 12376594.
16. Kawakita T, Espana EM, He H, Yeh LK, Liu CY, et al. (2004) Calcium-induced abnormal epidermal-like differentiation in cultures of mouse corneal-limbal epithelial cells. Invest Ophthalmol Vis Sci 45: 3507-3512. doi:10.1167/iovs.04-0266. PubMed: 15452056.
17. Chen YT, Li W, Hayashida Y, He H, Chen SY, et al. (2007) Human amniotic epithelial cells as novel feeder layers for promoting ex vivo expansion of limbal epithelial progenitor cells. Stem Cells 25: 1995-2005. doi:10.1634/stemcells.2006-0677. PubMed: 17495107.
18. Bian F, Qi H, Ma P, Zhang L, Yoon KC, et al. (2010) An immunoprotective privilege of corneal epithelial stem cells against Th17 inflammatory stress by producing glial cell-derived neurotrophic factor. Stem Cells 28: 2172-2181. doi:10.1002/stem.539. PubMed: 20936708.
19. De Paiva CS, Corrales RM, Villarreal AL, Farley WJ, Li DQ, et al. (2006) Corticosteroid and doxycycline suppress MMP-9 and inflammatory cytokine expression, MAPK activation in the corneal epithelium in experimental dry eye. Exp Eye Res 83: 526-535. doi:10.1016/j.exer.2006.02.004. PubMed: 16643899.
20. Yoon KC, De Paiva CS, Qi H, Chen Z, Farley WJ, et al. (2007) Expression of Th-1 chemokines and chemokine receptors on the ocular surface of C57BL/6 mice: effects of desiccating stress. Invest Ophthalmol Vis Sci 48: 2561-2569. doi:10.1167/iovs.07-0002. PubMed: 17525185.
21. Li S, Nikulina K, DeVoss J, Wu AJ, Strauss EC, et al. (2008) Small proline-rich protein 1B (SPRR1B) is a biomarker for squamous metaplasia in dry eye disease. Invest Ophthalmol Vis Sci 49: 34-41. doi:10.1167/iovs.07-0685. PubMed: 18172072.
22. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45. doi:10.1093/nar/29.9.e45. PubMed: 11328886.
23. Ouyang J, Shen YC, Yeh LK, Li W, Coyle BM, et al. (2006) Pax6 overexpression suppresses cell proliferation and retards the cell cycle in corneal epithelial cells. Invest Ophthalmol Vis Sci 47: 2397-2407. doi:10.1167/iovs.05-1083. PubMed: 16723449.
24. Zhou D, Chen YT, Chen F, Gallup M, Vijmasi T, et al. (2012) Critical involvement of macrophage infiltration in the development of Sjogren's syndrome-associated dry eye. Am J Pathol 181: 753-760. doi:10.1016/j.ajpath.2012.05.014. PubMed: 22770665.
25. Slack JM, (2007) Metaplasia and transdifferentiation: from pure biology to the clinic. Nat Rev Mol Cell Biol 8: 369-378. doi:10.1038/nrm2146. PubMed: 17377526.
26. Moll R, Krepler R, Franke WW, (1983) Complex cytokeratin polypeptide patterns observed in certain human carcinomas. Differ Res Biol Divers 23: 256-269. PubMed: 6189757.
27. Cooper KD, Breathnach SM, Caughman SW, Palini AG, Waxdal MJ, et al. (1985) Fluorescence microscopic and flow cytometric analysis of bone marrow-derived cells in human epidermis: a search for the human analogue of the murine dendritic Thy-1+ epidermal cell. J Invest Dermatol 85: 546-552. doi:10.1111/1523-1747.ep12277391. PubMed: 2866216.
28. Schermer A, Galvin S, Sun TT, (1986) 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 103: 49-62. doi:10.1083/jcb.103.1.49. PubMed: 2424919.
29. Chin-Chance CV, Newman MV, Aronovitz A, Blomeier H, Kruger J, et al. (2006) Role of the mitogen-activated protein kinases in cytokine-mediated inhibition of insulin gene expression. J Invest Med Off Publ American Federation For Clinical Research 54: 132-142. doi:10.2310/6650.2006.05035. PubMed: 16948396.
30. Gasche JA, Hoffmann J, Boland CR, Goel A, (2011) Interleukin-6 promotes tumorigenesis by altering DNA methylation in oral cancer cells. Int J Cancer J Int Cancer 129: 1053-1063. doi:10.1002/ijc.25764. PubMed: 21710491.
31. Sivak JM, West-Mays JA, Yee A, Williams T, Fini ME, (2004) Transcription Factors Pax6 and AP-2alpha Interact To Coordinate Corneal Epithelial Repair by Controlling Expression of Matrix Metalloproteinase Gelatinase B. Mol Cell Biol 24: 245-257. doi:10.1128/MCB.24.1.245-257.2004. PubMed: 14673159.
32. Blazejewska EA, Schlötzer-Schrehardt U, Zenkel M, Bachmann B, Chankiewitz E, et al. (2009) Corneal limbal microenvironment can induce transdifferentiation of hair follicle stem cells into corneal epithelial-like cells. Stem Cells 27: 642-652. doi:10.1634/stemcells.2008-0721. PubMed: 19074417.
33. Davis J, Duncan MK, Robison WG Jr., Piatigorsky J, (2003) Requirement for Pax6 in corneal morphogenesis: a role in adhesion. J Cell Sci 116: 2157-2167. doi:10.1242/jcs.00441. PubMed: 12692153.
34. Pearton DJ, Yang Y, Dhouailly D, (2005) Transdifferentiation of corneal epithelium into epidermis occurs by means of a multistep process triggered by dermal developmental signals. Proc Natl Acad Sci U S A 102: 3714-3719. doi:10.1073/pnas.0500344102. PubMed: 15738417.
35. Rowan S, Siggers T, Lachke SA, Yue Y, Bulyk ML, et al. (2010) Precise temporal control of the eye regulatory gene Pax6 via enhancer-binding site affinity. Genes Dev 24: 980-985. doi:10.1101/gad.1890410. PubMed: 20413611.