Desiccating stress-induced chemokine expression in the epithelium is dependent on upregulation of NKG2D/RAE-1 and release of IFN-γ in experimental dry eye

Journal of Immunology

Volumn 193, Issue 10, 2014, Pages 5264-5272

  Coursey, Terry G ^a   Bohat, Ritu ^a   Barbosa, Flavia L ^a   Pflugfelder, Stephen C ^a   De Paiva, Cintia S ^a  

^a CULLEN EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CXCL11 CHEMOKINE; CXCL9 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; NATURAL KILLER CELL RECEPTOR NKG2D; ANTIBODY; CXCL10 PROTEIN, MOUSE; CXCL11 PROTEIN, MOUSE; CXCL9 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; KLRB1C PROTEIN, MOUSE; KLRK1 PROTEIN, MOUSE; LY ANTIGEN; MEMBRANE PROTEIN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY B; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K; RAET1A PROTEIN, MOUSE; RAG-1 PROTEIN;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INFILTRATION; CELL STRESS; CONTROLLED STUDY; CORNEA EPITHELIUM; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE SEVERITY; DOWN REGULATION; DRY EYE; EPITHELIUM CELL; FEMALE; GENE; IMMUNE SYSTEM; INNATE IMMUNITY; MOUSE; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; RAE 1 GENE; SIGNAL TRANSDUCTION; T LYMPHOCYTE; UPREGULATION; ADOPTIVE TRANSFER; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CONJUNCTIVA; DESICCATION; DISEASE MODEL; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; PATHOLOGY; TRANSPLANTATION; XEROPHTHALMIA;

ADOPTIVE TRANSFER; ANIMALS; ANTIBODIES; ANTIGENS, LY; CHEMOKINE CXCL10; CHEMOKINE CXCL11; CHEMOKINE CXCL9; CONJUNCTIVA; DESICCATION; DISEASE MODELS, ANIMAL; EPITHELIUM, CORNEAL; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; IMMUNITY, INNATE; INTERFERON-GAMMA; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY B; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; T-LYMPHOCYTES; XEROPHTHALMIA;

EID: 84910136874     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400016     Document Type: Article

References (38)

1. Niederkorn, J. Y., M. E. Stern, S. C. Pflugfelder, C. S. De Paiva, R. M. Corrales, J. Gao, and K. Siemasko. 2006. Desiccating stress induces T cell-mediated Sjögren's syndrome-like lacrimal keratoconjunctivitis. J. Immunol. 176: 3950-3957.
2. de Paiva, C. S., S. Chotikavanich, S. B. Pangelinan, J. I. Pitcher, B. Fang, X. Zheng, P. Ma, W. J. Farley, K. S. Siemasko, J. Y. Niederkorn, et al. 2009. IL-17 disrupts corneal barrier following desiccating stress. Mucosal Immunol. 2: 243-253.
3. De Paiva, C. S., A. L. Villarreal, R. M. Corrales, H. T. Rahman, V. Y. Chang, W. J. Farley, M. E. Stern, J. Y. Niederkorn, D. Q. Li, and S. C. Pflugfelder. 2007. Dry eye-induced conjunctival epithelial squamous metaplasia is modulated by interferon-γ. Invest. Ophthalmol. Vis. Sci. 48: 2553-2560.
4. + T-cell-mediated Sjögren's syndrome-like corneal epithelial apoptosis via activation of the extrinsic apoptotic pathway by interferon-γ. Am. J. Pathol. 179: 1807-1814.
5. Lam, H., L. Bleiden, C. S. de Paiva, W. Farley, M. E. Stern, and S. C. Pflugfelder. 2009. Tear cytokine profiles in dysfunctional tear syndrome. Am. J. Ophthalmol. 147: 198-205, e1.
6. Syrbe, U., J. Siveke, and A. Hamann. 1999. Th1/Th2 subsets: distinct differences in homing and chemokine receptor expression? Springer Semin. Immunopathol. 21: 263-285.
7. Yoon, K. C., C. S. De Paiva, H. Qi, Z. Chen, W. J. Farley, D. Q. Li, and S. C. Pflugfelder. 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.
8. Yoon, K. C., C. S. Park, I. C. You, H. J. Choi, K. H. Lee, S. K. Im, H. Y. Park, and S. C. Pflugfelder. 2010. Expression of CXCL9, -10, -11, and CXCR3 in the tear film and ocular surface of patients with dry eye syndrome. Invest. Ophthalmol. Vis. Sci. 51: 643-650.
9. + T cell mediated ocular surface disease in experimental dry eye disease. PLoS ONE 8: e78508.
10. Middendorp, S., and E. E. Nieuwenhuis. 2009. NKT cells in mucosal immunity. Mucosal Immunol. 2: 393-402.
11. Matangkasombut, P., M. Pichavant, R. H. Dekruyff, and D. T. Umetsu. 2009. Natural killer T cells and the regulation of asthma. Mucosal Immunol. 2: 383-392.
12. Huber, S., C. Shi, and R. C. Budd. 2002. γδ T cells promote a Th1 response during coxsackievirus B3 infection in vivo: role of Fas and Fas ligand. J. Virol. 76: 6487-6494.
13. Pegram, H. J., D. M. Andrews, M. J. Smyth, P. K. Darcy, and M. H. Kershaw. 2011. Activating and inhibitory receptors of natural killer cells. Immunol. Cell Biol. 89: 216-224.
14. Kubin, M., L. Cassiano, J. Chalupny, W. Chin, D. Cosman, W. Fanslow, J. Müllberg, A. M. Rousseau, D. Ulrich, and R. Armitage. 2001. ULBP1, 2, 3: novel MHC class I-related molecules that bind to human cytomegalovirus glycoprotein UL16, activate NK cells. Eur. J. Immunol. 31: 1428-1437.
15. + T cells to human corneal epithelium in vitro. BMC Ophthalmol. 12: 6.
16. Raulet, D. H., S. Gasser, B. G. Gowen, W. Deng, and H. Jung. 2013. Regulation of ligands for the NKG2D activating receptor. Annu. Rev. Immunol. 31: 413-441.
17. Zhang, X., E. A. Volpe, N. B. Gandhi, C. S. Schaumburg, K. F. Siemasko, S. B. Pangelinan, S. D. Kelly, A. C. Hayday, D. Q. Li, M. E. Stern, et al. 2012. NK cells promote Th-17 mediated corneal barrier disruption in dry eye. PLoS ONE 7: e36822.
18. Chen, Y., S. K. Chauhan, D. R. Saban, Z. Sadrai, A. Okanobo, and R. Dana. 2011. Interferon-γ-secreting NK cells promote induction of dry eye disease. J. Leukoc. Biol. 89: 965-972.
19. Luo, L., D. Q. Li, A. Doshi, W. Farley, R. M. Corrales, and S. C. Pflugfelder. 2004. Experimental dry eye stimulates production of inflammatory cytokines and MMP-9 and activates MAPK signaling pathways on the ocular surface. Invest. Ophthalmol. Vis. Sci. 45: 4293-4301.
20. + NKT cells induce the death of colitis-associated cells: involvement of programmed death ligand-1. Eur. J. Immunol. 36: 1210-1221.
21. Sierro, F., C. Biben, L. Martínez-Muñoz, M. Mellado, R. M. Ransohoff,M. Li, B. Woehl, H. Leung, J. Groom, M. Batten, et al. 2007. Disrupted cardiacdevelopment but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc. Natl. Acad. Sci. USA 104: 14759-14764.
22. Lacotte, S., S. Brun, S. Muller, and H. Dumortier. 2009. CXCR3, inflammation, and autoimmune diseases. Ann. N. Y. Acad. Sci. 1173: 310-317.
23. Corrales, R. M., M. E. Stern, C. S. De Paiva, J. Welch, D. Q. Li, and S. C. Pflugfelder. 2006. Desiccating stress stimulates expression of matrix metalloproteinases by the corneal epithelium. Invest. Ophthalmol. Vis. Sci. 47: 3293-3302.
24. Li, D. Q., Z. Chen, X. J. Song, L. Luo, and S. C. Pflugfelder. 2004. Stimulation of matrix metalloproteinases by hyperosmolarity via a JNK pathway in human corneal epithelial cells. Invest. Ophthalmol. Vis. Sci. 45: 4302-4311.
25. Luo, L., D. Q. Li, R. M. Corrales, and S. C. Pflugfelder. 2005. Hyperosmolar saline is a proinflammatory stress on the mouse ocular surface. Eye Contact Lens 31: 186-193.
26. Schaumburg, C. S., K. F. Siemasko, C. S. De Paiva, L. A. Wheeler, J. Y. Niederkorn, S. C. Pflugfelder, and M. E. Stern. 2011. Ocular surface APCs are necessary for autoreactive T cell-mediated experimental autoimmune lacrimal keratoconjunctivitis. J. Immunol. 187: 3653-3662.
27. Bacman, S., A. Berra, L. Sterin-Borda, and E. Borda. 2001. Muscarinic acetylcholine receptor antibodies as a new marker of dry eye Sjögren syndrome. Invest. Ophthalmol. Vis. Sci. 42: 321-327.
28. Stern, M. E., C. S. Schaumburg, K. F. Siemasko, J. Gao, L. A. Wheeler, D. A. Grupe, C. S. De Paiva, V. L. Calder, M. Calonge, J. Y. Niederkorn, and S. C. Pflugfelder. 2012. Autoantibodies contribute to the immunopathogenesis of experimental dry eye disease. Invest. Ophthalmol. Vis. Sci. 53: 2062-2075.
29. Groom, J. R., and A. D. Luster. 2011. CXCR3 ligands: redundant, collaborative and antagonistic functions. Immunol. Cell Biol. 89: 207-215.
30. De Paiva, C. S., R. M. Corrales, A. L. Villarreal, W. J. Farley, D. Q. Li, M. E. Stern, and S. C. Pflugfelder. 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.
31. Li, D. Q., L. Luo, Z. Chen, H. S. Kim, X. J. Song, and S. C. Pflugfelder. 2006. JNK and ERK MAP kinases mediate induction of IL-1β, TNF-α and IL-8 following hyperosmolar stress in human limbal epithelial cells. Exp. Eye Res. 82: 588-596.
32. Seo, M. J., J. M. Kim, M. J. Lee, Y. S. Sohn, K. K. Kang, and M. Yoo. 2010. The therapeutic effect of DA-6034 on ocular inflammation via suppression of MMP-9 and inflammatory cytokines and activation of the MAPK signaling pathway in an experimental dry eye model. Curr. Eye Res. 35: 165-175.
33. Pan, Z., Z. Wang, H. Yang, F. Zhang, and P. S. Reinach. 2011. TRPV1 activation is required for hypertonicity-stimulated inflammatory cytokine release in human corneal epithelial cells. Invest. Ophthalmol. Vis. Sci. 52: 485-493.
34. Molinero, L. L., M. B. Fuertes, M. V. Girart, L. Fainboim, G. A. Rabinovich, M. A. Costas, and N. W. Zwirner. 2004. NF-κB regulates expression of the MHC class I-related chain A gene in activated T lymphocytes. J. Immunol. 173: 5583-5590.
35. Lin, D., H. Lavender, E. J. Soilleux, and C. A. O'Callaghan. 2012. NF-κB regulates MICA gene transcription in endothelial cell through a genetically inhibitable control site. J. Biol. Chem. 287: 4299-4310.
36. Hamerman, J. A., K. Ogasawara, and L. L. Lanier. 2004. Cutting edge: Toll-like receptor signaling in macrophages induces ligands for the NKG2D receptor. J. Immunol. 172: 2001-2005.
37. Redfern, R. L., N. Patel, S. Hanlon, W. Farley, M. Gondo, S. C. Pflugfelder, and A. M. McDermott. 2013. Toll-like receptor expression and activation in mice with experimental dry eye. Invest. Ophthalmol. Vis. Sci. 54: 1554-1563.
38. Rusakiewicz, S., G. Nocturne, T. Lazure, M. Semeraro, C. Flament, S. Caillat-Zucman, D. Sene, N. Delahaye, E. Vivier, K. Chaba, et al. 2013. NCR3/NKp30 contributes to pathogenesis in primary Sjogren's syndrome. Sci. Transl. Med. 5: 195ra96.