Immunological goings-on in visceral adipose tissue

Cell Metabolism

Volumn 17, Issue 6, 2013, Pages 851-859

  Mathis, Diane ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; TRANSCRIPTION FACTOR FOXP3;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; B LYMPHOCYTE; CELL DIFFERENTIATION; CELL SURVIVAL; CYTOKINE PRODUCTION; HUMAN; IMMUNOCOMPETENT CELL; INFLAMMATION; INNATE IMMUNITY; INSULIN RESISTANCE; INSULIN SENSITIVITY; INTRAABDOMINAL FAT; LYMPHOCYTIC INFILTRATION; MACROPHAGE MIGRATION; NATURAL KILLER T CELL; NONHUMAN; OBESITY; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE;

B-LYMPHOCYTES; DIABETES MELLITUS, TYPE 2; HUMANS; INFLAMMATION; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; MACROPHAGES; NATURAL KILLER T-CELLS; OBESITY; T-LYMPHOCYTES;

EID: 84878785347     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2013.05.008     Document Type: Review

References (74)

1. M. Alvehus, J. Burén, M. Sjöström, J. Goedecke, and T. Olsson The human visceral fat depot has a unique inflammatory profile Obesity (Silver Spring) 18 2010 879 883
2. 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
3. A. Chawla, K.D. Nguyen, and Y.P. Goh Macrophage-mediated inflammation in metabolic disease Nat. Rev. Immunol. 11 2011 738 749
4. X. Cheng, J. Wang, N. Xia, X.X. Yan, T.T. Tang, H. Chen, H.J. Zhang, J. Liu, W. Kong, and S. Sjöberg A guanidine-rich regulatory oligodeoxynucleotide improves type-2 diabetes in obese mice by blocking T-cell differentiation EMBO Mol Med 4 2012 1112 1125
5. D. Cipolletta, M. Feuerer, A. Li, N. Kamei, J. Lee, S.E. Shoelson, C. Benoist, and D. Mathis PPAR-γ is a major driver of the accumulation and phenotype of adipose tissue Treg cells Nature 486 2012 549 553
6. J. DeFuria, A.C. Belkina, M. Jagannathan-Bogdan, J. Snyder-Cappione, J.D. Carr, Y.R. Nersesova, D. Markham, K.J. Strissel, A.A. Watkins, and M. Zhu B cells promote inflammation in obesity and type 2 diabetes through regulation of T-cell function and an inflammatory cytokine profile Proc. Natl. Acad. Sci. USA 110 2013 5133 5138
7. J. Deiuliis, Z. Shah, N. Shah, B. Needleman, D. Mikami, V. Narula, K. Perry, J. Hazey, T. Kampfrath, and M. Kollengode Visceral adipose inflammation in obesity is associated with critical alterations in tregulatory cell numbers PLoS ONE 6 2011 e16376
8. T. Deng, C.J. Lyon, L.J. Minze, J. Lin, J. Zou, J.Z. Liu, Y. Ren, Z. Yin, D.J. Hamilton, and P.R. Reardon Class II major histocompatibility complex plays an essential role in obesity-induced adipose inflammation Cell Metab. 17 2013 411 422
9. M.Y. Donath, and S.E. Shoelson Type 2 diabetes as an inflammatory disease Nat. Rev. Immunol. 11 2011 98 107
10. 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
11. V. Elgazar-Carmon, A. Rudich, N. Hadad, and R. Levy Neutrophils transiently infiltrate intra-abdominal fat early in the course of high-fat feeding J. Lipid Res. 49 2008 1894 1903
12. K. Eller, A. Kirsch, A.M. Wolf, S. Sopper, A. Tagwerker, U. Stanzl, D. Wolf, W. Patsch, A.R. Rosenkranz, and P. Eller Potential role of regulatory T cells in reversing obesity-linked insulin resistance and diabetic nephropathy Diabetes 60 2011 2954 2962
13. 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
14. A.W. Goldrath, C.J. Luckey, R. Park, C. Benoist, and D. Mathis The molecular program induced in T cells undergoing homeostatic proliferation Proc. Natl. Acad. Sci. USA 101 2004 16885 16890
15. J. Henao-Mejia, E. Elinav, C. Jin, L. Hao, W.Z. Mehal, T. Strowig, C.A. Thaiss, A.L. Kau, S.C. Eisenbarth, and M.J. Jurczak Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity Nature 482 2012 179 185
16. L. Herrero, H. Shapiro, A. Nayer, J. Lee, and S.E. Shoelson Inflammation and adipose tissue macrophages in lipodystrophic mice Proc. Natl. Acad. Sci. USA 107 2010 240 245
17. G.S. Hotamisligil, N.S. Shargill, and B.M. Spiegelman Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance Science 259 1993 87 91
18. Y. Ilan, R. Maron, A.M. Tukpah, T.U. Maioli, G. Murugaiyan, K. Yang, H.Y. Wu, and H.L. Weiner Induction of regulatory T cells decreases adipose inflammation and alleviates insulin resistance in ob/ob mice Proc. Natl. Acad. Sci. USA 107 2010 9765 9770
19. H. Ji, K. Ohmura, U. Mahmood, D.M. Lee, F.M.A. Hofhuis, S.A. Boackle, K. Takahashi, V.M. Holers, M. Walport, and C. Gerard Arthritis critically dependent on innate immune system players Immunity 16 2002 157 168
20. Y. Ji, S. Sun, S. Xia, L. Yang, X. Li, and L. Qi Short term high fat diet challenge promotes alternative macrophage polarization in adipose tissue via natural killer T cells and interleukin-4 J. Biol. Chem. 287 2012 24378 24386
21. Y. Ji, S. Sun, A. Xu, P. Bhargava, L. Yang, K.S. Lam, B. Gao, C.H. Lee, S. Kersten, and L. Qi Activation of natural killer T cells promotes M2 Macrophage polarization in adipose tissue and improves systemic glucose tolerance via interleukin-4 (IL-4)/STAT6 protein signaling axis in obesity J. Biol. Chem. 287 2012 13561 13571
22. S.Z. Josefowicz, L.F. Lu, and A.Y. Rudensky Regulatory T cells: mechanisms of differentiation and function Annu. Rev. Immunol. 30 2012 531 564
23. N. Kamei, K. Tobe, R. Suzuki, M. Ohsugi, T. Watanabe, N. Kubota, N. Ohtsuka-Kowatari, K. Kumagai, K. Sakamoto, and M. Kobayashi Overexpression of monocyte chemoattractant protein-1 in adipose tissues causes macrophage recruitment and insulin resistance J. Biol. Chem. 281 2006 26602 26614
24. H. Kanda, S. Tateya, Y. Tamori, K. Kotani, K. Hiasa, R. Kitazawa, S. Kitazawa, H. Miyachi, S. Maeda, K. Egashira, and M. Kasuga MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity J. Clin. Invest. 116 2006 1494 1505
25. K. Kang, S.M. Reilly, V. Karabacak, M.R. Gangl, K. Fitzgerald, B. Hatano, and C.H. Lee Adipocyte-derived Th2 cytokines and myeloid PPARdelta regulate macrophage polarization and insulin sensitivity Cell Metab. 7 2008 485 495
26. 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
27. C.S. Klose, E.A. Kiss, V. Schwierzeck, K. Ebert, T. Hoyler, Y. d'Hargues, N. Göppert, A.L. Croxford, A. Waisman, Y. Tanriver, and A. Diefenbach A T-bet gradient controls the fate and function of CCR6-RORγt+ innate lymphoid cells Nature 494 2013 261 265
28. M.E. Kotas, H.Y. Lee, M.P. Gillum, C. Annicelli, B.A. Guigni, G.I. Shulman, and R. Medzhitov Impact of CD1d deficiency on metabolism PLoS ONE 6 2011 e25478
29. J. Liu, A. Divoux, J. Sun, J. Zhang, K. Clément, J.N. Glickman, G.K. Sukhova, P.J. Wolters, J. Du, and C.Z. Gorgun Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice Nat. Med. 15 2009 940 945
30. 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
31. C.N. Lumeng, S.M. Deyoung, J.L. Bodzin, and A.R. Saltiel Increased inflammatory properties of adipose tissue macrophages recruited during diet-induced obesity Diabetes 56 2007 16 23
32. 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
33. L. Lynch, M. Nowak, B. Varghese, J. Clark, A.E. Hogan, V. Toxavidis, S.P. Balk, D. O'Shea, C. O'Farrelly, and M.A. Exley Adipose tissue invariant NKT cells protect against diet-induced obesity and metabolic disorder through regulatory cytokine production Immunity 37 2012 574 587
34. Y. Macotela, J. Boucher, T.T. Tran, and C.R. Kahn Sex and depot differences in adipocyte insulin sensitivity and glucose metabolism Diabetes 58 2009 803 812
35. Y. Macotela, B. Emanuelli, M.A. Mori, S. Gesta, T.J. Schulz, Y.H. Tseng, and C.R. Kahn Intrinsic differences in adipocyte precursor cells from different white fat depots Diabetes 61 2012 1691 1699
36. 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
37. K. Meijer, M. de Vries, S. Al-Lahham, M. Bruinenberg, D. Weening, M. Dijkstra, N. Kloosterhuis, R.J. van der Leij, H. van der Want, and B.J. Kroesen Human primary adipocytes exhibit immune cell function: adipocytes prime inflammation independent of macrophages PLoS ONE 6 2011 e17154
38. A.B. Molofsky, J.C. Nussbaum, H.E. Liang, S.J. Van Dyken, L.E. Cheng, A. Mohapatra, A. Chawla, and R.M. Locksley Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages J. Exp. Med. 210 2013 535 549
39. D.L. Morris, K.W. Cho, J.L. Delproposto, K.E. Oatmen, L.M. Geletka, G. Martinez-Santibanez, K. Singer, and C.N. Lumeng Adipose tissue macrophages function as antigen presenting cells and regulate adipose tissue CD4+ T cells in mice Diabetes 2013 10.2337/db12-1404 Published online March 14, 2013
40. M.T. Nguyen, S. Favelyukis, A.K. Nguyen, D. Reichart, P.A. Scott, A. Jenn, R. Liu-Bryan, C.K. Glass, J.G. Neels, and J.M. Olefsky A subpopulation of macrophages infiltrates hypertrophic adipose tissue and is activated by free fatty acids via Toll-like receptors 2 and 4 and JNK-dependent pathways J. Biol. Chem. 282 2007 35279 35292
41. J.K. Nicholson, E. Holmes, J. Kinross, R. Burcelin, G. Gibson, W. Jia, and S. Pettersson Host-gut microbiota metabolic interactions Science 336 2012 1262 1267
42. 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
43. J.I. Odegaard, R.R. Ricardo-Gonzalez, M.H. Goforth, C.R. Morel, V. Subramanian, L. Mukundan, A. Red Eagle, D. Vats, F. Brombacher, A.W. Ferrante, and A. Chawla Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance Nature 447 2007 1116 1120
44. 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
45. T. Olszak, D. An, S. Zeissig, M.P. Vera, J. Richter, A. Franke, J.N. Glickman, R. Siebert, R.M. Baron, D.L. Kasper, and R.S. Blumberg Microbial exposure during early life has persistent effects on natural killer T cell function Science 336 2012 489 493
46. K. Orihara, H. Morita, A. Yagami, N. Kajiwara, S. Nakae, K. Matsumoto, H. Nagasaki, Y. Saito, H. Saito, and A. Matsuda TH2 cytokines potently induce an appetite-stimulating peptide, melanin-concentrating hormone, in human vascular endothelial cells J. Allergy Clin. Immunol. 124 2009 612 614 614, e1-e2
47. 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
48. D. Patsouris, P.P. Li, D. Thapar, J. Chapman, J.M. Olefsky, and J.G. Neels Ablation of CD11c-positive cells normalizes insulin sensitivity in obese insulin resistant animals Cell Metab. 8 2008 301 309
49. S. Perrini, L. Laviola, A. Cignarelli, M. Melchiorre, F. De Stefano, C. Caccioppoli, A. Natalicchio, M.R. Orlando, G. Garruti, and M. De Fazio Fat depot-related differences in gene expression, adiponectin secretion, and insulin action and signalling in human adipocytes differentiated in vitro from precursor stromal cells Diabetologia 51 2008 155 164
50. A.D. Pradhan, J.E. Manson, N. Rifai, J.E. Buring, and P.M. Ridker C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus JAMA 286 2001 327 334
51. X. Prieur, C.Y. Mok, V.R. Velagapudi, V. Núñez, L. Fuentes, D. Montaner, K. Ishikawa, A. Camacho, N. Barbarroja, and S. O'Rahilly Differential lipid partitioning between adipocytes and tissue macrophages modulates macrophage lipotoxicity and M2/M1 polarization in obese mice Diabetes 60 2011 797 809
52. M.E. Rausch, S. Weisberg, P. Vardhana, and D.V. Tortoriello Obesity in C57BL/6J mice is characterized by adipose tissue hypoxia and cytotoxic T-cell infiltration Int J Obes (Lond) 32 2008 451 463
53. R.R. Ricardo-Gonzalez, A. Red Eagle, J.I. Odegaard, H. Jouihan, C.R. Morel, J.E. Heredia, L. Mukundan, D. Wu, R.M. Locksley, and A. Chawla IL-4/STAT6 immune axis regulates peripheral nutrient metabolism and insulin sensitivity Proc. Natl. Acad. Sci. USA 107 2010 22617 22622
54. 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
55. J. Rossjohn, D.G. Pellicci, O. Patel, L. Gapin, and D.I. Godfrey Recognition of CD1d-restricted antigens by natural killer T cells Nat. Rev. Immunol. 12 2012 845 857
56. M. Satoh, Y. Andoh, C.S. Clingan, H. Ogura, S. Fujii, K. Eshima, T. Nakayama, M. Taniguchi, N. Hirata, and N. Ishimori Type II NKT cells stimulate diet-induced obesity by mediating adipose tissue inflammation, steatohepatitis and insulin resistance PLoS ONE 7 2012 e30568
57. H.S. Schipper, M. Rakhshandehroo, S.F. van de Graaf, K. Venken, A. Koppen, R. Stienstra, S. Prop, J. Meerding, N. Hamers, and G. Besra Natural killer T cells in adipose tissue prevent insulin resistance J. Clin. Invest. 122 2012 3343 3354
58. M.E. Shaul, G. Bennett, K.J. Strissel, A.S. Greenberg, and M.S. Obin Dynamic, M2-like remodeling phenotypes of CD11c+ adipose tissue macrophages during high-fat diet - induced obesity in mice Diabetes 59 2010 1171 1181
59. R. Stienstra, J.A. van Diepen, C.J. Tack, M.H. Zaki, F.L. van de Veerdonk, D. Perera, G.A. Neale, G.J. Hooiveld, A. Hijmans, and I. Vroegrijk Inflammasome is a central player in the induction of obesity and insulin resistance Proc. Natl. Acad. Sci. USA 108 2011 15324 15329
60. D. Strodthoff, A.M. Lundberg, H.E. Agardh, D.F. Ketelhuth, G. Paulsson-Berne, P. Arner, G.K. Hansson, and N. Gerdes Lack of invariant natural killer t cells affects lipid metabolism in adipose tissue of diet-induced obese mice Arterioscler. Thromb. Vasc. Biol. 2013 10.1161/ATVBAHA.112.301105 Published online March 21, 2013
61. S. Talukdar, Y. Oh, G. Bandyopadhyay, D. Li, J. Xu, J. McNelis, M. Lu, P. Li, Q. Yan, and Y. Zhu Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase Nat. Med. 18 2012 1407 1412
62. 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
63. B. Vandanmagsar, Y.H. Youm, A. Ravussin, J.E. Galgani, K. Stadler, R.L. Mynatt, E. Ravussin, J.M. Stephens, and V.D. Dixit The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance Nat. Med. 17 2011 179 188
64. 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
65. S.P. Weisberg, D. Hunter, R. Huber, J. Lemieux, S. Slaymaker, K. Vaddi, I. Charo, R.L. Leibel, and A.W. Ferrante Jr. CCR2 modulates inflammatory and metabolic effects of high-fat feeding J. Clin. Invest. 116 2006 115 124
66. H. Wen, D. Gris, Y. Lei, S. Jha, L. Zhang, M.T. Huang, W.J. Brickey, and J.P. Ting Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling Nat. Immunol. 12 2011 408 415
67. 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
68. 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
69. H. Wu, S. Ghosh, X.D. Perrard, L. Feng, G.E. Garcia, J.L. Perrard, J.F. Sweeney, L.E. Peterson, L. Chan, C.W. Smith, and C.M. Ballantyne T-cell accumulation and regulated on activation, normal T cell expressed and secreted upregulation in adipose tissue in obesity Circulation 115 2007 1029 1038
70. D. Wu, A.B. Molofsky, H.E. Liang, R.R. Ricardo-Gonzalez, H.A. Jouihan, J.K. Bando, A. Chawla, and R.M. Locksley Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis Science 332 2011 243 247
71. L. Wu, V.V. Parekh, C.L. Gabriel, D.P. Bracy, P.A. Marks-Shulman, R.A. Tamboli, S. Kim, Y.V. Mendez-Fernandez, G.S. Besra, and J.P. Lomenick 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. USA 109 2012 E1143 E1152
72. 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
73. H. Yang, Y.H. Youm, B. Vandanmagsar, A. Ravussin, J.M. Gimble, F. Greenway, J.M. Stephens, R.L. Mynatt, and V.D. Dixit Obesity increases the production of proinflammatory mediators from adipose tissue T cells and compromises TCR repertoire diversity: implications for systemic inflammation and insulin resistance J. Immunol. 185 2010 1836 1845
74. L.A. Zúñiga, W.J. Shen, B. Joyce-Shaikh, E.A. Pyatnova, A.G. Richards, C. Thom, S.M. Andrade, D.J. Cua, F.B. Kraemer, and E.C. Butcher IL-17 regulates adipogenesis, glucose homeostasis, and obesity J. Immunol. 185 2010 6947 6959