PD-L1 limits the mucosal CD8+ T cell response to chlamydia trachomatis

Journal of Immunology

Volumn 192, Issue 3, 2014, Pages 1079-1090

  Fankhauser, Sarah C ^a   Starnbach, Michael N ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIGAND; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN PD L1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL GROWTH; BACTERIUM DETECTION; BACTERIUM ISOLATION; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CHLAMYDIA TRACHOMATIS; CHLAMYDIASIS; CONTROLLED STUDY; FLOW CYTOMETRY; GENITAL SYSTEM; GENITAL TRACT INFECTION; LYMPHOCYTE DEPLETION; LYMPHOCYTE TRANSFER; MOUSE; MUCOSA; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTIGENS, CD274; ANTIGENS, CD80; CD8-POSITIVE T-LYMPHOCYTES; CERVIX UTERI; CHLAMYDIA INFECTIONS; CHLAMYDIA TRACHOMATIS; FEMALE; GENITAL DISEASES, FEMALE; HEMATOPOIETIC STEM CELLS; IMMUNE TOLERANCE; IMMUNITY, MUCOSAL; MICE; MICE, INBRED C57BL; MUCOUS MEMBRANE; RADIATION CHIMERA; T-LYMPHOCYTE SUBSETS; UTERUS;

EID: 84893344579     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301657     Document Type: Article

References (45)

1. Centers for Disease Control and Prevention. 2011. 2011 Sexually Transmitted Disease Surveillance. Department of Health and Human Services.
2. Paavonen, J., and W. Eggert-Kruse. 1999. Chlamydia trachomatis: impact on human reproduction. Hum. Reprod. Update 5: 433-447.
3. Starnbach, M. N., W. P. Loomis, P. Ovendale, D. Regan, B. Hess, M. R. Alderson, and S. P. Fling. 2003. An inclusion membrane protein from Chlamydia trachomatis enters the MHC class I pathway and stimulates a CD8+ T cell response. J. Immunol. 171: 4742-4749.
4. Loomis, W. P., and M. N. Starnbach. 2006. Chlamydia trachomatis infection alters the development of memory CD8+ T cells. J. Immunol. 177: 4021-4027.
5. Wherry, E. J., D. L. Barber, S. M. Kaech, J. N. Blattman, and R. Ahmed. 2004. Antigen-independent memory CD8 T cells do not develop during chronic viral infection. Proc. Natl. Acad. Sci. USA 101: 16004-16009.
6. 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.
7. Trautmann, L., F. M. Mbitikon-Kobo, J. P. Goulet, Y. Peretz, Y. Shi, J. Van Grevenynghe, F. A. Procopio, M. R. Boulassel, J. P. Routy, N. Chomont, et al. 2012. Profound metabolic, functional, and cytolytic differences characterize HIV-specific CD8 T cells in primary and chronic HIV infection. Blood 120: 3466-3477.
8. Yamamoto, T., D. A. Price, J. P. Casazza, G. Ferrari, M. Nason, P. K. Chattopadhyay,M. Roederer, E. Gostick, P. D. Katsikis, D. C. Douek, et al. 2011. Surface expression patterns of negative regulatory molecules identify determinants of virus-specific CD8+ T-cell exhaustion in HIV infection. Blood 117: 4805-4815.
9. Fourcade, J., Z. Sun, O. Pagliano, P. Guillaume, I. F. Luescher, C. Sander, J. M. Kirkwood, D. Olive, V. Kuchroo, and H. M. Zarour. 2012. CD8(+) T cells specific for tumor antigens can be rendered dysfunctional by the tumor microenvironment through upregulation of the inhibitory receptors BTLA and PD-1. Cancer Res. 72: 887-896.
10. Jin, H. T., A. C. Anderson, W. G. Tan, E. E. West, S. J. Ha, K. Araki, G. J. Freeman, V. K. Kuchroo, and R. Ahmed. 2010. Cooperation of Tim-3 and PD-1 in CD8 T-cell exhaustion during chronic viral infection. Proc. Natl. Acad. Sci. USA 107: 14733-14738.
11. Richter, K., P. Agnellini, and A. Oxenius. 2010. On the role of the inhibitory receptor LAG-3 in acute and chronic LCMV infection. Int. Immunol. 22: 13-23.
12. Blackburn, S. D., H. Shin, W. N. Haining, T. Zou, C. J. Workman, A. Polley, M. R. Betts, G. J. Freeman, D. A. Vignali, and E. J. Wherry. 2009. Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat. Immunol. 10: 29-37.
13. Shin, H., and E. J. Wherry. 2007. CD8 T cell dysfunction during chronic viral infection. Curr. Opin. Immunol. 19: 408-415.
14. Latchman, Y. E., S. C. Liang, Y. Wu, T. Chernova, R. A. Sobel, M. Klemm, V. K. Kuchroo, G. J. Freeman, and A. H. Sharpe. 2004. PD-L1-deficient mice show that PD-L1 on T cells, antigen-presenting cells, and host tissues negatively regulates T cells. Proc. Natl. Acad. Sci. USA 101: 10691-10696.
15. Barber, D. L., K. D. Mayer-Barber, C. G. Feng, A. H. Sharpe, and A. Sher. 2011. CD4 T cells promote rather than control tuberculosis in the absence of PD-1-mediated inhibition. J. Immunol. 186: 1598-1607.
16. Coers, J., M. N. Starnbach, and J. C. Howard. 2009. Modeling infectious disease in mice: co-Adaptation and the role of host-specific IFNgamma responses. PLoS Pathog. 5: e1000333.
17. Gondek, D. C., A. J. Olive, G. Stary, and M. N. Starnbach. 2012. CD4+ T cells are necessary and sufficient to confer protection against Chlamydia trachomatis infection in the murine upper genital tract. J. Immunol. 189: 2441-2449.
18. Roan, N. R., and M. N. Starnbach. 2006. Antigen-specific CD8+ T cells respond to Chlamydia trachomatis in the genital mucosa. J. Immunol. 177: 7974-7979.
19. Day, C. L., D. E. Kaufmann, P. Kiepiela, J. A. Brown, E. S. Moodley, S. Reddy, E. W. Mackey, J. D. Miller, A. J. Leslie, C. DePierres, et al. 2006. PD-1 ex-pression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 443: 350-354.
20. Trautmann, L., L. Janbazian, N. Chomont, E. A. Said, S. Gimmig, B. Bessette, M. R. Boulassel, E. Delwart, H. Sepulveda, R. S. Balderas, et al. 2006. Upregulation of PD-1 expression on HIV-specific CD8+ T cells leads to reversible immune dysfunction. Nat. Med. 12: 1198-1202.
21. Golden-Mason, L., B. Palmer, J. Klarquist, J. A. Mengshol, N. Castelblanco, and H. R. Rosen. 2007. Upregulation of PD-1 expression on circulating and intrahepatic hepatitis C virus-specific CD8+ T cells associated with reversible immune dysfunction. J. Virol. 81: 9249-9258.
22. Maier, H., M. Isogawa, G. J. Freeman, and F. V. Chisari. 2007. PD-1:PD-L1 interactions contribute to the functional suppression of virus-specific CD8+ T lymphocytes in the liver. J. Immunol. 178: 2714-2720.
23. Peng, B., C. Lu, L. Tang, I. T. Yeh, Z. He, Y. Wu, and G. Zhong. 2011. Enhanced upper genital tract pathologies by blocking Tim-3 and PD-L1 signaling pathways in mice intravaginally infected with Chlamydia muridarum. BMC Infect. Dis. 11: 347.
24. Keir, M. E., S. C. Liang, I. Guleria, Y. E. Latchman, A. Qipo, L. A. Albacker, M. Koulmanda, G. J. Freeman, M. H. Sayegh, and A. H. Sharpe. 2006. Tissue expression of PD-L1 mediates peripheral T cell tolerance. J. Exp. Med. 203: 883-895.
25. Iwai, Y., M. Ishida, Y. Tanaka, T. Okazaki, T. Honjo, and N. Minato. 2002. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc. Natl. Acad. Sci. USA 99: 12293-12297.
26. Rodig, N., T. Ryan, J. A. Allen, H. Pang, N. Grabie, T. Chernova, E. A. Greenfield, S. C. Liang, A. H. Sharpe, A. H. Lichtman, and G. J. Freeman. 2003. Endothelial expression of PD-L1 and PD-L2 down-regulates CD8+ T cell activation and cytolysis. Eur. J. Immunol. 33: 3117-3126.
27. Paterson, A. M., K. E. Brown, M. E. Keir, V. K. Vanguri, L. V. Riella, A. Chandraker, M. H. Sayegh, B. R. Blazar, G. J. Freeman, and A. H. Sharpe. 2011. The programmed death-1 ligand 1:B7-1 pathway restrains diabetogenic effector T cells in vivo. J. Immunol. 187: 1097-1105.
28. Bachmann, M. F., P. Wolint, K. Schwarz, P. Jager, and A. Oxenius. 2005. Functional properties and lineage relationship of CD8+ T cell subsets identified by expression of IL-7 receptor alpha and CD62L. J. Immunol. 175: 4686-4696.
29. Sallusto, F., D. Lenig, R. Fo rster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401: 708-712.
30. Masopust, D., V. Vezys, A. L. Marzo, and L. Lefrançois. 2001. Preferential localization of effector memory cells in nonlymphoid tissue. Science 291: 2413-2417.
31. Erickson, J. J., P. Gilchuk, A. K. Hastings, S. J. Tollefson, M. Johnson, M. B. Downing, K. L. Boyd, J. E. Johnson, A. S. Kim, S. Joyce, and J. V. Williams. 2012. Viral acute lower respiratory infections impair CD8+ T cells through PD-1. J. Clin. Invest. 122: 2967-2982.
32. Abiko, K., M. Mandai, J. Hamanishi, Y. Yoshioka, N. Matsumura, T. Baba, K. Yamaguchi, R. Murakami, A. Yamamoto, B. Kharma, et al. 2013. PD-L1 on tumor cells is induced in ascites and promotes peritoneal dissemination of ovarian cancer through CTL dysfunction. Clin. Cancer Res. 19: 1363-1374.
33. Rowe, J. H., T. M. Johanns, J. M. Ertelt, and S. S. Way. 2008. PDL-1 blockade impedes T cell expansion and protective immunity primed by attenuated Listeria monocytogenes. J. Immunol. 180: 7553-7557.
34. Seo, S. K., H. Y. Jeong, S. G. Park, S. W. Lee, I. W. Choi, L. Chen, and I. Choi. 2008. Blockade of endogenous B7-H1 suppresses antibacterial protection after primary Listeria monocytogenes infection. Immunology 123: 90-99.
35. Wang, J., G. Roderiquez, and M. A. Norcross. 2012. Control of adaptive immune responses by Staphylococcus aureus through IL-10, PD-L1, and TLR2. Sci. Rep. 2: 606.
36. Murthy, A. K., W. Li, B. K. Chaganty, S. Kamalakaran, M. N. Guentzel, J. Seshu, T. G. Forsthuber, G. Zhong, and B. P. Arulanandam. 2011. Tumor necrosis factor alpha production from CD8+ T cells mediates oviduct pathological sequelae following primary genital Chlamydia muridarum infection. Infect. Immun. 79: 2928-2935.
37. Kimani, J., I. W. Maclean, J. J. Bwayo, K. MacDonald, J. Oyugi, G. M. Maitha, R. W. Peeling, M. Cheang, N. J. Nagelkerke, F. A. Plummer, and R. C. Brunham. 1996. Risk factors for Chlamydia trachomatis pelvic inflammatory disease among sex workers in Nairobi, Kenya. J. Infect. Dis. 173: 1437-1444.
38. Trimble, C. L., R. A. Clark, C. Thoburn, N. C. Hanson, J. Tassello, D. Frosina, F. Kos, J. Teague, Y. Jiang, N. C. Barat, and A. A. Jungbluth. 2010. Human papillomavirus 16-Associated cervical intraepithelial neoplasia in humans excludes CD8 T cells from dysplastic epithelium. J. Immunol. 185: 7107-7114.
39. Wherry, E. J., V. Teichgraber, T. C. Becker, D. Masopust, S. M. Kaech, R. Antia, U. H. von Andrian, and R. Ahmed. 2003. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat. Immunol. 4: 225-234.
40. Klonowski, K. D., A. L. Marzo, K. J. Williams, S. J. Lee, Q. M. Pham, and L. Lefrançois. 2006. CD8 T cell recall responses are regulated by the tissue tropism of the memory cell and pathogen. J. Immunol. 177: 6738-6746.
41. Bachmann, M. F., P. Wolint, K. Schwarz, and A. Oxenius. 2005. Recall proliferation potential of memory CD8+ T cells and antiviral protection. J. Immunol. 175: 4677-4685.
42. Casey, K. A., K. A. Fraser, J. M. Schenkel, A. Moran, M. C. Abt, L. K. Beura, P. J. Lucas, D. Artis, E. J. Wherry, K. Hogquist, et al. 2012. Antigen-independent differentiation and maintenance of effector-like resident memory T cells in tissues. J. Immunol. 188: 4866-4875.
43. Cheroutre, H., and L. Madakamutil. 2005. Mucosal effector memory T cells: the other side of the coin. Cell. Mol. Life Sci. 62: 2853-2866.
44. Roberts, A. D., and D. L. Woodland. 2004. Cutting edge: effector memory CD8+ T cells play a prominent role in recall responses to secondary viral infection in the lung. J. Immunol. 172: 6533-6537.
45. 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.