Intrahepatic IL-10 maintains NKG2A+Ly49- liver NK cells in a functionally hyporesponsive state

Journal of Immunology

Volumn 184, Issue 5, 2010, Pages 2693-2701

  Lassen, Matthew G ^a,b   Lukens, John R ^a,b   Dolina, Joseph S ^a,b   Brown, Michael G ^a,b   Hahn, Young S ^a,b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR; INTERLEUKIN 12; INTERLEUKIN 18; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY A; NATURAL KILLER CELL RECEPTOR NKG2A; GRANZYME; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY C;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; IMMUNE RESPONSE; IMMUNOSTIMULATION; IN VIVO STUDY; LIVER CELL; LYMPHOCYTE MIGRATION; LYMPHOCYTE SUBPOPULATION; LYMPHOCYTE TRANSFER; MOUSE; NATURAL KILLER CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING; SPLEEN CELL; ADOPTIVE TRANSFER; ANIMAL; C57BL MOUSE; CELL MOTION; CYTOTOXICITY; DRUG EFFECT; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; LIVER; METABOLISM; SPLEEN;

ADOPTIVE TRANSFER; ANIMALS; CELL MOVEMENT; CHEMOKINE CCL3; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; FLOW CYTOMETRY; GRANZYMES; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-12; INTERLEUKIN-18; KILLER CELLS, NATURAL; LIVER; MICE; MICE, INBRED C57BL; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY A; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY C; RECEPTORS, INTERLEUKIN-10; SPLEEN;

EID: 77951909054     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901362     Document Type: Article

References (52)

1. Andrews, D. M., A. A. Scalzo, W. M. Yokoyama, M. J. Smyth, and M. A. Degli-Esposti. 2003. Functional interactions between dendritic cells and NK cells during viral infection. Nat. Immunol. 4: 175-181.
2. Martín-Fontecha, A., L. L. Thomsen, S. Brett, C. Gerard, M. Lipp, A. Lanzavecchia, and F. Sallusto. 2004. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat. Immunol. 5: 1260-1265.
3. Lodoen, M. B., and L. L. Lanier. 2006. Natural killer cells as an initial defense against pathogens. Curr. Opin. Immunol. 18: 391-398.
4. Kim, S., K. Iizuka, H. S. Kang, A. Dokun, A. R. French, S. Greco, and W. M. Yokoyama. 2002. In vivo developmental stages in murine natural killer cell maturation. Nat. Immunol. 3: 523-528.
5. Dorfman, J. R., and D. H. Raulet. 1998. Acquisition of Ly49 receptor expression by developing natural killer cells. J. Exp. Med. 187: 609-618.
6. Sivakumar, P. V., A. Gunturi, M. Salcedo, J. D. Schatzle, W. C. Lai, Z. Kurepa, L. Pitcher, M. S. Seaman, F. A. Lemonnier, M. Bennett, et al. 1999. Cutting edge: expression of functional CD94/NKG2A inhibitory receptors on fetal NK1.1+Ly-49- cells: a possible mechanism of tolerance during NK cell development. J. Immunol. 162: 6976-6980.
7. Williams, N. S., A. Kubota, M. Bennett, V. Kumar, and F. Takei. 2000. Clonal analysis of NK cell development from bone marrow progenitors in vitro: orderly acquisition of receptor gene expression. Eur. J. Immunol. 30: 2074-2082.
8. Adams, D. H., B. Eksteen, and S. M. Curbishley. 2008. Immunology of the gut and liver: a love/hate relationship. Gut 57: 838-848.
9. Crispe, I. N. 2003. Hepatic T cells and liver tolerance. Nat. Rev. Immunol. 3: 51-62.
10. Bowen, D. G., G. W. McCaughan, and P. Bertolino. 2005. Intrahepatic immunity: a tale of two sites? Trends Immunol. 26: 512-517.
11. Goddard, S., J. Youster, E. Morgan, and D. H. Adams. 2004. Interleukin-10 secretion differentiates dendritic cells from human liver and skin. Am. J. Pathol. 164: 511-519.
12. Guidotti, L. G., and F. V. Chisari. 2006. Immunobiology and pathogenesis of viral hepatitis. Annu. Rev. Pathol. 1: 23-61.
13. Doherty, D. G., and C. O'Farrelly. 2000. Innate and adaptive lymphoid cells in the human liver. Immunol. Rev. 174: 5-20.
14. Klugewitz, K., F. Blumenthal-Barby, K. Eulenburg, M. Emoto, and A. Hamann. 2004. The spectrum of lymphoid subsets preferentially recruited into the liver reflects that of resident populations. Immunol. Lett. 93: 159-162.
15. Hamerman, J. A., K. Ogasawara, and L. L. Lanier. 2005. NK cells in innate immunity. Curr. Opin. Immunol. 17: 29-35.
16. Jinushi, M., T. Takehara, T. Tatsumi, S. Yamaguchi, R. Sakamori, N. Hiramatsu, T. Kanto, K. Ohkawa, and N. Hayashi. 2007. Natural killer cell and hepatic cell interaction via NKG2A leads to dendritic cell-mediated induction of CD4 CD25 T cells with PD-1-dependent regulatory activities. Immunology 120: 73-82.
17. Jinushi, M., T. Takehara, T. Tatsumi, T. Kanto, T. Miyagi, T. Suzuki, Y. Kanazawa, N. Hiramatsu, and N. Hayashi. 2004. Negative regulation of NK cell activities by inhibitory receptor CD94/NKG2A leads to altered NK cell-induced modulation of dendritic cell functions in chronic hepatitis C virus infection. J. Immunol. 173: 6072-6081. (Pubitemid 39487763)
18. Nattermann, J., G. Feldmann, G. Ahlenstiel, B. Langhans, T. Sauerbruch, and U. Spengler. 2006. Surface expression and cytolytic function of natural killer cell receptors is altered in chronic hepatitis C. Gut 55: 869-877. (Pubitemid 43764560)
19. Li, M. O., and R. A. Flavell. 2008. Contextual regulation of inflammation: a duet by transforming growth factor-beta and interleukin-10. Immunity 28: 468-476.
20. Moore, K. W., R. de Waal Malefyt, R. L. Coffman, and A. O'Garra. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19: 683-765.
21. Tu, Z., A. Bozorgzadeh, R. H. Pierce, J. Kurtis, I. N. Crispe, and M. S. Orloff. 2008. TLR-dependent cross talk between human Kupffer cells and NK cells. J. Exp. Med. 205: 233-244.
22. Degli-Esposti, M. A., and M. J. Smyth. 2005. Close encounters of different kinds: dendritic cells and NK cells take centre stage. Nat. Rev. Immunol. 5: 112-124.
23. Daniels, K. A., G. Devora, W. C. Lai, C. L.O'Donnell, M. Bennett, and R. M. Welsh. 2001. Murine cytomegalovirus is regulated by a discrete subset of natural killer cells reactive with monoclonal antibody to Ly49H. J. Exp. Med. 194: 29-44.
24. Takeda, K., E. Cretney, Y. Hayakawa, T. Ota, H. Akiba, K. Ogasawara, H. Yagita, K. Kinoshita, K. Okumura, and M. J. Smyth. 2005. TRAIL identifies immature natural killer cells in newborn mice and adult mouse liver. Blood 105: 2082-2089. (Pubitemid 40731795)
25. Hayakawa, Y., and M. J. Smyth. 2006. CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J. Immunol. 176: 1517-1524. (Pubitemid 43134295)
26. Fernandez, N. C., E. Treiner, R. E. Vance, A. M. Jamieson, S. Lemieux, and D. H. Raulet. 2005. A subset of natural killer cells achieves self-tolerance without expressing inhibitory receptors specific for self-MHC molecules. Blood 105: 4416-4423.
27. Kim, S., J. Poursine-Laurent, S. M. Truscott, L. Lybarger, Y. J. Song, L. Yang, A. R. French, J. B. Sunwoo, S. Lemieux, T. H. Hansen, and W. M. Yokoyama. 2005. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 436: 709-713. (Pubitemid 41117274)
28. Chaix, J., M. S. Tessmer, K. Hoebe, N. Fuséri, B. Ryffel, M. Dalod, L. Alexopoulou, B. Beutler, L. Brossay, E. Vivier, and T. Walzer. 2008. Cutting edge: priming of NK cells by IL-18. J. Immunol. 181: 1627-1631.
29. Zhang, T., K. Kawakami, M. H. Qureshi, H. Okamura, M. Kurimoto, and A. Saito. 1997. Interleukin-12 (IL-12) and IL-18 synergistically induce the fungicidal activity of murine peritoneal exudate cells against Cryptococcus neoformans through production of gamma interferon by natural killer cells. Infect. Immun. 65: 3594-3599.
30. Nakanishi, K., T. Yoshimoto, H. Tsutsui, and H. Okamura. 2001. Interleukin-18 regulates both Th1 and Th2 responses. Annu. Rev. Immunol. 19: 423-474.
31. Pillarisetty, V. G., A. B. Shah, G. Miller, J. I. Bleier, and R. P. DeMatteo. 2004. Liver dendritic cells are less immunogenic than spleen dendritic cells because of differences in subtype composition. J. Immunol. 172: 1009-1017.
32. + hepatic dendritic cells in the induction of innate immune responses. Clin. Exp. Immunol. 149: 335-343.
33. Xia, S., Z. Guo, X. Xu, H. Yi, Q. Wang, and X. Cao. 2008. Hepatic microenvironment programs hematopoietic progenitor differentiation into regulatory dendritic cells, maintaining liver tolerance. Blood 112: 3175-3185.
34. Grant, L. R., Z. J. Yao, C. M. Hedrich, F. Wang, A. Moorthy, K. Wilson, D. Ranatunga, and J. H. Bream. 2008. Stat4-dependent, T-bet-independent regulation of IL-10 in NK cells. Genes Immun. 9: 316-327.
35. Maroof, A., L. Beattie, S. Zubairi, M. Svensson, S. Stager, and P. M. Kaye. 2008. Posttranscriptional regulation of II10 gene expression allows natural killer cells to express immunoregulatory function. Immunity 29: 295-305.
36. Salazar-Mather, T. P., T. A. Hamilton, and C. A. Biron. 2000. A chemokine-to-cytokine-to-chemokine cascade critical in antiviral defense. J. Clin. Invest. 105: 985-993.
37. Vosshenrich, C. A., S. I. Samson-Villéger, and J. P. Di Santo. 2005. Distinguishing features of developing natural killer cells. Curr. Opin. Immunol. 17: 151-158.
38. Della Chiesa, M., M. Vitale, S. Carlomagno, G. Ferlazzo, L. Moretta, and A. Moretta. 2003. The natural killer cell-mediated killing of autologous dendritic cells is confined to a cell subset expressing CD94/NKG2A, but lacking inhibitory killer Ig-like receptors. Eur. J. Immunol. 33: 1657-1666.
39. Buelens, C., F. Willems, A. Delvaux, G. Piérard, J. P. Delville, T. Velu, and M. Goldman. 1995. Interleukin-10 differentially regulates B7-1 (CD80) and B7-2 (CD86) expression on human peripheral blood dendritic cells. Eur. J. Immunol. 25: 2668-2672.
40. Ding, L., P. S. Linsley, L. Y. Huang, R. N. Germain, and E. M. Shevach. 1993. IL-10 inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression. J. Immunol. 151: 1224-1234. (Pubitemid 23219258)
41. Demangel, C., P. Bertolino, and W. J. Britton. 2002. Autocrine IL-10 impairs dendritic cell (DC)-derived immune responses to mycobacterial infection by suppressing DC trafficking to draining lymph nodes and local IL-12 production. Eur. J. Immunol. 32: 994-1002.
42. Aste-Amezaga, M., X. Ma, A. Sartori, and G. Trinchieri. 1998. Molecular mechanisms of the induction of IL-12 and its inhibition by IL-10. J. Immunol. 160: 5936-5944. (Pubitemid 28298054)
43. Pascal, V., N. R. Nathan, E. Claudio, U. Siebenlist, and S. K. Anderson. 2007. NF-kappa B p50/p65 affects the frequency of Ly49 gene expression by NK cells. J. Immunol. 179: 1751-1759.
44. Yoshidome, H., A. Kato, M. J. Edwards, and A. B. Lentsch. 1999. Interleukin-10 inhibits pulmonary NF-kappaB activation and lung injury induced by hepatic ischemia-reperfusion. Am. J. Physiol. 277: L919-L923.
45. Li, X., D. Klintman, T. Sato, G. Hedlund, R. Schramm, B. Jeppsson, and H. Thorlacius. 2004. Interleukin-10 mediates the protective effect of Linomide by reducing CXC chemokine production in endotoxin-induced liver injury. Br. J. Pharmacol. 143: 865-871.
46. De Creus, A., M. Abe, A. H. Lau, H. Hackstein, G. Raimondi, and A. W. Thomson. 2005. Low TLR4 expression by liver dendritic cells correlates with reduced capacity to activate allogeneic T cells in response to endotoxin. J. Immunol. 174: 2037-2045.
47. You, Q., L. Cheng, R. M. Kedl, and C. Ju. 2008. Mechanism of T cell tolerance induction by murine hepatic Kupffer cells. Hepatology 48: 978-990.
48. Corado, J., F. Toro, H. Rivera, N. E. Bianco, L. Deibis, and J. B. De Sanctis. 1997. Impairment of natural killer (NK) cytotoxic activity in hepatitis C virus (HCV) infection. Clin. Exp. Immunol. 109: 451-457.
49. De Maria, A., M. Fogli, S. Mazza, M. Basso, A. Picciotto, P. Costa, S. Congia, M. C. Mingari, and L. Moretta. 2007. Increased natural cytotoxicity receptor expression and relevant IL-10 production in NK cells from chronically infected viremic HCV patients. Eur. J. Immunol. 37: 445-455.
50. Meier, U. C., R. E. Owen, E. Taylor, A. Worth, N. Naoumov, C. Willberg, K. Tang, P. Newton, P. Pellegrino, I. Williams, et al. 2005. Shared alterations in NK cell frequency, phenotype, and function in chronic human immunodeficiency virus and hepatitis C virus infections. J. Virol. 79: 12365-12374.
51. Golden-Mason, L., and H. R. Rosen. 2006. Natural killer cells: primary target for hepatitis C virus immune evasion strategies? Liver Transpl. 12: 363-372.
52. Khakoo, S. I., C. L. Thio, M. P. Martin, C. R. Brooks, X. Gao, J. Astemborski, J. Cheng, J. J. Goedert, D. Vlahov, M. Hilgartner, et al. 2004. HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science 305: 872-874.