A bidirectional crosstalk between iNKT cells and adipocytes mediated by leptin modulates susceptibility for T cell mediated hepatitis

Journal of Hepatology

Volumn 60, Issue 1, 2014, Pages 175-182

  Venken, Koen ^a   Seeuws, Sylvie ^a   Zabeau, Lennart ^a   Jacques, Peggy ^a   Decruy, Tine ^a   Coudenys, Julie ^a   Verheugen, Eveline ^a   Windels, Fien ^a   Catteeuw, Dominiek ^a   Drennan, Michael ^a   Van Calenbergh, Serge ^a   Lambrecht, Bart N ^a   Yoshimura, Akihiko ^b,c   Tavernier, Jan ^a   Elewaut, Dirk ^a  

^a GHENT UNIVERSITY   (Belgium)

^b KEIO UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Adipokines; ConA; Immunology; Immunometabolism; Liver pathology

Indexed keywords

CD3 ANTIBODY; INSULIN; JANUS KINASE 2; LEPTIN; LEPTIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; NANOBODY; CYTOKINE; INTERLEUKIN 12; INTERLEUKIN 18; MESSENGER RNA;

ADIPOCYTE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL INTERACTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HEPATITIS; INSULIN RESISTANCE; METABOLIC PARAMETERS; MOLECULAR MECHANICS; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; WILD TYPE; ANIMAL EXPERIMENT; LIVER HISTOLOGY; LYMPHOCYTE PROLIFERATION; NATURAL KILLER T CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE ACTIVATION;

ADIPOKINES; ALANINE AMINOTRANSFERASE; ALT; ASPARTATE AMINOTRANSFERASE; AST; CONA; CONCANAVALIN A; IMMUNOLOGY; IMMUNOMETABOLISM; INKT CELL; INVARIANT NATURAL KILLER T CELL; LEPTIN RECEPTOR; LIVER PATHOLOGY; LR; MALB; MAPK; MITOGEN-ACTIVATED PROTEIN KINASE; MOUSE SERUM ALBUMIN SPECIFIC NANOBODY; N.D.; NOT DETECTABLE; SOCS; SUPPRESSOR OF CYTOKINE SIGNALING; WAT; WHITE ADIPOSE TISSUE; Α-GALACTOSYLCERAMIDE; Α-GALCER;

ADIPOCYTES; ADIPOSE TISSUE; ANIMALS; CELL COMMUNICATION; DISEASE SUSCEPTIBILITY; HEPATITIS; LEPTIN; LYMPHOCYTE ACTIVATION; MAP KINASE SIGNALING SYSTEM; MICE; NATURAL KILLER T-CELLS; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, LEPTIN; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; T-LYMPHOCYTES;

EID: 84890559372     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2013.08.008     Document Type: Article

References (31)

1. N.R. Cohen, S. Garg, and M.B. Brenner Antigen presentation by CD1 lipids, T cells, and NKT cells in microbial immunity Adv Immunol 102 2009 1 94
2. D.I. Godfrey, D.G. Pellicci, O. Patel, L. Kjer-Nielsen, J. McCluskey, and J. Rossjohn Antigen recognition by CD1d-restricted NKT T cell receptors Semin Immunol 22 2010 61 67
3. D. Mathis, and S.E. Shoelson Immunometabolism: an emerging frontier Nat Rev Immunol 11 2011 81
4. L. Lynch, D. O'Shea, D.C. Winter, J. Geoghegan, D.G. Doherty, and C. O'Farrelly Invariant NKT cells and CD1d(+) cells amass in human omentum and are depleted in patients with cancer and obesity Eur J Immunol 39 2009 1893 1901
5. H.S. Schipper, M. Rakhshandehroo, S.F. van de Graaf, K. Venken, A. Koppen, and R. Stienstra Natural killer T cells in adipose tissue prevent insulin resistance J Clin Invest 122 2012 3343 3354
6. Y. Ji, S. Sun, A. Xu, P. Bhargava, L. Yang, and K.S. Lam Activation of natural killer T cells promotes M2 macrophage polarization in adipose tissue and improves systemic glucose tolerance via the IL-4/STAT6 signaling axis in obesity J Biol Chem 287 2012 13561 13571
7. M.E. Kotas, H.Y. Lee, M.P. Gillum, C. Annicelli, B.A. Guigni, and G.I. Shulman Impact of CD1d deficiency on metabolism PLoS One 6 2011 e25478
8. K. Ohmura, N. Ishimori, Y. Ohmura, S. Tokuhara, A. Nozawa, and S. Horii Natural killer T cells are involved in adipose tissues inflammation and glucose intolerance in diet-induced obese mice Arterioscler Thromb Vasc Biol 30 2010 193 199
9. L. Wu, V.V. Parekh, C.L. Gabriel, D.P. Bracy, P.A. Marks-Shulman, and R.A. Tamboli Activation of invariant natural killer T cells by lipid excess promotes tissue inflammation, insulin resistance, and hepatic steatosis in obese mice Proc Natl Acad Sci U S A 109 2012 E1143 E1152
10. L. Lynch, M. Nowak, B. Varghese, J. Clark, A.E. Hogan, and V. Toxavidis Adipose tissue invariant NKT cells protect against diet-induced obesity and metabolic disorder through regulatory cytokine production Immunity 37 2012 574 587
11. J.Y. Huh, J.I. Kim, Y.J. Park, I.J. Hwang, Y.S. Lee, and J.H. Sohn A novel function of adipocytes in lipid antigen presentation to iNKT cells Mol Cell Biol 33 2013 328 339
12. R.V. Considine, M.K. Sinha, M.L. Heiman, A. Kriauciunas, T.W. Stephens, and M.R. Nyce Serum immunoreactive-leptin concentrations in normal-weight and obese humans N Engl J Med 334 1996 292 295
13. D. Boillot, R. Assan, M. Dardenne, M. Bray-Sachs, and J.F. Bach T-lymphopenia and T-cell imbalance in diabetic db/db mice Diabetes 35 1986 198 203
14. J.K. Howard, G.M. Lord, G. Matarese, S. Vendetti, M.A. Ghatei, and M.A. Ritter Leptin protects mice from starvation-induced lymphoid atrophy and increases thymic cellularity in ob/ob mice J Clin Invest 104 1999 1051 1059
15. J. Cui, T. Shin, T. Kawano, H. Sato, E. Kondo, and I. Toura Requirement for Valpha14 NKT cells in IL-12-mediated rejection of tumors Science 278 1997 1623 1626
16. M. Nakaya, M. Hashimoto, R. Nakagawa, Y. Wakabayashi, T. Ishizaki, and I. Takada SOCS3 in T and NKT cells negatively regulates cytokine production and ameliorates ConA-induced hepatitis J Immunol 183 2009 7047 7053
17. L. Zabeau, A. Verhee, D. Catteeuw, L. Faes, S. Seeuws, and T. Decruy Selection of non-competitive leptin antagonists using a random nanobody-based approach Biochem J 441 2012 425 434
18. P. Jacques, K. Venken, B.K. Van, H. Hammad, S. Seeuws, and M.B. Drennan Invariant natural killer T cells are natural regulators of murine spondylarthritis Arthritis Rheum 62 2010 988 999
19. V. Laloux, L. Beaudoin, C. Ronet, and A. Lehuen Phenotypic and functional differences between NKT cells colonizing splanchnic and peripheral lymph nodes J Immunol 168 2002 3251 3258
20. Y. Kaneko, M. Harada, T. Kawano, M. Yamashita, Y. Shibata, and F. Gejyo Augmentation of Valpha14 NKT cell-mediated cytotoxicity by interleukin 4 in an autocrine mechanism resulting in the development of concanavalin A-induced hepatitis J Exp Med 191 2000 105 114
21. G.M. Lord, G. Matarese, J.K. Howard, S.R. Bloom, and R.I. Lechler Leptin inhibits the anti-CD3-driven proliferation of peripheral blood T cells but enhances the production of proinflammatory cytokines J Leukoc Biol 72 2002 330 338
22. E. Papathanassoglou, K. El-Haschimi, X.C. Li, G. Matarese, T. Strom, and C. Mantzoros Leptin receptor expression and signaling in lymphocytes: kinetics during lymphocyte activation, role in lymphocyte survival, and response to high fat diet in mice J Immunol 176 2006 7745 7752
23. H. Fei, H.J. Okano, C. Li, G.H. Lee, C. Zhao, and R. Darnell Anatomic localization of alternatively spliced leptin receptors (Ob-R) in mouse brain and other tissues Proc Natl Acad Sci U S A 94 1997 7001 7005
24. M.C. Leite-de-Moraes, A. Hameg, A. Arnould, F. Machavoine, Y. Koezuka, and E. Schneider A distinct IL-18-induced pathway to fully activate NK T lymphocytes independently from TCR engagement J Immunol 163 1999 5871 5876
25. V. De Rosa, C. Procaccini, G. Cali, G. Pirozzi, S. Fontana, and S. Zappacosta A key role of leptin in the control of regulatory T cell proliferation Immunity 26 2007 241 255
26. K. Takeda, Y. Hayakawa, K.L. Van, H. Matsuda, H. Yagita, and K. Okumura Critical contribution of liver natural killer T cells to a murine model of hepatitis Proc Natl Acad Sci U S A 97 2000 5498 5503
27. R. Faggioni, J. Jones-Carson, D.A. Reed, C.A. Dinarello, K.R. Feingold, and C. Grunfeld Leptin-deficient (ob/ob) mice are protected from T cell-mediated hepatotoxicity: role of tumor necrosis factor alpha and IL-18 Proc Natl Acad Sci U S A 97 2000 2367 2372
28. M.E. Gove, D.H. Rhodes, M. Pini, J.W. van Baal, J.A. Sennello, and R. Fayad Role of leptin receptor-induced STAT3 signaling in modulation of intestinal and hepatic inflammation in mice J Leukoc Biol 85 2009 491 496
29. J. Wauman, and J. Tavernier Leptin receptor signaling: pathways to leptin resistance Front Biosci 16 2011 2771 2793
30. B.S. Mantell, M. Stefanovic-Racic, X. Yang, N. Dedousis, I.J. Sipula, and R.M. O'Doherty Mice lacking NKT cells but with a complete complement of CD8+ T-cells are not protected against the metabolic abnormalities of diet-induced obesity PLoS One 6 2011 e19831
31. M. Guebre-Xabier, S. Yang, H.Z. Lin, R. Schwenk, U. Krzych, and A.M. Diehl Altered hepatic lymphocyte subpopulations in obesity-related murine fatty livers: potential mechanism for sensitization to liver damage Hepatology 31 2000 633 640