Kupffer cells support hepatitis B virus-mediated CD8+ T cell exhaustion via hepatitis B core antigen-TLR2 interactions in mice

Journal of Immunology

Volumn 195, Issue 7, 2015, Pages 3100-3109

  Li, Min ^a   Sun, Rui ^a,b,c   Xu, Long ^c   Yin, Wenwei ^c   Chen, Yongyan ^c   Zheng, Xiaodong ^c   Lian, Zhexiong ^a,c   Wei, Haiming ^a,c   Tian, Zhigang ^a,b,c  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; HEPATITIS B CORE ANTIGEN; HEPATITIS B SURFACE ANTIGEN; HEPATITIS B(E) ANTIGEN; INTERLEUKIN 10; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA; IL10 PROTEIN, MOUSE; INTERLEUKIN 10 RECEPTOR; TLR2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CELL COUNT; CELL DIFFERENTIATION; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; HEPATITIS B; HEPATITIS B VIRUS; HUMORAL IMMUNITY; HYDRODYNAMICS; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; IMMUNOSTIMULATION; KUPFFER CELL; MALE; MOUSE; NONHUMAN; PHENOTYPE; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PURIFICATION; QUANTITATIVE ANALYSIS; RADIOIMMUNOASSAY; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VIRUS CARRIER; ANIMAL; BIOSYNTHESIS; BONE MARROW CELL; C57BL MOUSE; DISEASE MODEL; GENETICS; HETEROZYGOTE; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; VIROLOGY;

ANIMALS; BONE MARROW CELLS; CARRIER STATE; CD8-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; HEPATITIS B CORE ANTIGENS; HEPATITIS B VIRUS; HEPATITIS B, CHRONIC; INTERLEUKIN-10; KUPFFER CELLS; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, INTERLEUKIN-10; TOLL-LIKE RECEPTOR 2;

EID: 84942465585     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500839     Document Type: Article

References (43)

1. Crispe, I. N. 2009. The liver as a lymphoid organ. Annu. Rev. Immunol. 27: 147-163.
2. Protzer, U., M. K. Maini, and P. A. Knolle. 2012. Living in the liver: hepatic infections. Nat. Rev. Immunol. 12: 201-213.
3. Guidotti, L. G., R. Rochford, J. Chung, M. Shapiro, R. Purcell, and F. V. Chisari. 1999. Viral clearance without destruction of infected cells during acute HBV infection. Science 284: 825-829.
4. Maini, M. K., C. Boni, C. K. Lee, J. R. Larrubia, S. Reignat, G. S. Ogg, A. S. King, J. Herberg, R. Gilson, A. Alisa, et al. 2000. The role of virus-specific CD8(+) cells in liver damage and viral control during persistent hepatitis B virus infection. J. Exp. Med. 191: 1269-1280.
5. Kong, X., R. Sun, Y. Chen, H. Wei, and Z. Tian. 2014. gdT cells drive myeloidderived suppressor cell-mediated CD8+ T cell exhaustion in hepatitis B virusinduced immunotolerance. J. Immunol. 193: 1645-1653.
6. Stross, L., J. Günther, G. Gasteiger, T. Asen, S. Graf, M. Aichler, I. Esposito, D. H. Busch, P. Knolle, T. Sparwasser, and U. Protzer. 2012. Foxp3+ regulatory T cells protect the liver from immune damage and compromise virus control during acute experimental hepatitis B virus infection in mice. Hepatology 56: 873-883.
7. Knolle, P., J. Schlaak, A. Uhrig, P. Kempf, K. H. Meyer zum Büschenfelde, and G. Gerken. 1995. Human Kupffer cells secrete IL-10 in response to lipopolysaccharide (LPS) challenge. J. Hepatol. 22: 226-229.
8. Kamei, T., M. P. Callery, and M. W. Flye. 1990. Kupffer cell blockade prevents induction of portal venous tolerance in rat cardiac allograft transplantation. J. Surg. Res. 48: 393-396.
9. Sato, K., K. Yabuki, T. Haba, and T. Maekawa. 1996. Role of Kupffer cells in the induction of tolerance after liver transplantation. J. Surg. Res. 63: 433-438.
10. Ju, C., J. P. McCoy, C. J. Chung, M. L. Graf, and L. R. Pohl. 2003. Tolerogenic role of Kupffer cells in allergic reactions. Chem. Res. Toxicol. 16: 1514-1519.
11. Xu, L., W. Yin, R. Sun, H. Wei, and Z. Tian. 2014. Kupffer cell-derived IL-10 plays a key role in maintaining humoral immune tolerance in hepatitis B viruspersistent mice. Hepatology 59: 443-452.
12. Nebbia, G., D. Peppa, A. Schurich, P. Khanna, H. D. Singh, Y. Cheng, W. Rosenberg, G. Dusheiko, R. Gilson, J. ChinAleong, et al. 2012. Upregulation of the Tim-3/galectin-9 pathway of T cell exhaustion in chronic hepatitis B virus infection. PLoS One 7: e47648.
13. Li, H., K.Wu, K. Tao, L. Chen, Q. Zheng, X. Lu, J. Liu, L. Shi, C. Liu, G. Wang, and W. Zou. 2012. Tim-3/galectin-9 signaling pathway mediates T-cell dysfunction and predicts poor prognosis in patients with hepatitis B virus-associated hepatocellular carcinoma. Hepatology 56: 1342-1351.
14. Bagheri, V., A. Askari, M. K. Arababadi, and D. Kennedy. 2014. Can Toll-Like Receptor (TLR) 2 be considered as a new target for immunotherapy against hepatitis B infection? Hum. Immunol. 75: 549-554.
15. Netea, M. G., J. W. Van der Meer, and B. J. Kullberg. 2004. Toll-like receptors as an escape mechanism from the host defense. Trends Microbiol. 12: 484-488.
16. Yang, H. Z., B. Cui, H. Z. Liu, S. Mi, J. Yan, H. M. Yan, F. Hua, H. Lin, W. F. Cai, W. J. Xie, et al. 2009. Blocking TLR2 activity attenuates pulmonary metastases of tumor. PLoS One 4: e6520.
17. Yamazaki, S., K. Okada, A. Maruyama, M. Matsumoto, H. Yagita, and T. Seya. 2011. TLR2-dependent induction of IL-10 and Foxp3+ CD25+ CD4+ regulatory T cells prevents effective anti-tumor immunity induced by Pam2 lipopeptides in vivo. PLoS One 6: e18833.
18. Cooper, A., G. Tal, O. Lider, and Y. Shaul. 2005. Cytokine induction by the hepatitis B virus capsid in macrophages is facilitated by membrane heparan sulfate and involves TLR2. J. Immunol. 175: 3165-3176.
19. Wu, J., M. Lu, Z. Meng, M. Trippler, R. Broering, A. Szczeponek, F. Krux, U. Dittmer, M. Roggendorf, G. Gerken, and J. F. Schlaak. 2007. Toll-like receptor-mediated control of HBV replication by nonparenchymal liver cells in mice. Hepatology 46: 1769-1778.
20. Isogawa, M., M. D. Robek, Y. Furuichi, and F. V. Chisari. 2005. Toll-like receptor signaling inhibits hepatitis B virus replication in vivo. J. Virol. 79: 7269-7272.
21. Kormann, M. S., R. Ferstl, M. Depner, N. Klopp, S. Spiller, T. Illig, C. Vogelberg, E. von Mutius, C. J. Kirschning, and M. Kabesch. 2009. Rare TLR2 mutations reduce TLR2 receptor function and can increase atopy risk. Allergy 64: 636-642.
22. Huang, L. R., H. L. Wu, P. J. Chen, and D. S. Chen. 2006. An immunocompetent mouse model for the tolerance of human chronic hepatitis B virus infection. Proc. Natl. Acad. Sci. USA 103: 17862-17867.
23. Xu, L., W. Yin, R. Sun, H. Wei, and Z. Tian. 2013. Liver type I regulatory T cells suppress germinal center formation in HBV-tolerant mice. Proc. Natl. Acad. Sci. USA 110: 16993-16998.
24. Wang, J., R. Sun, H. Wei, Z. Dong, B. Gao, and Z. Tian. 2006. Poly I:C prevents T cell-mediated hepatitis via an NK-dependent mechanism. J. Hepatol. 44: 446-454.
25. Hou, X., R. Zhou, H. Wei, R. Sun, and Z. Tian. 2009. NKG2D-retinoic acid early inducible-1 recognition between natural killer cells and Kupffer cells in a novel murine natural killer cell-dependent fulminant hepatitis. Hepatology 49: 940-949.
26. Zeng, Z., X. Kong, F. Li, H. Wei, R. Sun, and Z. Tian. 2013. IL-12-based vaccination therapy reverses liver-induced systemic tolerance in a mouse model of hepatitis B virus carrier. J. Immunol. 191: 4184-4193.
27. Wherry, E. J. 2011. T cell exhaustion. Nat. Immunol. 12: 492-499.
28. Lazdina, U., M. Alheim, J. Nyström, C. Hultgren, G. Borisova, I. Sominskaya, P. Pumpens, D. L. Peterson, D. R. Milich, and M. Sällberg. 2003. Priming of cytotoxic T cell responses to exogenous hepatitis B virus core antigen is B cell dependent. J. Gen. Virol. 84: 139-146.
29. Heymann, F., J. Peusquens, I. Ludwig-Portugall, M. Kohlhepp, C. Ergen, P. Niemietz, C. Martin, N. van Rooijen, J. C. Ochando, G. J. Randolph, et al. 2015. Liver inflammation abrogates immunological tolerance induced by Kupffer cells. Hepatology 62: 279-291.
30. Cullen, J. M., B. Faiola, D. H. Melich, R. A. Peterson, H. L. Jordan, C. L. Kimbrough, J. S. Prescott, and R. T. Miller. 2013. Effects of Kupffer cell depletion on acute alpha-naphthylisothiocyanate-induced liver toxicity in male mice. Toxicol. Pathol. 41: 7-17.
31. Publicover, J., A. Gaggar, S. Nishimura, C. M. Van Horn, A. Goodsell, M. O. Muench, R. L. Reinhardt, N. van Rooijen, A. E. Wakil, M. Peters, et al. 2013. Age-dependent hepatic lymphoid organization directs successful immunity to hepatitis B. J. Clin. Invest. 123: 3728-3739.
32. Wu, X., R. Sun, Y. Chen, X. Zheng, L. Bai, Z. Lian, H.Wei, and Z. Tian. 2015. Oral ampicillin inhibits liver regeneration by breaking hepatic innate immune tolerance normally maintained by gut commensal bacteria. Hepatology 62: 253-264.
33. Chen, Z., Y. Cheng, Y. Xu, J. Liao, X. Zhang, Y. Hu, Q. Zhang, J. Wang, Z. Zhang, F. Shen, and Z. Yuan. 2008. Expression profiles and function of Tolllike receptors 2 and 4 in peripheral blood mononuclear cells of chronic hepatitis B patients. Clin. Immunol. 128: 400-408.
34. Wei, X. Q., Z. F. Wen, F. P. Zheng, and J. L. Yao. 2007. [Changes of Toll-like receptor (TLR) 2 and TLR4 on the peripheral blood mononuclear cells in patients with chronic hepatitis B and chronic severe hepatitis B]. Zhonghua Gan Zang Bing Za Zhi 15: 354-357.
35. Zhang, X., Z. Ma, H. Liu, J. Liu, Z. Meng, R. Broering, D. Yang, J. F. Schlaak, M. Roggendorf, and M. Lu. 2012. Role of Toll-like receptor 2 in the immune response against hepadnaviral infection. J. Hepatol. 57: 522-528.
36. Sutmuller, R. P., M. H. den Brok, M. Kramer, E. J. Bennink, L. W. Toonen, B. J. Kullberg, L. A. Joosten, S. Akira, M. G. Netea, and G. J. Adema. 2006. Toll-like receptor 2 controls expansion and function of regulatory T cells. J. Clin. Invest. 116: 485-494.
37. Tu, Z., R. H. Pierce, J. Kurtis, Y. Kuroki, I. N. Crispe, and M. S. Orloff. 2010. Hepatitis C virus core protein subverts the antiviral activities of human Kupffer cells. Gastroenterology 138: 305-314.
38. Wang, S., Z. Chen, C. Hu, F. Qian, Y. Cheng, M. Wu, B. Shi, J. Chen, Y. Hu, and Z. Yuan. 2013. Hepatitis B virus surface antigen selectively inhibits TLR2 ligand-induced IL-12 production in monocytes/macrophages by interfering with JNK activation. J. Immunol. 190: 5142-5151.
39. Twu, J. S., C. H. Lee, P. M. Lin, and R. H. Schloemer. 1988. Hepatitis B virus suppresses expression of human beta-interferon. Proc. Natl. Acad. Sci. USA 85: 252-256.
40. Hyodo, N., I. Nakamura, and M. Imawari. 2004. Hepatitis B core antigen stimulates interleukin-10 secretion by both T cells and monocytes from peripheral blood of patients with chronic hepatitis B virus infection. Clin. Exp. Immunol. 135: 462-466.
41. Lin, Y. J., L. R. Huang, H. C. Yang, H. T. Tzeng, P. N. Hsu, H. L. Wu, P. J. Chen, and D. S. Chen. 2010. Hepatitis B virus core antigen determines viral persistence in a C57BL/6 mouse model. Proc. Natl. Acad. Sci. USA 107: 9340-9345.
42. Liu, F., Y. Song, and D. Liu. 1999. Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA. Gene Ther. 6: 1258-1266.
43. Ye, B., X. Liu, X. Li, H. Kong, L. Tian, and Y. Chen. 2015. T-cell exhaustion in chronic hepatitis B infection: current knowledge and clinical significance. Cell Death Dis. 6: e1694.