The role of intrahepatic CD8+ T cell trapping and NK1.1+ cells in liver-mediated immune regulation

Clinical Immunology

Volumn 111, Issue 1, 2004, Pages 82-92

  Shibolet, Oren ^a   Alper, Ruslana ^a   Zolotarov, Lydia ^a   Trop, Shivti ^a   Thalenfeld, Barbara ^b   Engelhardt, Dean ^b   Rabbani, Elazar ^b   Ilan, Yaron ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b Enzon Incorporated   (United States)

Author keywords

2,4,6 trinitrobenzenesulfonic acid; Experimental colitis; IFN ; Interferon ; LAL; Liver associated lymphocytes; NK1.1 T cells; Oral tolerance; TGF 1; TNBS; TNF ; Transforming growth factor 1; Tumor necrosis factor

Indexed keywords

ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 4; TRINITROBENZENESULFONIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENVIRONMENTAL FACTOR; ENZYME LINKED IMMUNOSORBENT ASSAY; EVALUATION; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOREGULATION; INFLAMMATION; MALE; MICROSCOPY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SCORING SYSTEM; T LYMPHOCYTE; TISSUE SECTION;

ANIMALS; ANTIGENS; ANTIGENS, SURFACE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; COLITIS; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNE TOLERANCE; KILLER CELLS, NATURAL; LECTINS, C-TYPE; LIVER; MALE; MICE; MICE, INBRED C57BL; PROTEINS; TRINITROBENZENESULFONIC ACID;

EID: 1842735264     PISSN: 15216616     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.clim.2003.12.001     Document Type: Article

References (51)

1. Crispe I.N., Mehal W.Z. Strange brew: T cells in the liver. Immunol. Today. 17:1996;522-525.
2. Crispe I.N., Dao T., Klugewitz K., Mehal W.Z., Metz D.P. The liver as a site of T-cell apoptosis: graveyard, or killing field? Immunol. Rev. 174:2000;47-62.
3. Crispe I.N. Isolation of mouse intrahepatic lymphocytes. Curr. Protoc. Immunol. 3:1996;22-28.
4. Winnock M. Human liver-associated lymphocytes: an overview. J. Gastroenterol. Hepatol. 10:1995;43-46.
5. Godfrey D.J., Hammond K.J., Poulon L.D., Smyth M.J., Baxter A.G. NKT cells: facts, functions and fallacies. Immunol. Today. 21:2000;573-583.
6. Abo T., Kawamura T., Wataanabe H. Physiological responses of extrathymic T cells in the liver. Immunol. Rev. 174:2000;135-149.
7. MacDonaland R.H. NK1.1+ T cells: new clues to their origin, specificity and function. J. Exp. Med. 182:1995;633-638.
8. Bendelac A., Rivera M.N., Park S.-H., Roark J.H. Mouse CD1 specific NK1 T cells: development, specificity and function. Annu. Rev. Immunol. 15:1997;535-562.
9. Huang L., Soldevila G., Leeker M., Flavell R.A., Crispe I.N. Liver is the site of T cell destruction during peripheral deletion. Immunity. 1:1994;741-749.
10. Mehal W.Z., Juedes A., Crispe I.N. Selective retention of activated CD8+ T cells by the normal liver. J. Immunol. 163:1999;3202-3210.
11. Renno T., Hahne M., Tschopp J., MacDonald H.R. Peripheral T cells undergoing superantigen-induced apoptosis in vivo express B220 and upregulate Fas and Fas ligand. J. Exp. Med. 183:1996;431-437.
12. Iwakoshi N.N., Goldschneider I., Tausche E., Mordes J.P., Rossini A.A. High frequency apoptosis of recent thymic emigrants in the liver of lymphopenic diabetes-prone BioBreeding rats. J. Immunol. 161:1998;5838-5850.
13. Huang L., Crispe I.N. Superantigen-driven peripheral deletion of T cells. Deletion occurs in cells which have lost the T cell antigen receptor. J. Immunol. 151:1993;184-185.
14. Neurath M., Kelasall B.L., Presky D.H., Waegell W., Strober W. Experimental granulomatous colitis in mice is abrogated by induction of TGFβ-mediated oral tolerance. J. Exp. Med. 183:1996;2605-2616.
15. Ilan Y., Weksler-Zangen S., Ben-Horin S., Diment J., Sauter B., Rabbani E., Engelhardt D., Roy Chowdhury N., Roy Chowdhury J., Goldin E. Treatment of experimental colitis by oral tolerance induction: a central role for suppressor lymphocytes. Am. J. Gastroenterol. 95:2000;966-973.
16. Trop S., Samsonov D., Gotsman I., Alper R., Diment J., Ilan Y. Liver associated lymphocytes expressing NK1.1 are essential for oral tolerance induction in a murine model. Hepatology. 27:1999;746-755.
17. Shibolet O., Menachem Y., Kolker O., Alper R., Avraham Y., Thalenfeld B., Engelhardt D., Rabbani E., Berry E.M., Ilan Y. The role of NK1.1+ liver associated lymphocytes in peripheral immunomodulation of experimental colitis via oral tolerance or diet restriction. Gastroenterology. 120:2001;690.
18. De-Moraes L., Moreau M.C., Arnould G., Machavoine A.et al. IL4 producing NK T cells are biased towards IFNg production by IL12. Influence of the microenvironment on the functional capacities of NK T cells. Eur. J. Immunol. 28:1998;1507-1515.
19. Russell J.Q., Morrissette M., Weidner, Budd R.C. Liver damage preferentially results from CD8+ T cells triggered by high affinity peptide antigens. J. Exp. Med. 188:1998;1147-1157.
20. Belz G.T., Altrnan J.D., Doherty P.C. Characteristics of virus-specific CD8+ T cells in the liver during the control and resolution phases of influenza pneumonia. Proc. Natl. Acad. Sci. U. S. A. 95:1998;13812-13817.
21. Ni R.et al. Fas-mediated apoptosis in primary cultured mouse hepatocytes. Exp. Cell Res. 215:1994;332-337.
22. Bonfoco E.et al. Inducible nonlymphoid expression of Fas ligand is responsible for superantigen-induced peripheral deletion of T cells. Immunity. 9:1998;711-720.
23. Morita M., Watanabe Y., Akaike T. Inflammatory cytokines upregulate intercellular adhesion molecule-1 expression on primary cultured hepatocytes and T-lymphocyte adhesion. Hepatology. 19:1994;426-431.
24. El-Wahsh M., Fuller B., Burroughs A.K., Dhillon P.A., Rolles K.D. Correlation of ICAM-1 expression with post-operative acute cellular rejection in human liver allograft. Biochem. Trans. 25:1997;5005.
25. Mizoguchi A., Mizoguchi E., Chiba C., Spiekermann G.M., Tonegawa S., Anderson C.N., Bhan A.K. Cytokine imbalance and autoantibody production in T cell receptor-mutant mice with inflammatory bowel disease. J. Exp. Med. 183:1996;847-856.
26. Strober W., Kelsall B., Fuss L., Marth T., Ludviksson B., Ehrhardt R., Neurath M. Reciprocal IFNγ and TGFβ responses regulate the occurrence of mucosal inflammation. Immunol. Today. 18:1997;61-64.
27. Strobel S., Mowat A.M. Immune response to dietary antigens: oral tolerance. Immunol. Today. 4:1998;173-181.
28. Ilan Y., Prakash R., Davidson A., Jona V.K., Droguett G., Horwitz M.S., Roy Chowdhury N., Roy Chowdhury J. Oral tolerization to adenoviral antigens permits long term gene expression using recombinant adenoviral vectors. J. Clin. Invest. 99:1997;1098-1106.
29. Ilan Y., Sauter B., Roy Chowdhury N., Reddy B.V.N., Thummala N.R., Droguett G., Davidson A., Ott M., Horwitz M.S., Roy Chowdhury J. Oral tolerization to adenoviral proteins permits repeated adenovirus-mediated gene therapy in rats with pre-existing immunity to adenovirus. Hepatology. 27:1998;1368-1376.
30. Weiner H.L., Mackin G.A., Matsui M., Orav E.J., Khoury S.J., Dawson D.M., Hafler D.A. Double blind pilot trial of oral tolerization with myelin antigen in multiple sclerosis. Science. 261:1993;1321-1324.
31. Doherty D.G., Norris S., Collins C., McEntee G., Traynor O., Hegarty J., O'Farrelly C. Natural T cells in the human liver: cytotoxic lymphocytes with dual T cell and natural killer cell phenotype and function are phenotypically heterogeneous and include Vα24-JαQ and γδ T cell receptor bearing cells. Hum. Immunol. 60:1999;20-31.
32. Doherty D.G., Norris S., Madrigal-Estebas L., McEntee G., Traynor O., Hegarty J.E., O'Farrelly C. The human liver contains multiple population of NK cells, T cells, and CD3+CD56+ natural T cells with distinct cytotoxic activities and Th1, Th2, and Th0 cytokine secretion patterns. J. Immunol. 163:1999;2314-2321.
33. Chen Y.H., Chiu N.M., Mandal M., Wang N., Wang C.R. Impaired NK1.1+ T cell development and early IL4 production in CD1-deficient mice. Immunity. 6:1997;459-467.
34. Ebrel G., Lees R., Smiley S.T., Taniuchi M., Grusby M.J., MacDonald H.R. Tissue-specific segregation of CD1d-dependent and CD1d-independent NK T cells. J. Immunol. 162:1999;6410-6419.
35. Mendiratta S.K., Martin W.D., Hong S., Boesteanu A., Joyce S., Van Kaer L. CD1d1 mutant mice are deficient in natural T cells that promptly produce IL4. Immunity. 6:1997;469-477.
36. Chen H., Paul W.E. Cultured NK1.1+ CD4+ T cells produce large amounts of IL.4 and IFN upon activation by anti, CD3 or CD1. J. Immunol. 159:1997;2240-2249.
37. Arase H., Arase N., Saito T. IFNγ production by NK cells and NK1.1+T cells upon NKR-P1 cross-linking. J. Exp. Med. V. 183:1996;2391-2396.
38. Gotsman I., Jurim O., Trop S., Pappo O., Ilan Y. Effect of peripheral immune tolerance on liver-associated-T-lymphocytes expressing NK1.1. Transp. Proc. 32:2000;749-750.
39. Samsonov D., Trop S., Alper R., Diment J., Ilan Y. Enhancement of immune tolerance via induction of NK1.1 positive liver-associated-lymphocytes under immunosuppressive conditions in a murine model. J. Hepatol. 32:2000;812-820.
40. Lantz O., Sharara L.I., Tilloy F., Andersson A., DiSanto J.P. Lineage relationships and differentiation of natural killer (NK) T cells: intrathymic selection and interleukin (IL)-4 production in the absence of NKR-P1 and Ly49 molecules. J. Exp. Med. 185:1997;1395.
41. Kawamura T., Takeda K., Mendiratta S.K., Kawamura H., Van Kaer L., Yagita H., Abo T., Okumura K. Cutting edge: critical role of NK1+ T cells in IL-12-induced immune responses in vivo. J. Immunol. 160:1998;16.
42. Yoshimoto T., Bendelac A., Watson C., Hu-Li J., Paul W.E. Role of NK1.1+ T cells in a TH2 response and in immunoglobulin E production. Science. 270:1995;1845.
43. Yang Y., Bao M., Yoon J.W. Intrinsic defects in the T-cell lineage results in natural killer T-cell deficiency and the development of diabetes in the nonobese diabetic mouse. Diabetes. 12:2001;2691-2699.
44. Saubermann L.J., Beck P., De Jong Y.P., Pitman R.S., Ryan M.S., Kim H.S., Exley M., Snapper S., Balk S.P., Hagen S.J., Kanauchi O., Motoki K., Sakai T., Terhorst C., Koezuka Y., Podolsky D.K., Blumberg R.S. Activation of natural killer T cells by alpha-galactosylceramide in the presence of CD1d provides protection against colitis in mice. Gastroenterology. 119:2000;119-128.
45. Park S.H., Roark J.H., Bendelac A. Tissue-specific recognition of mouse CD1 molecules. J. Immunol. 160:1998;3128.
46. Brossay L., Tangri S., Bix M., Cardell S., Locksley R., Kronenberg M. Mouse CD1-autoreactive T cells have diverse patterns of reactivity to CD1+ targets. J. Immunol. 160:1998;3681.
47. Spada F.M., Koezuka Y., Porcelli S.A. CD1d-restricted recognition of synthetic glycolipid antigens by human natural killer T cells. J. Exp. Med. 188:1998;1529.
48. Brossay L., Chioda M., Burdin N., Koezuka Y., Casorati G., Dellabona P., Kronenberg M. CD1d-mediated recognition of an α-galactosylceramide by natural killer T cells is highly conserved through mammalian evolution. J. Exp. Med. 188:1998;1521.
49. Kawano T., Cui J., Koezuka Y., Toura I., Kaneko Y., Motoki K., Ueno H., Nakagawa R., Sato H., Kondo E., Koseki H., Taniguchi M. CD1d-restricted and TCR-mediated activation of Vα14 NKT cells by glycosylceramides. Science. 278:1997;1626.
50. Smiley S.T., Kaplan M.H., Grusby M.J. Immunoglobulin E production in the absence of interleukin-4-secreting CD1-dependent cells. Science. 275:1997;977.
51. Eberl G., Lees R., Smiley S.T.†, Taniguchi M., Grusby M.J., MacDonald H.R. Tissue-specific segregation of CD1d-dependent and CD1d-independent NK T cells. J. Immunol. 162:1999;6410-6419.