Pathogenic function of herpesvirus entry mediator in experimental autoimmune uveitis by induction of Th1- and Th17-type T cell responses

Journal of Immunology

Volumn 196, Issue 7, 2016, Pages 2947-2954

  Sakoda, Yukimi ^a   Nagai, Tomohiko ^a   Murata, Sizuka ^a   Mizuno, Yukari ^a   Kurosawa, Hiromi ^a   Shoda, Hiromi ^a   Morishige, Naoyuki ^a   Yanai, Ryoji ^a   Sonoda, Koh Hei ^a   Tamada, Koji ^a  

^a YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HERPESVIRUS ENTRY MEDIATOR; BTLA PROTEIN, MOUSE; CYTOKINE; HERPESVIRUS ENTRY MEDIATOR LIGAND; IMMUNOGLOBULIN RECEPTOR; LIGAND; MONOCLONAL ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE UVEITIS; CELL DIFFERENTIATION; CELLULAR IMMUNITY; CHEMOLUMINESCENCE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE COURSE; DISEASE PREDISPOSITION; IMMUNOMODULATION; IMMUNOREGULATION; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; OPHTHALMOSCOPY; PATHOGENESIS; PHENOTYPE; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TH1 CELL; TH17 CELL; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; AUTOIMMUNE DISEASES; CYTOLOGY; DISEASE MODEL; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; UVEITIS;

ANIMALS; ANTIBODIES, MONOCLONAL; AUTOIMMUNE DISEASES; CELL DIFFERENTIATION; CYTOKINES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; LIGANDS; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; RECEPTORS, IMMUNOLOGIC; RECEPTORS, TUMOR NECROSIS FACTOR, MEMBER 14; SIGNAL TRANSDUCTION; TH1 CELLS; TH17 CELLS; TUMOR NECROSIS FACTOR LIGAND SUPERFAMILY MEMBER 14; UVEITIS;

EID: 84962568409     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501742     Document Type: Article

References (49)

1. Suttorp-Schulten, M. S., and A. Rothova. 1996. The possible impact of uveitis in blindness: a literature survey. Br. J. Ophthalmol. 80:844-848.
2. Gritz, D. C., and I. G. Wong. 2004. Incidence and prevalence of uveitis in Northern California; the Northern California Epidemiology of Uveitis Study. Ophthalmology 111:491-500, discussion 500.
3. Tomkins-Netzer, O., L. Talat, A. Bar, A. Lula, S. R. Taylor, L. Joshi, and S. Lightman. 2014. Long-term clinical outcome and causes of vision loss in patients with uveitis. Ophthalmology 121:2387-2392.
4. Barisani-Asenbauer, T., S. M. Maca, L. Mejdoubi, W. Emminger, K. Machold, and H. Auer. 2012. Uveitis-a rare disease often associated with systemic diseases and infections-a systematic review of 2619 patients. Orphanet J. Rare Dis. 7:57-63.
5. Uchiyama, E., G. N. Papaliodis, A. M. Lobo, and L. Sobrin. 2014. Side-effects of anti-inflammatory therapy in uveitis. Semin. Ophthalmol. 29:456-467.
6. Sangwan, V. S. 2010. Treatment of uveitis: beyond steroids. Indian J. Ophthalmol. 58:1-2.
7. Caspi, R. R., F. G. Roberge, C. C. Chan, B. Wiggert, G. J. Chader, L. A. Rozenszajn, Z. Lando, and R. B. Nussenblatt. 1988. A new model of autoimmune disease. Experimental autoimmune uveoretinitis induced in mice with two different retinal antigens. J. Immunol. 140:1490-1495.
8. Tang, J., W. Zhu, P. B. Silver, S. B. Su, C. C. Chan, and R. R. Caspi. 2007. Autoimmune uveitis elicited with antigen-pulsed dendritic cells has a distinct clinical signature and is driven by unique effector mechanisms: initial encounter with autoantigen defines disease phenotype. J. Immunol. 178:5578-5587.
9. Amadi-Obi, A., C. R. Yu, X. Liu, R. M. Mahdi, G. L. Clarke, R. B. Nussenblatt, I. Gery, Y. S. Lee, and C. E. Egwuagu. 2007. TH17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1. Nat. Med. 13:711-718.
10. Luger, D., P. B. Silver, J. Tang, D. Cua, Z. Chen, Y. Iwakura, E. P. Bowman, N. M. Sgambellone, C. C. Chan, and R. R. Caspi. 2008. Either a Th17 or a Th1 effector response can drive autoimmunity: conditions of disease induction affect dominant effector category. J. Exp. Med. 205:799-810.
11. Yoshimura, T., K. H. Sonoda, Y. Miyazaki, Y. Iwakura, T. Ishibashi, A. Yoshimura, and H. Yoshida. 2008. Differential roles for IFN-gamma and IL-17 in experimental autoimmune uveoretinitis. Int. Immunol. 20:209-214.
12. Yoshimura, T., K. H. Sonoda, N. Ohguro, Y. Ohsugi, T. Ishibashi, D. J. Cua, T. Kobayashi, H. Yoshida, and A. Yoshimura. 2009. Involvement of Th17 cells and the effect of anti-IL-6 therapy in autoimmune uveitis. Rheumatology (Oxford) 48:347-354.
13. Damsker, J. M., A. M. Hansen, and R. R. Caspi. 2010. Th1 and Th17 cells: adversaries and collaborators. Ann. N. Y. Acad. Sci. 1183:211-221.
14. Chen, L., and D. B. Flies. 2013. Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat. Rev. Immunol. 13:227-242.
15. Murphy, T. L., and K. M. Murphy. 2010. Slow down and survive: Enigmatic immunoregulation by BTLA and HVEM. Annu. Rev. Immunol. 28:389-411.
16. Mauri, D. N., R. Ebner, R. I. Montgomery, K. D. Kochel, T. C. Cheung, G. L. Yu, S. Ruben, M. Murphy, R. J. Eisenberg, G. H. Cohen, et al. 1998. LIGHT, a new member of the TNF superfamily, and lymphotoxin alpha are ligands for herpesvirus entry mediator. Immunity 8:21-30.
17. Sakoda, Y., J. J. Park, Y. Zhao, A. Kuramasu, D. Geng, Y. Liu, E. Davila, and K. Tamada. 2011. Dichotomous regulation of GVHD through bidirectional functions of the BTLA-HVEM pathway. Blood 117:2506-2514.
18. Xu, Y., A. S. Flies, D. B. Flies, G. Zhu, S. Anand, S. J. Flies, H. Xu, R. A. Anders, W. W. Hancock, L. Chen, and K. Tamada. 2007. Selective targeting of the LIGHT-HVEM costimulatory system for the treatment of graftversushost disease. Blood 109:4097-4104.
19. Tamada, K., K. Shimozaki, A. I. Chapoval, Y. Zhai, J. Su, S. F. Chen, S. L. Hsieh, S. Nagata, J. Ni, and L. Chen. 2000. LIGHT, a TNF-like molecule, costimulates T cell proliferation and is required for dendritic cell-mediated allogeneic T cell response. J. Immunol. 164:4105-4110.
20. + T cells through interaction with herpesvirus entry mediator. Nat. Immunol. 9:176-185.
21. Sedy, J. R., M. Gavrieli, K. G. Potter, M. A. Hurchla, R. C. Lindsley, K. Hildner, S. Scheu, K. Pfeffer, C. F. Ware, T. L. Murphy, and K. M. Murphy. 2005. B and T lymphocyte attenuator regulates T cell activation through interaction with herpesvirus entry mediator. Nat. Immunol. 6:90-98.
22. Ye, Q., C. C. Fraser, W. Gao, L. Wang, S. J. Busfield, C. Wang, Y. Qiu, A. J. Coyle, J. C. Gutierrez-Ramos, and W. W. Hancock. 2002. Modulation of LIGHT-HVEM costimulation prolongs cardiac allograft survival. J. Exp. Med. 195:795-800.
23. Wang, Y., S. K. Subudhi, R. A. Anders, J. Lo, Y. Sun, S. Blink, Y. Wang, J. Wang, X. Liu, K. Mink, et al. 2005. The role of herpesvirus entry mediator as a negative regulator of T cell-mediated responses. J. Clin. Invest. 115:711-717.
24. Pierer, M., A. Schulz, M. Rossol, E. Kendzia, D. Kyburz, H. Haentzschel, C. Baerwald, and U. Wagner. 2009. Herpesvirus entry mediator-Ig treatment during immunization aggravates rheumatoid arthritis in the collagen-induced arthritis model. J. Immunol. 182:3139-3145.
25. Sakoda, Y., S. Anand, Y. Zhao, J. J. Park, Y. Liu, A. Kuramasu, N. Van Rooijen, L. Chen, S. E. Strome, W. W. Hancock, et al. 2011. Herpesvirus entry mediator regulates hypoxia-inducible factor-1α and erythropoiesis in mice. J. Clin. Invest. 121:4810-4819.
26. Chan, C. C., R. R. Caspi, M. Ni, W. C. Leake, B. Wiggert, G. J. Chader, and R. B. Nussenblatt. 1990. Pathology of experimental autoimmune uveoretinitis in mice. J. Autoimmun. 3:247-255.
27. Avichezer, D., P. B. Silver, C. C. Chan, B. Wiggert, and R. R. Caspi. 2000. Identification of a new epitope of human IRBP that induces autoimmune uveoretinitis in mice of the H-2b haplotype. Invest. Ophthalmol. Vis. Sci. 41:127-131.
28. Tao, R., L. Wang, K. M. Murphy, C. C. Fraser, and W. W. Hancock. 2008. Regulatory T cell expression of herpesvirus entry mediator suppresses the function of B and T lymphocyte attenuator-positive effector T cells. J. Immunol. 180:6649-6655.
29. Sharma, S., N. K. Rajasagi, T. Veiga-Parga, and B. T. Rouse. 2014. Herpes virus entry mediator (HVEM) modulates proliferation and activation of regulatory T cells following HSV-1 infection. Microbes Infect. 16:648-660.
30. Huang, Y., Y. Zhao, X. Ran, and C. Wang. 2014. Increased expression of herpesvirus entry mediator in 1, 25-dihydroxyvitamin D3-treated mouse bone marrow-derived dendritic cells promotes the generation of CD4. CD25. Foxp3. regulatory T cells. Mol. Med. Rep. 9:813-818.
31. Shui, J. W., A. Larange, G. Kim, J. L. Vela, S. Zahner, H. Cheroutre, and M. Kronenberg. 2012. HVEM signalling at mucosal barriers provides host defence against pathogenic bacteria. Nature 488:222-225.
32. Shui, J. W., and M. Kronenberg. 2013. HVEM: An unusual TNF receptor family member important for mucosal innate immune responses to microbes. Gut Microbes 4:146-151.
33. Liang, D., A. Zuo, H. Shao, W. K. Born, R. L. O'Brien, H. J. Kaplan, and D. Sun. 2013. IL-23 receptor expression on gd T cells correlates with their enhancing or suppressive effects on autoreactive T cells in experimental autoimmune uveitis. J. Immunol. 191:1118-1125.
34. Cui, Y., H. Shao, C. Lan, H. Nian, R. L. O'Brien, W. K. Born, H. J. Kaplan, and D. Sun. 2009. Major role of gamma delta T cells in the generation of IL-17+ uveitogenic T cells. J. Immunol. 183:560-567.
35. Kwon, B. S., K. B. Tan, J. Ni, K. O. Oh, Z. H. Lee, K. K. Kim, Y. J. Kim, S. Wang, R. Gentz, G. L. Yu, et al. 1997. A newly identified member of the tumor necrosis factor receptor superfamily with a wide tissue distribution and involvement in lymphocyte activation. J. Biol. Chem. 272:14272-14276.
36. Steinberg, M. W., O. Turovskaya, R. B. Shaikh, G. Kim, D. F. McCole, K. Pfeffer, K. M. Murphy, C. F. Ware, and M. Kronenberg. 2008. A crucial role for HVEM and BTLA in preventing intestinal inflammation. J. Exp. Med. 205:1463-1476.
37. Kovacs, S. K., V. Tiwari, E. Prandovszky, S. Dosa, S. Bacsa, K. Valyi-Nagy, D. Shukla, and T. Valyi-Nagy. 2009. Expression of herpes virus entry mediator (HVEM) in the cornea and trigeminal ganglia of normal and HSV-1 infected mice. Curr. Eye Res. 34:896-904.
38. Akhtar, J., V. Tiwari, M. J. Oh, M. Kovacs, A. Jani, S. K. Kovacs, T. Valyi-Nagy, and D. Shukla. 2008. HVEM and nectin-1 are the major mediators of herpes simplex virus 1 (HSV-1) entry into human conjunctival epithelium. Invest. Ophthalmol. Vis. Sci. 49:4026-4035.
39. Usui, Y., H. Akiba, M. Takeuchi, T. Kezuka, A. Takeuchi, T. Hattori, Y. Okunuki, T. Yamazaki, H. Yagita, M. Usui, and K. Okumura. 2006. The role of the ICOS/B7RP-1 T cell costimulatory pathway in murine experimental autoimmune uveoretinitis. Eur. J. Immunol. 36:3071-3081.
40. Hou, Y., L. Xing, S. Fu, X. Zhang, J. Liu, H. Liu, B. Lv, and H. Cui. 2009. Downregulation of inducible co-stimulator (ICOS) by intravitreal injection of small interfering RNA (siRNA) plasmid suppresses ongoing experimental autoimmune uveoretinitis in rats. Graefes Arch. Clin. Exp. Ophthalmol. 247:755-765.
41. Verwaerde, C., M. C. Naud, A. Delanoye, M. Wood, B. Thillaye-Goldenberg, C. Auriault, and Y. De Kozak. 2003. Ocular transfer of retinal glial cells transduced ex vivo with adenovirus expressing viral IL-10 or CTLA4-Ig inhibits experimental autoimmune uveoretinitis. Gene Ther. 10:1970-1981.
42. Wei, C. Y., Y. H. Chou, F. M. Ho, S. L. Hsieh, and W. W. Lin. 2006. Signaling pathways of LIGHT induced macrophage migration and vascular smooth muscle cell proliferation. J. Cell. Physiol. 209:735-743.
43. + Th1 cell response, and resistance to Leishmania major. J. Immunol. 179:6901-6909.
44. Jin, W., X. F. Zhou, J. Yu, X. Cheng, and S. C. Sun. 2009. Regulation of Th17 cell differentiation and EAE induction by MAP3K NIK. Blood 113:6603-6610.
45. Haruta, H., N. Ohguro, M. Fujimoto, S. Hohki, F. Terabe, S. Serada, S. Nomura, K. Nishida, T. Kishimoto, and T. Naka. 2011. Blockade of interleukin-6 signaling suppresses not only th17 but also interphotoreceptor retinoid binding protein-specific Th1 by promoting regulatory T cells in experimental autoimmune uveoretinitis. Invest. Ophthalmol. Vis. Sci. 52:3264-3271.
46. Silver, P. B., R. Horai, J. Chen, Y. Jittayasothorn, C. C. Chan, R. Villasmil, M. R. Kesen, and R. R. Caspi. 2015. Retina-specific T regulatory cells bring about resolution and maintain remission of autoimmune uveitis. J. Immunol. 194:3011-3019.
47. + T cells. J. Immunol. 174:3377-3385.
48. Letko, E., S. Yeh, C. S. Foster, U. Pleyer, M. Brigell, and C. L. Grosskreutz, AIN457A2208 Study Group. 2015. Efficacy and safety of intravenous secukinumab in noninfectious uveitis requiring steroid-sparing immunosuppressive therapy. Ophthalmology 122:939-948.
49. Maya, J. R., M. A. Sadiq, L. J. Zapata, M. Hanout, S. Sarwar, N. Rajagopalan, K. E. Guinn, Y. J. Sepah, and Q. D. Nguyen. 2014. Emerging therapies for noninfectious uveitis: what may be coming to the clinics. J. Ophthalmol. 2014:310329.