Improved insulin sensitivity despite increased visceral adiposity in mice deficient for the immune cell transcription factor T-bet

Cell Metabolism

Volumn 17, Issue 4, 2013, Pages 520-533

  Stolarczyk, Emilie ^a   Vong, Chi Teng ^a   Perucha, Esperanza ^a   Jackson, Ian ^a   Cawthorne, Michael A ^b   Wargent, Edward T ^b   Powell, Nick ^a,c   Canavan, James B ^a,c   Lord, Graham M ^a   Howard, Jane K ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF BUCKINGHAM   (United Kingdom)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

RAG2 PROTEIN; TRANSCRIPTION FACTOR T BET;

ABDOMINAL OBESITY; ADAPTIVE IMMUNITY; ADIPOSE TISSUE; ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CELL POPULATION; CONTROLLED STUDY; CYTOKINE RELEASE; GLUCOSE HOMEOSTASIS; INNATE IMMUNITY; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; MALE; METABOLISM; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; WILD TYPE;

ADIPOSE TISSUE; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CYTOKINES; DIET, HIGH-FAT; DNA-BINDING PROTEINS; ENERGY METABOLISM; IMMUNE SYSTEM; INSULIN RESISTANCE; INTERFERON-GAMMA; INTRA-ABDOMINAL FAT; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; OBESITY; PHENOTYPE; T-BOX DOMAIN PROTEINS;

MUS;

EID: 84875883411     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2013.02.019     Document Type: Article

References (50)

1. B. Afzali, G. Lombardi, R.I. Lechler, and G.M. Lord The role of T helper 17 (Th17) and regulatory T cells (Treg) in human organ transplantation and autoimmune disease Clin. Exp. Immunol. 148 2007 32 46
2. M. Bellahcene, J.F. O'Dowd, E.T. Wargent, M.S. Zaibi, D.C. Hislop, R.A. Ngala, D.M. Smith, M.A. Cawthorne, C.J. Stocker, and J.R. Arch Male mice that lack the G-protein-coupled receptor GPR41 have low energy expenditure and increased body fat content Br. J. Nutr. 2012 Oct 31:1-10 [Epub ahead of print]
3. E. Bettelli, B. Sullivan, S.J. Szabo, R.A. Sobel, L.H. Glimcher, and V.K. Kuchroo Loss of T-bet, but not STAT1, prevents the development of experimental autoimmune encephalomyelitis J. Exp. Med. 200 2004 79 87
4. S. Caspar-Bauguil, B. Cousin, A. Galinier, C. Segafredo, M. Nibbelink, M. André, L. Casteilla, and L. Pénicaud Adipose tissues as an ancestral immune organ: site-specific change in obesity FEBS Lett. 579 2005 3487 3492
5. C. Duffaut, J. Galitzky, M. Lafontan, and A. Bouloumié Unexpected trafficking of immune cells within the adipose tissue during the onset of obesity Biochem. Biophys. Res. Commun. 384 2009 482 485
6. A. Faedo, F. Ficara, M. Ghiani, A. Aiuti, J.L. Rubenstein, and A. Bulfone Developmental expression of the T-box transcription factor T-bet/Tbx21 during mouse embryogenesis Mech. Dev. 116 2002 157 160
7. I.A. Ferber, S. Brocke, C. Taylor-Edwards, W. Ridgway, C. Dinisco, L. Steinman, D. Dalton, and C.G. Fathman Mice with a disrupted IFN-gamma gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE) J. Immunol. 156 1996 5 7
8. M. Feuerer, L. Herrero, D. Cipolletta, A. Naaz, J. Wong, A. Nayer, J. Lee, A.B. Goldfine, C. Benoist, S. Shoelson, and D. Mathis Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters Nat. Med. 15 2009 930 939
9. W.S. Garrett, G.M. Lord, S. Punit, G. Lugo-Villarino, S.K. Mazmanian, S. Ito, J.N. Glickman, and L.H. Glimcher Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system Cell 131 2007 33 45
10. W.S. Garrett, S. Punit, C.A. Gallini, M. Michaud, D. Zhang, K.S. Sigrist, G.M. Lord, J.N. Glickman, and L.H. Glimcher Colitis-associated colorectal cancer driven by T-bet deficiency in dendritic cells Cancer Cell 16 2009 208 219
11. G.K. Hansson, P. Libby, U. Schönbeck, and Z.Q. Yan Innate and adaptive immunity in the pathogenesis of atherosclerosis Circ. Res. 91 2002 281 291
12. A.C. Horton, and J.J. Gibson-Brown Evolution of developmental functions by the Eomesodermin, T-brain-1, Tbx21 subfamily of T-box genes: insights from amphioxus J. Exp. Zool. 294 2002 112 121
13. J.K. Howard, G.M. Lord, G. Matarese, S. Vendetti, M.A. Ghatei, M.A. Ritter, R.I. Lechler, and S.R. Bloom Leptin protects mice from starvation-induced lymphoid atrophy and increases thymic cellularity in ob/ob mice J. Clin. Invest. 104 1999 1051 1059
14. J.K. Howard, B.J. Cave, L.J. Oksanen, I. Tzameli, C. Bjørbaek, and J.S. Flier Enhanced leptin sensitivity and attenuation of diet-induced obesity in mice with haploinsufficiency of Socs3 Nat. Med. 10 2004 734 738
15. K.E. Inouye, H. Shi, J.K. Howard, C.H. Daly, G.M. Lord, B.J. Rollins, and J.S. Flier Absence of CC chemokine ligand 2 does not limit obesity-associated infiltration of macrophages into adipose tissue Diabetes 56 2007 2242 2250
16. R.G. Jenner, M.J. Townsend, I. Jackson, K. Sun, R.D. Bouwman, R.A. Young, L.H. Glimcher, and G.M. Lord The transcription factors T-bet and GATA-3 control alternative pathways of T-cell differentiation through a shared set of target genes Proc. Natl. Acad. Sci. USA 106 2009 17876 17881
17. A. Kanhere, A. Hertweck, U. Bhatia, M.R. Gökmen, E. Perucha, I. Jackson, G.M. Lord, and R.G. Jenner T-bet and GATA3 orchestrate Th1 and Th2 differentiation through lineage-specific targeting of distal regulatory elements Nat. Commun. 3 2012 1268
18. A.D. Karelis Metabolically healthy but obese individuals Lancet 372 2008 1281 1283
19. J.Y. Kim, E. van de Wall, M. Laplante, A. Azzara, M.E. Trujillo, S.M. Hofmann, T. Schraw, J.L. Durand, H. Li, and G. Li Obesity-associated improvements in metabolic profile through expansion of adipose tissue J. Clin. Invest. 117 2007 2621 2637
20. U. Kintscher, M. Hartge, K. Hess, A. Foryst-Ludwig, M. Clemenz, M. Wabitsch, P. Fischer-Posovszky, T.F. Barth, D. Dragun, and T. Skurk T-lymphocyte infiltration in visceral adipose tissue: a primary event in adipose tissue inflammation and the development of obesity-mediated insulin resistance Arterioscler. Thromb. Vasc. Biol. 28 2008 1304 1310
21. G. Lametschwandtner, T. Biedermann, C. Schwärzler, C. Günther, J. Kund, S. Fassl, S. Hinteregger, N. Carballido-Perrig, S.J. Szabo, L.H. Glimcher, and J.M. Carballido Sustained T-bet expression confers polarized human TH2 cells with TH1-like cytokine production and migratory capacities J. Allergy Clin. Immunol. 113 2004 987 994
22. A.A. Lighvani, D.M. Frucht, D. Jankovic, H. Yamane, J. Aliberti, B.D. Hissong, B.V. Nguyen, M. Gadina, A. Sher, W.E. Paul, and J.J. O'Shea T-bet is rapidly induced by interferon-gamma in lymphoid and myeloid cells Proc. Natl. Acad. Sci. USA 98 2001 15137 15142
23. G.M. Lord, G. Matarese, J.K. Howard, R.J. Baker, S.R. Bloom, and R.I. Lechler Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression Nature 394 1998 897 901
24. G.M. Lord, R.M. Rao, H. Choe, B.M. Sullivan, A.H. Lichtman, F.W. Luscinskas, and L.H. Glimcher T-bet is required for optimal proinflammatory CD4+ T-cell trafficking Blood 106 2005 3432 3439
25. G. Lugo-Villarino, R. Maldonado-Lopez, R. Possemato, C. Penaranda, and L.H. Glimcher T-bet is required for optimal production of IFN-gamma and antigen-specific T cell activation by dendritic cells Proc. Natl. Acad. Sci. USA 100 2003 7749 7754
26. C.N. Lumeng, J.L. Bodzin, and A.R. Saltiel Obesity induces a phenotypic switch in adipose tissue macrophage polarization J. Clin. Invest. 117 2007 175 184
27. C.N. Lumeng, I. Maillard, and A.R. Saltiel T-ing up inflammation in fat Nat. Med. 15 2009 846 847
28. D.R. Matthews, J.P. Hosker, A.S. Rudenski, B.A. Naylor, D.F. Treacher, and R.C. Turner Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man Diabetologia 28 1985 412 419
29. S. Mitsui, K.M. Igarashi, K. Mori, and Y. Yoshihara Genetic visualization of the secondary olfactory pathway in Tbx21 transgenic mice Neural Syst. Circuits 1 2011 5
30. I. Nieto-Vazquez, S. Fernández-Veledo, D.K. Krämer, R. Vila-Bedmar, L. Garcia-Guerra, and M. Lorenzo Insulin resistance associated to obesity: the link TNF-alpha Arch. Physiol. Biochem. 114 2008 183 194
31. S. Nishimura, I. Manabe, M. Nagasaki, K. Eto, H. Yamashita, M. Ohsugi, M. Otsu, K. Hara, K. Ueki, and S. Sugiura CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity Nat. Med. 15 2009 914 920
32. R.W. O'Rourke, A.E. White, M.D. Metcalf, B.R. Winters, B.S. Diggs, X. Zhu, and D.L. Marks Systemic inflammation and insulin sensitivity in obese IFN-γ knockout mice Metabolism 61 2012 1152 1161
33. K. Ohmura, N. Ishimori, Y. Ohmura, S. Tokuhara, A. Nozawa, S. Horii, Y. Andoh, S. Fujii, K. Iwabuchi, K. Onoé, and H. Tsutsui 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
34. O. Osborn, and J.M. Olefsky The cellular and signaling networks linking the immune system and metabolism in disease Nat. Med. 18 2012 363 374
35. N. Powell, A.W. Walker, E. Stolarczyk, J.B. Canavan, M.R. Gökmen, E. Marks, I. Jackson, A. Hashim, M.A. Curtis, and R.G. Jenner The transcription factor T-bet regulates intestinal inflammation mediated by interleukin-7 receptor+ innate lymphoid cells Immunity 37 2012 674 684
36. V.Z. Rocha, E.J. Folco, G. Sukhova, K. Shimizu, I. Gotsman, A.H. Vernon, and P. Libby Interferon-gamma, a Th1 cytokine, regulates fat inflammation: a role for adaptive immunity in obesity Circ. Res. 103 2008 467 476
37. S. Schulte, G.K. Sukhova, and P. Libby Genetically programmed biases in Th1 and Th2 immune responses modulate atherogenesis Am. J. Pathol. 172 2008 1500 1508
38. K. Soderquest, N. Powell, C. Luci, N. van Rooijen, A. Hidalgo, F. Geissmann, T. Walzer, G.M. Lord, and A. Martín-Fontecha Monocytes control natural killer cell differentiation to effector phenotypes Blood 117 2011 4511 4518
39. C.J. Stocker, E. Wargent, J. O'Dowd, C. Cornick, J.R. Speakman, J.R. Arch, and M.A. Cawthorne Prevention of diet-induced obesity and impaired glucose tolerance in rats following administration of leptin to their mothers Am. J. Physiol. Regul. Integr. Comp. Physiol. 292 2007 R1810 R1818
40. S.J. Szabo, S.T. Kim, G.L. Costa, X. Zhang, C.G. Fathman, and L.H. Glimcher A novel transcription factor, T-bet, directs Th1 lineage commitment Cell 100 2000 655 669
41. S.J. Szabo, B.M. Sullivan, C. Stemmann, A.R. Satoskar, B.P. Sleckman, and L.H. Glimcher Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells Science 295 2002 338 342
42. M.J. Townsend, A.S. Weinmann, J.L. Matsuda, R. Salomon, P.J. Farnham, C.A. Biron, L. Gapin, and L.H. Glimcher T-bet regulates the terminal maturation and homeostasis of NK and Valpha14i NKT cells Immunity 20 2004 477 494
43. T.T. Tran, Y. Yamamoto, S. Gesta, and C.R. Kahn Beneficial effects of subcutaneous fat transplantation on metabolism Cell Metab. 7 2008 410 420
44. J.B. Weir New methods for calculating metabolic rate with special reference to protein metabolism J. Physiol. 109 1949 1 9
45. S.P. Weisberg, D. McCann, M. Desai, M. Rosenbaum, R.L. Leibel, and A.W. Ferrante Jr. Obesity is associated with macrophage accumulation in adipose tissue J. Clin. Invest. 112 2003 1796 1808
46. S. Winer, Y. Chan, G. Paltser, D. Truong, H. Tsui, J. Bahrami, R. Dorfman, Y. Wang, J. Zielenski, and F. Mastronardi Normalization of obesity-associated insulin resistance through immunotherapy Nat. Med. 15 2009 921 929
47. D.A. Winer, S. Winer, L. Shen, P.P. Wadia, J. Yantha, G. Paltser, H. Tsui, P. Wu, M.G. Davidson, and M.N. Alonso B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies Nat. Med. 17 2011 610 617
48. N. Wong, B.C. Fam, G.R. Cempako, G.R. Steinberg, K. Walder, T.W. Kay, J. Proietto, and S. Andrikopoulos Deficiency in interferon-gamma results in reduced body weight and better glucose tolerance in mice Endocrinology 152 2011 3690 3699
49. H. Xu, G.T. Barnes, Q. Yang, G. Tan, D. Yang, C.J. Chou, J. Sole, A. Nichols, J.S. Ross, L.A. Tartaglia, and H. Chen Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance J. Clin. Invest. 112 2003 1821 1830
50. J. Zhu, and W.E. Paul CD4 T cells: fates, functions, and faults Blood 112 2008 1557 1569