Jejunal T Cell Inflammation in Human Obesity Correlates with Decreased Enterocyte Insulin Signaling

Cell Metabolism

Volumn 22, Issue 1, 2015, Pages 113-124

  Monteiro Sepulveda, Milena ^a,b,e   Touch, Sothea ^a,c,e   Mendes Sá, Carla ^c,e   André, Sébastien ^a,c,e   Poitou, Christine ^a,c,e   Allatif, Omran ^a,c,e   Cotillard, Aurélie ^a,c,e   Fohrer Ting, Hélène ^a,b   Hubert, Edwige Ludiwyne ^a,b,e   Remark, Romain ^b,d   Genser, Laurent ^a,c,e   Tordjman, Joan ^a,c,e   Garbin, Kevin ^a,b   Osinski, Céline ^a,b   Sautès Fridman, Catherine ^b,d   Leturque, Armelle ^a,b,e   Clément, Karine ^a,c,e   Brot Laroche, Edith ^a,b,e  

^a SORBONNE UNIVERSITÉ   (France)

^b CENTRE DE RECHERCHE DES CORDELIERS   (France)

^c Institute OfCardiometabolism and Nutrition   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; CD8ALPHABETA ANTIGEN; GLUCOSE TRANSPORTER 2; INSULIN; UNCLASSIFIED DRUG; SLC2A2 PROTEIN, HUMAN;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; APOPTOSIS; ARTICLE; BODY MASS; CELL DENSITY; CELL POPULATION; COMORBIDITY; CONTROLLED STUDY; CYTOKINE RELEASE; HUMAN; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; INSULIN RESISTANCE; INTESTINE CELL; INTESTINE MUCOSA; JEJUNUM; LAMINA PROPRIA; LIPID METABOLISM; MAJOR CLINICAL STUDY; NONALCOHOLIC FATTY LIVER; OBESITY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE; ADULT; CELL CULTURE; COMPLICATION; CYTOLOGY; FEMALE; IMMUNOLOGY; INFLAMMATION; MALE; MIDDLE AGED; PATHOLOGY;

ADULT; ANTIGENS, CD8; CELLS, CULTURED; ENTEROCYTES; FEMALE; GLUCOSE TRANSPORTER TYPE 2; HUMANS; INFLAMMATION; INSULIN; INSULIN RESISTANCE; INTESTINAL MUCOSA; JEJUNUM; MALE; MIDDLE AGED; OBESITY; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84937513385     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2015.05.020     Document Type: Article

References (45)

1. A. Ait-Omar, M. Monteiro-Sepulveda, C. Poitou, M. Le Gall, A. Cotillard, J. Gilet, K. Garbin, A. Houllier, D. Château, A. Lacombe, and et al. GLUT2 accumulation in enterocyte apical and intracellular membranes: a study in morbidly obese human subjects and ob/ob and high fat-fed mice Diabetes 60 2011 2598 2607
2. P. Bedossa, C. Poitou, N. Veyrie, J.L. Bouillot, A. Basdevant, V. Paradis, J. Tordjman, and K. Clement Histopathological algorithm and scoring system for evaluation of liver lesions in morbidly obese patients Hepatology 56 2012 1751 1759
3. P. Brandtzaeg, T.S. Halstensen, K. Kett, P. Krajci, D. Kvale, T.O. Rognum, H. Scott, and L.M. Sollid Immunobiology and immunopathology of human gut mucosa: humoral immunity and intraepithelial lymphocytes Gastroenterology 97 1989 1562 1584
4. E.E. Calle, and R. Kaaks Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms Nat. Rev. Cancer 4 2004 579 591
5. R. Cancello, J. Tordjman, C. Poitou, G. Guilhem, J.L. Bouillot, D. Hugol, C. Coussieu, A. Basdevant, A. Bar Hen, P. Bedossa, and et al. Increased infiltration of macrophages in omental adipose tissue is associated with marked hepatic lesions in morbid human obesity Diabetes 55 2006 1554 1561
6. H. Cheroutre, F. Lambolez, and D. Mucida The light and dark sides of intestinal intraepithelial lymphocytes Nat. Rev. Immunol. 11 2011 445 456
7. A. Cotillard, S.P. Kennedy, L.C. Kong, E. Prifti, N. Pons, E. Le Chatelier, M. Almeida, B. Quinquis, F. Levenez, N. Galleron ANR MicroObes consortium Dietary intervention impact on gut microbial gene richness Nature 500 2013 585 588
8. E. Dalmas, N. Venteclef, C. Caer, C. Poitou, I. Cremer, J. Aron-Wisnewsky, S. Lacroix-Desmazes, J. Bayry, S.V. Kaveri, K. Clément, and et al. T cell-derived IL-22 amplifies IL-1β-driven inflammation in human adipose tissue: relevance to obesity and type 2 diabetes Diabetes 63 2014 1966 1977
9. J. Deiuliis, Z. Shah, N. Shah, B. Needleman, D. Mikami, V. Narula, K. Perry, J. Hazey, T. Kampfrath, M. Kollengode, and et al. Visceral adipose inflammation in obesity is associated with critical alterations in tregulatory cell numbers PLoS ONE 6 2011 e16376
10. S. Ding, and P.K. Lund Role of intestinal inflammation as an early event in obesity and insulin resistance Curr. Opin. Clin. Nutr. Metab. Care 14 2011 328 333
11. A. Divoux, S. Moutel, C. Poitou, D. Lacasa, N. Veyrie, A. Aissat, M. Arock, M. Guerre-Millo, and K. Clément Mast cells in human adipose tissue: link with morbid obesity, inflammatory status, and diabetes J. Clin. Endocrinol. Metab. 97 2012 E1677 E1685
12. C. Duffaut, A. Zakaroff-Girard, V. Bourlier, P. Decaunes, M. Maumus, P. Chiotasso, C. Sengenès, M. Lafontan, J. Galitzky, and A. Bouloumié Interplay between human adipocytes and T lymphocytes in obesity: CCL20 as an adipochemokine and T lymphocytes as lipogenic modulators Arterioscler. Thromb. Vasc. Biol. 29 2009 1608 1614
13. 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
14. L. Fändriks The angiotensin II type 2 receptor and the gastrointestinal tract J. Renin Angiotensin Aldosterone Syst. 11 2010 43 48
15. 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
16. K. Ganeshan, and A. Chawla Metabolic regulation of immune responses Annu. Rev. Immunol. 32 2014 609 634
17. T. Gebhardt, and L.K. Mackay Local immunity by tissue-resident CD8(+) memory T cells Front. Immunol. 3 2012 340
18. A. Geremia, P. Biancheri, P. Allan, G.R. Corazza, and A. Di Sabatino Innate and adaptive immunity in inflammatory bowel disease Autoimmun. Rev. 13 2013 3 10
19. M.F. Gregor, and G.S. Hotamisligil Inflammatory mechanisms in obesity Annu. Rev. Immunol. 29 2011 415 445
20. M. Haidari, N. Leung, F. Mahbub, K.D. Uffelman, R. Kohen-Avramoglu, G.F. Lewis, and K. Adeli Fasting and postprandial overproduction of intestinally derived lipoproteins in an animal model of insulin resistance. Evidence that chronic fructose feeding in the hamster is accompanied by enhanced intestinal de novo lipogenesis and ApoB48-containing lipoprotein overproduction J. Biol. Chem. 277 2002 31646 31655
21. 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
22. A. Izcue, J.L. Coombes, and F. Powrie Regulatory lymphocytes and intestinal inflammation Annu. Rev. Immunol. 27 2009 313 338
23. A.M. Johnson, and J.M. Olefsky The origins and drivers of insulin resistance Cell 152 2013 673 684
24. U. Kintscher, M. Hartge, K. Hess, A. Foryst-Ludwig, M. Clemenz, M. Wabitsch, P. Fischer-Posovszky, T.F. Barth, D. Dragun, T. Skurk, and et al. 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
25. J.M. Leung, M. Davenport, M.J. Wolff, K.E. Wiens, W.M. Abidi, M.A. Poles, I. Cho, T. Ullman, L. Mayer, and P. Loke IL-22-producing CD4+ cells are depleted in actively inflamed colitis tissue Mucosal Immunol. 7 2014 124 133
26. C.N. Lumeng Innate immune activation in obesity Mol. Aspects Med. 34 2013 12 29
27. S. Melgar, A. Bas, S. Hammarström, and M.L. Hammarström Human small intestinal mucosa harbours a small population of cytolytically active CD8+ alphabeta T lymphocytes Immunology 106 2002 476 485
28. S. Nishimura, I. Manabe, M. Nagasaki, K. Eto, H. Yamashita, M. Ohsugi, M. Otsu, K. Hara, K. Ueki, S. Sugiura, and et al. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity Nat. Med. 15 2009 914 920
29. R.W. O'Rourke, M.D. Metcalf, A.E. White, A. Madala, B.R. Winters, I.I. Maizlin, B.A. Jobe, C.T. Roberts Jr., M.K. Slifka, and D.L. Marks Depot-specific differences in inflammatory mediators and a role for NK cells and IFN-gamma in inflammation in human adipose tissue Int. J. Obes. (Lond) 33 2009 978 990
30. L. Peyrin-Biroulet, M. Chamaillard, F. Gonzalez, E. Beclin, C. Decourcelle, L. Antunes, J. Gay, C. Neut, J.F. Colombel, and P. Desreumaux Mesenteric fat in Crohn's disease: a pathogenetic hallmark or an innocent bystander? Gut 56 2007 577 583
31. V.T. Samuel, and G.I. Shulman Mechanisms for insulin resistance: common threads and missing links Cell 148 2012 852 871
32. O. Schulz, and O. Pabst Antigen sampling in the small intestine Trends Immunol. 34 2013 155 161
33. D.S. Shouval, J. Ouahed, A. Biswas, J.A. Goettel, B.H. Horwitz, C. Klein, A.M. Muise, and S.B. Snapper Interleukin 10 receptor signaling: master regulator of intestinal mucosal homeostasis in mice and humans Adv. Immunol. 122 2014 177 210
34. V. Tobin, M. Le Gall, X. Fioramonti, E. Stolarczyk, A.G. Blazquez, C. Klein, M. Prigent, P. Serradas, M.H. Cuif, C. Magnan, and et al. Insulin internalizes GLUT2 in the enterocytes of healthy but not insulin-resistant mice Diabetes 57 2008 555 562
35. A. Tran, and P. Gual Non-alcoholic steatohepatitis in morbidly obese patients Clin. Res. Hepatol. Gastroenterol. 37 2013 17 29
36. P. Vajro, G. Paolella, and A. Fasano Microbiota and gut-liver axis: their influences on obesity and obesity-related liver disease J. Pediatr. Gastroenterol. Nutr. 56 2013 461 468
37. A. Veilleux, E. Grenier, P. Marceau, A.C. Carpentier, D. Richard, and E. Levy Intestinal lipid handling: evidence and implication of insulin signaling abnormalities in human obese subjects Arterioscler. Thromb. Vasc. Biol. 34 2014 644 653
38. M. Veldhoen, and V. Brucklacher-Waldert Dietary influences on intestinal immunity Nat. Rev. Immunol. 12 2012 696 708
39. M. Versini, P.Y. Jeandel, E. Rosenthal, and Y. Shoenfeld Obesity in autoimmune diseases: not a passive bystander Autoimmun. Rev. 13 2014 981 1000
40. K. Wang, and M. Karin Common flora and intestine: A carcinogenic marriage Cell. Logist. 3 2013 e24975
41. X. Wang, N. Ota, P. Manzanillo, L. Kates, J. Zavala-Solorio, C. Eidenschenk, J. Zhang, J. Lesch, W.P. Lee, J. Ross, and et al. Interleukin-22 alleviates metabolic disorders and restores mucosal immunity in diabetes Nature 514 2014 237 241
42. 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
43. 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
44. M. Zeyda, D. Farmer, J. Todoric, O. Aszmann, M. Speiser, G. Györi, G.J. Zlabinger, and T.M. Stulnig Human adipose tissue macrophages are of an anti-inflammatory phenotype but capable of excessive pro-inflammatory mediator production Int. J. Obes. (Lond) 31 2007 1420 1428
45. R. Zhao, D. Tang, S. Yi, W. Li, C. Wu, Y. Lu, X. Hou, J. Song, P. Lin, L. Chen, and L. Sun Elevated peripheral frequencies of Th22 cells: a novel potent participant in obesity and type 2 diabetes PLoS ONE 9 2014 e85770