HCV-infected hepatocytes drive CD4+CD25+Foxp3+ regulatory T-cell development through the Tim-3/Gal-9 pathway

European Journal of Immunology

Volumn 43, Issue 2, 2013, Pages 458-467

  Ji, Xiao J ^a,b   Ma, Cheng J ^a   Wang, Jia M ^a,c   Wu, Xiao Y ^a   Niki, Toshiro ^d   Hirashima, Mitsumi ^e   Moorman, Jonathan P ^a,f   Yao, Zhi Q ^a,f  

^a East Tennessee State University   (United States)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c SOOCHOW UNIVERSITY   (China)

^d GalPharma Co Ltd   (Japan)

^e KAGAWA UNIVERSITY   (Japan)

^f VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Gal 9; HCV; Hepatocytes; Immune modulation; Tim 3

Indexed keywords

CELL PROTEIN; ECALECTIN; GAMMA INTERFERON; INTERLEUKIN 10; TIM 3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CD25+ FOXP3+ REGULATORY T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; HEPATITIS C; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; UPREGULATION; VIRAL CLEARANCE;

CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; COCULTURE TECHNIQUES; FORKHEAD TRANSCRIPTION FACTORS; GALECTINS; HEPACIVIRUS; HEPATITIS C, CHRONIC; HEPATOCYTES; HUMANS; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; MEMBRANE PROTEINS; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA;

EID: 84873702305     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201242768     Document Type: Article

References (28)

1. Shepard, C. W., Finelli, L. and Alter, M. J., Global epidemiology of hepatitis C virus infection. Lancet Infect. Dis. 2005. 5: 558-567.
2. Walker, C. M., Adaptive immunity to the hepatitis C virus. Adv. Virus Res. 2010. 78: 43-86.
3. Belkaid, Y. and Chen, W., Regulatory ripples. Nat. Immunol. 2010. 11: 1077-1078.
4. Hori, S., Nomura, T. and Sakaguchi, S., Control of regulatory T cell development by the transcription factor Foxp3. Science 2003. 299: 1057-1061.
5. + T regulatory cell-mediated suppression. Immunity 2009. 30: 636-645.
6. von Boehmer, H., Mechanisms of suppression by suppressor T cells. Nat. Immunol. 2005. 6: 338-344.
7. Gavin, M. A., Rasmussen, J. P., Fontenot, J. D., Vasta, V., Manganiello, V. C., Beavo, J. A. and Rudensky, A. Y., Foxp3-dependent programme of regulatory T-cell differentiation. Nature 2007. 445: 771-775.
8. Belkaid, Y., Regulatory T cells and infection: a dangerous necessity. Nat. Rev. Immunol. 2007. 7: 875-888.
9. Shevach, E. M., CD4+CD25+ suppressor T cells: more questions than answers. Nat. Rev. Immunol. 2002. 2: 389-400.
10. Nishimura, H. and Honjo, T., PD-1: an inhibitory immunoreceptor involved in peripheral tolerance. Trends Immunol. 2001. 22: 265-268.
11. Hafler, D. A. and Kuchroo, V., TIMs: central regulators of immune responses. J. Exp. Med. 2008. 205: 2699.
12. + HCV-specific human CTLs is associated with viral persistence, and its blockade restores hepatocyte-directed in vitro cytotoxicity. J. Clin. Invest. 2010. 1172: 4546-2557.
13. Vali, B., Jones, R. B., Sakhdari, A., Sheth, P. M., Clayton, K., Yue, F. Y., Gyenes, G. et al., HCV-specific T cells in HCV/HIV co-infection show elevated frequencies of dual Tim-3/PD-1 expression that correlate with liver disease progression. Eur. J. Immunol. 2010. 40: 2493-505.
14. Ni, L., Ma, C. J., Zhang, Y., Nandakumar, S., Zhang, C. L., Wu, X. Y., Borthwick, T. et al., PD-1 modulates regulatory T cells and suppresses T cell responses in HCV-associated lymphoma. Immunol. Cell Biol. 2011. 89: 535-539.
15. + Tregs by limiting STAT-5 phosphorylation in subjects chronically infected with HCV. J. Clin. Invest. 2009. 119: 551-564.
16. Moorman, J. P., Wang, J. M., Zhang, Y., Ji, X. J., Ma, C. J., Wu, X. Y., Jia, Z. S. et al., Tim-3 controls regulatory and effector T cell balance during HCV Infection. J. Immunol. 2012. 189: 755-766.
17. Mengshol, J. A., Golden-Mason, L., Arikawa, T., Smith, M., Niki, T., McWilliams, R., Randall, J. A. et al., A crucial role for Kupffer cell-derived galectin-9 in regulation of T cell immunity in hepatitis C infection. PLoS One 2010. 5: e9504.
18. Zhang, Y., Ma, C. J., Ni, L., Wu, X. Y., Atia, A. N., Thayer, P., Shanker, U. et al., Crosstalk between PD-1 and SOCS-1 in HCV core-mediated IL-12 suppression. J. Immunol. 2011. 186: 3093-103.
19. Zhang, Y., Ma, C. J., Wu, X. Y., Moorman, J. P. and Yao, Z. Q., A crucial role for Tim-3 in negative regulation of monocyte IL-12 production in chronic hepatitis C infection. PLoS One 2011. 6: e19664.
20. Sehrewat, S., Suryawanshi, A., Hirashima, M. and Rouse, B. T., Role of Tim-3/Galectin-9 inhibitory interaction in viral-induced immunopathology: shifting the balance toward regulators. J. Immunol. 2009. 182: 3191-3201.
21. Sehrawat, S., Reddy, P. B., Rajasagi, N., Suryawanshi, A., Hirashima, M. and Rouse, B. T., Galecint-9/Tim-3 interaction regulates virus-specific primary and memory CD8 T cell response. PLos Pathog. 2010. 6: e100082.
22. Seki, M., Oomizu, S., Sakata, K., Sakata, A., Arikawa, T., Watanable, K., Ito, K. et al., Galectin-9 suppresses the generation of Th17, promotes the induction of regulatory T cells, and regulates experimental autoimmune arthritis. Clin. Immunol. 2008. 127: 78-88.
23. + Tregs. J. Clin. Invest. 2012. 122: 2395-2404.
24. Marie, J. C., Letterio, J. J., Gavin, M. and Rudensky, A. Y., TGF-beta I maintains suppressor function and Foxp3 expression in CD4+CD25+ regulatory T cells. J. Exp. Med. 2005. 201: 1061-1067.
25. Murai, M., Turovskaya, O., Kim, G., Madan, R., Karp, C. L., Cheroutre, H. and Kronenberg, M., Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat. Immunol. 2009. 10: 1178-1184.
26. Kimura, T., Saito, T., Yoshimura, M., Yixuan, S., Baba, M., Ji, G., Muramatsu, M. et al., Association of transforming growth factor-beta I functional polymorphisms with natural clearance of hepatitis C virus. J. Infect. Dis. 2006. 193: 1371-1374.
27. + T cells through the production of TGF-β. PLoS One 2010. 5: e12154.
28. +Monocytes. J. Leukoc. Biol. 2011. 91: 189-196.