B7x in the periphery abrogates pancreas-specific damage mediated by self-reactive CD8 T cells

Journal of Immunology

Volumn 189, Issue 8, 2012, Pages 4165-4174

  Lee, Jun Sik ^a,e   Scandiuzzi, Lisa ^a   Ray, Anjana ^a   Wei, Joyce ^b   Hofmeyer, Kimberly A ^a   Abadi, Yael M ^a   Loke, P'ng ^c   Lin, Juan ^a   Yuan, Jianda ^b   Serreze, David V ^d   Allison, James P ^a   Zang, Xingxing ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d JACKSON LABORATORY   (United States)

^e Chosun University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

B7X PROTEIN; LYMPHOCYTE ANTIGEN; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; ARTICLE; AUTOIMMUNITY; CD8+ T LYMPHOCYTE; CELL DEATH; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DIABETES MELLITUS; DISEASE SEVERITY; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; LYMPHOCYTE MIGRATION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; PANCREAS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; AUTOANTIGENS; CD8-POSITIVE T-LYMPHOCYTES; DIABETES MELLITUS, EXPERIMENTAL; DISEASE RESISTANCE; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PANCREAS; V-SET DOMAIN-CONTAINING T-CELL ACTIVATION INHIBITOR 1;

EID: 84867321651     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1201241     Document Type: Article

References (58)

1. Zang, X., P. Loke, J. Kim, K. Murphy, R. Waitz, and J. P. Allison. 2003. B7x: a widely expressed B7 family member that inhibits T cell activation. Proc. Natl. Acad. Sci. USA 100: 10388-10392.
2. Prasad, D. V., S. Richards, X. M. Mai, and C. Dong. 2003. B7S1, a novel B7 family member that negatively regulates T cell activation. Immunity 18: 863-873.
3. Sica, G. L., I. H. Choi, G. Zhu, K. Tamada, S. D. Wang, H. Tamura, A. I. Chapoval, D. B. Flies, J. Bajorath, and L. Chen. 2003. B7-H4, a molecule of the B7 family, negatively regulates T cell immunity. Immunity 18: 849-861.
4. Wei, J., P. Loke, X. Zang, and J. P. Allison. 2011. Tissue-specific expression of B7x protects from CD4 T cell-mediated autoimmunity. J. Exp. Med. 208: 1683-1694.
5. Rai, E., and E. K. Wakeland. 2011. Genetic predisposition to autoimmunity - what have we learned? Semin. Immunol. 23: 67-83.
6. Scandiuzzi, L., K. Ghosh, and X. Zang. 2011. T cell costimulation and coinhibition: genetics and disease. Discov. Med. 12: 119-128.
7. Todd, J. A. 2010. Etiology of type 1 diabetes. Immunity 32: 457-467.
8. Rainbow, D. B., C. Moule, H. I. Fraser, J. Clark, S. K. Howlett, O. Burren, M. Christensen, V. Moody, C. A. Steward, J. P. Mohammed, et al. 2011. Evidence that Cd101 is an autoimmune diabetes gene in nonobese diabetic mice. J. Immunol. 187: 325-336.
9. Hinks, A., A. Barton, N. Shephard, S. Eyre, J. Bowes, M. Cargill, E. Wang, X. Ke, G. C. Kennedy, S. John, et al British Society of Paediatric and Adolescent Rheumatology Study Group. 2009. Identification of a novel susceptibility locus for juvenile idiopathic arthritis by genome-wide association analysis. Arthritis Rheum. 60: 258-263.
10. Bottema, R. W., D. S. Postma, N. E. Reijmerink, C. Thijs, F. F. Stelma, H. A. Smit, C. P. van Schayck, B. Brunekreef, G. H. Koppelman, and M. Kerkhof. 2010. Interaction of T-cell and antigen presenting cell costimulatory genes in childhood IgE. Eur. Respir. J. 35: 54-63.
11. DiLorenzo, T. P., R. T. Graser, T. Ono, G. J. Christianson, H. D. Chapman, D. C. Roopenian, S. G. Nathenson, and D. V. Serreze. 1998. Major histocompatibility complex class I-restricted T cells are required for all but the end stages of diabetes development in nonobese diabetic mice and use a prevalent T cell receptor alpha chain gene rearrangement. Proc. Natl. Acad. Sci. USA 95: 12538-12543.
12. Lieberman, S. M., T. Takaki, B. Han, P. Santamaria, D. V. Serreze, and T. P. DiLorenzo. 2004. Individual nonobese diabetic mice exhibit unique patterns of CD8+ T cell reactivity to three islet antigens, including the newly identified widely expressed dystrophia myotonica kinase. J. Immunol. 173: 6727-6734.
13. Choisy-Rossi, C. M., T. M. Holl, M. A. Pierce, H. D. Chapman, and D. V. Serreze. 2004. Enhanced pathogenicity of diabetogenic T cells escaping a non-MHC gene-controlled near death experience. J. Immunol. 173: 3791-3800.
14. Ratzinger, G., J. Baggers, M. A. de Cos, J. Yuan, T. Dao, J. L. Reagan, C. Münz, G. Heller, and J. W. Young. 2004. Mature human Langerhans cells derived from CD34+ hematopoietic progenitors stimulate greater cytolytic T lymphocyte activity in the absence of bioactive IL-12p70, by either single peptide presentation or cross-priming, than do dermal-interstitial or monocyte-derived dendritic cells. J. Immunol. 173: 2780-2791.
15. Loke, P., and J. P. Allison. 2003. PD-L1 and PD-L2 are differentially regulated by Th1 and Th2 cells. Proc. Natl. Acad. Sci. USA 100: 5336-5341.
16. Loke, P., A. S. MacDonald, A. Robb, R. M. Maizels, and J. E. Allen. 2000. Alternatively activated macrophages induced by nematode infection inhibit proliferation via cell-to-cell contact. Eur. J. Immunol. 30: 2669-2678.
17. Weber, S. E., H. Tian, and L. A. Pirofski. 2011. CD8+ cells enhance resistance to pulmonary serotype 3 Streptococcus pneumoniae infection in mice. J. Immunol. 186: 432-442.
18. Takaki, T., S. M. Lieberman, T. M. Holl, B. Han, P. Santamaria, D. V. Serreze, and T. P. DiLorenzo. 2004. Requirement for both H-2Db and H-2Kd for the induction of diabetes by the promiscuous CD8+ T cell clonotype AI4. J. Immunol. 173: 2530-2541.
19. Sheehy, M. E., A. B. McDermott, S. N. Furlan, P. Klenerman, and D. F. Nixon. 2001. A novel technique for the fluorometric assessment of T lymphocyte antigen specific lysis. J. Immunol. Methods 249: 99-110.
20. Zang, X., P. S. Sullivan, R. A. Soslow, R. Waitz, V. E. Reuter, A. Wilton, H. T. Thaler, M. Arul, S. F. Slovin, J. Wei, et al. 2010. Tumor associated endothelial expression of B7-H3 predicts survival in ovarian carcinomas. Mod. Pathol. 23: 1104-1112.
21. Tringler, B., S. Zhuo, G. Pilkington, K. C. Torkko, M. Singh, M. S. Lucia, D. E. Heinz, J. Papkoff, and K. R. Shroyer. 2005. B7-h4 is highly expressed in ductal and lobular breast cancer. Clin. Cancer Res. 11: 1842-1848.
22. Graser, R. T., T. P. DiLorenzo, F. Wang, G. J. Christianson, H. D. Chapman, D. C. Roopenian, S. G. Nathenson, and D. V. Serreze. 2000. Identification of a CD8 T cell that can independently mediate autoimmune diabetes development in the complete absence of CD4 T cell helper functions. J. Immunol. 164: 3913-3918.
23. Gagnerault, M. C., J. J. Luan, C. Lotton, and F. Lepault. 2002. Pancreatic lymph nodes are required for priming of beta cell reactive T cells in NOD mice. J. Exp. Med. 196: 369-377.
24. Turley, S., L. Poirot, M. Hattori, C. Benoist, and D. Mathis. 2003. Physiological beta cell death triggers priming of self-reactive T cells by dendritic cells in a type-1 diabetes model. J. Exp. Med. 198: 1527-1537.
25. Zhang, Y., B. O'Brien, J. Trudeau, R. Tan, P. Santamaria, and J. P. Dutz. 2002. In situ beta cell death promotes priming of diabetogenic CD8 T lymphocytes. J. Immunol. 168: 1466-1472.
26. Thomas, H. E., J. A. Trapani, and T. W. Kay. 2010. The role of perforin and granzymes in diabetes. Cell Death Differ. 17: 577-585.
27. von Herrath, M. G., and M. B. Oldstone. 1997. Interferon-gamma is essential for destruction of beta cells and development of insulin-dependent diabetes mellitus. J. Exp. Med. 185: 531-539.
28. Kay, T.W., I. L. Campbell, L. Oxbrow, and L. C. Harrison. 1991. Overexpression of class I major histocompatibility complex accompanies insulitis in the nonobese diabetic mouse and is prevented by anti-interferon-gamma antibody. Diabetologia 34: 779-785.
29. Suk, K., S. Kim, Y. H. Kim, K. A. Kim, I. Chang, H. Yagita, M. Shong, and M. S. Lee. 2001. IFN-gamma/TNF-alpha synergism as the final effector in autoimmune diabetes: a key role for STAT1/IFN regulatory factor-1 pathway in pancreatic beta cell death. J. Immunol. 166: 4481-4489.
30. Kelchtermans, H., A. Billiau, and P. Matthys. 2008. How interferon-gamma keeps autoimmune diseases in check. Trends Immunol. 29: 479-486.
31. Flaishon, L., I. Topilski, D. Shoseyov, R. Hershkoviz, E. Fireman, Y. Levo, S. Marmor, and I. Shachar. 2002. Cutting edge: anti-inflammatory properties of low levels of IFN-gamma. J. Immunol. 168: 3707-3711.
32. Francisco, L. M., P. T. Sage, and A. H. Sharpe. 2010. The PD-1 pathway in tolerance and autoimmunity. Immunol. Rev. 236: 219-242.
33. Barber, D. L., E. J. Wherry, D. Masopust, B. Zhu, J. P. Allison, A. H. Sharpe, G. J. Freeman, and R. Ahmed. 2006. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439: 682-687.
34. Hofmeyer, K. A., H. Jeon, and X. Zang. 2011. The PD-1/PD-L1 (B7-H1) pathway in chronic infection-induced cytotoxic T lymphocyte exhaustion. J. Biomed. Biotechnol. 2011: 451694.
35. Parish, I. A., S. Rao, G. K. Smyth, T. Juelich, G. S. Denyer, G. M. Davey, A. Strasser, and W. R. Heath. 2009. The molecular signature of CD8+ T cells undergoing deletional tolerance. Blood 113: 4575-4585.
36. Kamimura, Y., H. Kobori, J. Piao, M. Hashiguchi, K. Matsumoto, S. Hirose, and M. Azuma. 2009. Possible involvement of soluble B7-H4 in T cell-mediated inflammatory immune responses. Biochem. Biophys. Res. Commun. 389: 349-353.
37. Hathcock, K. S., G. Laszlo, C. Pucillo, P. Linsley, and R. J. Hodes. 1994. Comparative analysis of B7-1 and B7-2 costimulatory ligands: expression and function. J. Exp. Med. 180: 631-640.
38. Prabhu Das, M. R., S. S. Zamvil, F. Borriello, H. L. Weiner, A. H. Sharpe, and V. K. Kuchroo. 1995. Reciprocal expression of co-stimulatory molecules, B7-1 and B7-2, on murine T cells following activation. Eur. J. Immunol. 25: 207-211.
39. Liang, L., E. M. Porter, and W. C. Sha. 2002. Constitutive expression of the B7h ligand for inducible costimulator on naive B cells is extinguished after activation by distinct B cell receptor and interleukin 4 receptor-mediated pathways and can be rescued by CD40 signaling. J. Exp. Med. 196: 97-108.
40. Aicher, A., M. Hayden-Ledbetter, W. A. Brady, A. Pezzutto, G. Richter, D. Magaletti, S. Buckwalter, J. A. Ledbetter, and E. A. Clark. 2000. Characterization of human inducible costimulator ligand expression and function. J. Immunol. 164: 4689-4696.
41. Yamazaki, T., H. Akiba, H. Iwai, H. Matsuda, M. Aoki, Y. Tanno, T. Shin, H. Tsuchiya, D. M. Pardoll, K. Okumura, et al. 2002. Expression of programmed death 1 ligands by murine T cells and APC. J. Immunol. 169: 5538-5545.
42. Ishida, M., Y. Iwai, Y. Tanaka, T. Okazaki, G. J. Freeman, N. Minato, and T. Honjo. 2002. Differential expression of PD-L1 and PD-L2, ligands for an inhibitory receptor PD-1, in the cells of lymphohematopoietic tissues. Immunol. Lett. 84: 57-62.
43. Liang, S. C., Y. E. Latchman, J. E. Buhlmann, M. F. Tomczak, B. H. Horwitz, G. J. Freeman, and A. H. Sharpe. 2003. Regulation of PD-1, PD-L1, and PD-L2 expression during normal and autoimmune responses. Eur. J. Immunol. 33: 2706-2716.
44. Mazanet, M. M., and C. C. Hughes. 2002. B7-H1 is expressed by human endothelial cells and suppresses T cell cytokine synthesis. J. Immunol. 169: 3581-3588.
45. Chapoval, A. I., J. Ni, J. S. Lau, R. A. Wilcox, D. B. Flies, D. Liu, H. Dong, G. L. Sica, G. Zhu, K. Tamada, and L. Chen. 2001. B7-H3: a costimulatory molecule for T cell activation and IFN-gamma production. Nat. Immunol. 2: 269-274.
46. Suh, W. K., B. U. Gajewska, H. Okada, M. A. Gronski, E. M. Bertram, W. Dawicki, G. S. Duncan, J. Bukczynski, S. Plyte, A. Elia, et al. 2003. The B7 family member B7-H3 preferentially down-regulates T helper type 1-mediated immune responses. Nat. Immunol. 4: 899-906.
47. Steinberger, P., O. Majdic, S. V. Derdak, K. Pfistershammer, S. Kirchberger, C. Klauser, G. Zlabinger, W. F. Pickl, J. Stöckl, and W. Knapp. 2004. Molecular characterization of human 4Ig-B7-H3, a member of the B7 family with four Iglike domains. J. Immunol. 172: 2352-2359.
48. Goodnow, C. C. 2007. Multistep pathogenesis of autoimmune disease. Cell 130: 25-35.
49. Walker, L. S., and A. K. Abbas. 2002. The enemy within: keeping self-reactive T cells at bay in the periphery. Nat. Rev. Immunol. 2: 11-19.
50. Redmond, W. L., and L. A. Sherman. 2005. Peripheral tolerance of CD8 T lymphocytes. Immunity 22: 275-284.
51. Wherry, E. J., S. J. Ha, S. M. Kaech, W. N. Haining, S. Sarkar, V. Kalia, S. Subramaniam, J. N. Blattman, D. L. Barber, and R. Ahmed. 2007. Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 27: 670-684.
52. Cameron, M. J., G. A. Arreaza, M. Grattan, C. Meagher, S. Sharif, M. D. Burdick, R. M. Strieter, D. N. Cook, and T. L. Delovitch. 2000. Differential expression of CC chemokines and the CCR5 receptor in the pancreas is associated with progression to type I diabetes. J. Immunol. 165: 1102-1110.
53. Hanifi-Moghaddam, P., S. Kappler, J. Seissler, S. Müller-Scholze, S. Martin, B. O. Roep, K. Strassburger, H. Kolb, and N. C. Schloot. 2006. Altered chemokine levels in individuals at risk of Type 1 diabetes mellitus. Diabet. Med. 23: 156-163.
54. Maurer, M., and E. von Stebut. 2004. Macrophage inflammatory protein-1. Int. J. Biochem. Cell Biol. 36: 1882-1886.
55. Wang, X., J. Hao, D. L. Metzger, Z. Ao, L. Chen, D. Ou, C. B. Verchere, A. Mui, and G. L. Warnock. 2012. B7-H4 Treatment of T cells inhibits ERK, JNK, p38, and AKT activation. PLoS ONE 7: e28232.
56. Yuan, C. L., J. F. Xu, J. Tong, H. Yang, F. R. He, Q. Gong, P. Xiong, L. Duan, M. Fang, Z. Tan, et al. 2009. B7-H4 transfection prolongs beta-cell graft survival. Transpl. Immunol. 21: 143-149.
57. Wang, X., J. Hao, D. L. Metzger, A. Mui, Z. Ao, C. B. Verchere, L. Chen, D. Ou, and G. L. Warnock. 2009. Local expression of B7-H4 by recombinant adenovirus transduction in mouse islets prolongs allograft survival. Transplantation 87: 482-490.
58. Wang, X., J. Hao, D. L. Metzger, A. Mui, Z. Ao, N. Akhoundsadegh, S. Langermann, L. Liu, L. Chen, D. Ou, et al. 2011. Early treatment of NOD mice with B7-H4 reduces the incidence of autoimmune diabetes. Diabetes 60: 3246-3255.