The intestinal immune system in obesity and insulin resistance

Cell Metabolism

Volumn 23, Issue 3, 2016, Pages 413-426

  Winer, Daniel A ^a,b,c   Luck, Helen ^a,b   Tsai, Sue ^a   Winer, Shawn ^a,b,d  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

^d ST MICHAEL'S HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; TOLL LIKE RECEPTOR;

ADAPTIVE IMMUNITY; DISEASE ASSOCIATION; DYSBIOSIS; ENTERITIS; GASTROINTESTINAL TRACT; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOPATHOGENESIS; INFLAMMATION; INNATE IMMUNITY; INSULIN RESISTANCE; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; METABOLIC DISORDER; MOLECULAR PATHOLOGY; MUCOSAL IMMUNITY; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; ANIMAL; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MICROFLORA;

ADAPTIVE IMMUNITY; ANIMALS; GASTROINTESTINAL TRACT; HUMANS; IMMUNITY, INNATE; INSULIN RESISTANCE; MICROBIOTA; OBESITY;

EID: 84960810832     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2016.01.003     Document Type: Review

References (123)

1. R.M. Al-Sadi, and T.Y. Ma IL-1beta causes an increase in intestinal epithelial tight junction permeability J. Immunol. 178 2007 4641 4649
2. J. Amar, R. Burcelin, J.B. Ruidavets, P.D. Cani, J. Fauvel, M.C. Alessi, B. Chamontin, and J. Ferriéres Energy intake is associated with endotoxemia in apparently healthy men Am. J. Clin. Nutr. 87 2008 1219 1223
3. J. Amar, C. Chabo, A. Waget, P. Klopp, C. Vachoux, L.G. Bermúdez-Humarán, N. Smirnova, M. Bergé, T. Sulpice, S. Lahtinen, and et al. Intestinal mucosal adherence and translocation of commensal bacteria at the early onset of type 2 diabetes: molecular mechanisms and probiotic treatment EMBO Mol. Med. 3 2011 559 572
4. J. Amar, M. Serino, C. Lange, C. Chabo, J. Iacovoni, S. Mondot, P. Lepage, C. Klopp, J. Mariette, O. Bouchez, et al. D.E.S.I.R. Study Group Involvement of tissue bacteria in the onset of diabetes in humans: evidence for a concept Diabetologia 54 2011 3055 3061
5. F.F. Anhê, D. Roy, G. Pilon, S. Dudonné, S. Matamoros, T.V. Varin, C. Garofalo, Q. Moine, Y. Desjardins, E. Levy, and A. Marette A polyphenol-rich cranberry extract protects from diet-induced obesity, insulin resistance and intestinal inflammation in association with increased Akkermansia spp. population in the gut microbiota of mice Gut 64 2015 872 883
6. F. Bäckhed, H. Ding, T. Wang, L.V. Hooper, G.Y. Koh, A. Nagy, C.F. Semenkovich, and J.I. Gordon The gut microbiota as an environmental factor that regulates fat storage Proc. Natl. Acad. Sci. USA 101 2004 15718 15723
7. F. Bäckhed, J.K. Manchester, C.F. Semenkovich, and J.I. Gordon Mechanisms underlying the resistance to diet-induced obesity in germ-free mice Proc. Natl. Acad. Sci. USA 104 2007 979 984
8. F.S. Belforte, F. Coluccio Leskow, E. Poskus, and A. Penas Steinhardt Toll-like receptor 4 D299G polymorphism in metabolic disorders: a meta-analysis Mol. Biol. Rep. 40 2013 3015 3020
9. R.L. Bertrand, S. Senadheera, I. Markus, L. Liu, L. Howitt, H. Chen, T.V. Murphy, S.L. Sandow, and P.P. Bertrand A Western diet increases serotonin availability in rat small intestine Endocrinology 152 2011 36 47
10. S.B. Biddinger, and C.R. Kahn From mice to men: insights into the insulin resistance syndromes Annu. Rev. Physiol. 68 2006 123 158
11. J.R. Brestoff, B.S. Kim, S.A. Saenz, R.R. Stine, L.A. Monticelli, G.F. Sonnenberg, J.J. Thome, D.L. Farber, K. Lutfy, P. Seale, and D. Artis Group 2 innate lymphoid cells promote beiging of white adipose tissue and limit obesity Nature 519 2015 242 246
12. J. Brignardello, P. Morales, E. Diaz, J. Romero, O. Brunser, and M. Gotteland Pilot study: alterations of intestinal microbiota in obese humans are not associated with colonic inflammation or disturbances of barrier function Aliment. Pharmacol. Ther. 32 2010 1307 1314
13. E.M. Brown, M. Sadarangani, and B.B. Finlay The role of the immune system in governing host-microbe interactions in the intestine Nat. Immunol. 14 2013 660 667
14. P. Brun, I. Castagliuolo, V. Di Leo, A. Buda, M. Pinzani, G. Palù, and D. Martines Increased intestinal permeability in obese mice: new evidence in the pathogenesis of nonalcoholic steatohepatitis Am. J. Physiol. Gastrointest. Liver Physiol. 292 2007 G518 G525
15. R. Caesar, V. Tremaroli, P. Kovatcheva-Datchary, P.D. Cani, and F. Bäckhed Crosstalk between Gut Microbiota and Dietary Lipids Aggravates WAT Inflammation through TLR Signaling Cell Metab. 22 2015 658 668
16. P.D. Cani, J. Amar, M.A. Iglesias, M. Poggi, C. Knauf, D. Bastelica, A.M. Neyrinck, F. Fava, K.M. Tuohy, C. Chabo, and et al. Metabolic endotoxemia initiates obesity and insulin resistance Diabetes 56 2007 1761 1772
17. P.D. Cani, R. Bibiloni, C. Knauf, A. Waget, A.M. Neyrinck, N.M. Delzenne, and R. Burcelin Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice Diabetes 57 2008 1470 1481
18. E. Cario, I.M. Rosenberg, S.L. Brandwein, P.L. Beck, H.C. Reinecker, and D.K. Podolsky Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing Toll-like receptors J. Immunol. 164 2000 966 972
19. B.M. Carvalho, D. Guadagnini, D.M. Tsukumo, A.A. Schenka, P. Latuf-Filho, J. Vassallo, J.C. Dias, L.T. Kubota, J.B. Carvalheira, and M.J. Saad Modulation of gut microbiota by antibiotics improves insulin signalling in high-fat fed mice Diabetologia 55 2012 2823 2834
20. B. Chassaing, O. Koren, J.K. Goodrich, A.C. Poole, S. Srinivasan, R.E. Ley, and A.T. Gewirtz Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome Nature 519 2015 92 96
21. C.C. Chen, J.L. Huang, C.J. Chang, and M.S. Kong Fecal calprotectin as a correlative marker in clinical severity of infectious diarrhea and usefulness in evaluating bacterial or viral pathogens in children J. Pediatr. Gastroenterol. Nutr. 55 2012 541 547
22. Y. Cong, T. Feng, K. Fujihashi, T.R. Schoeb, and C.O. Elson A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota Proc. Natl. Acad. Sci. USA 106 2009 19256 19261
23. A. Cotillard, S.P. Kennedy, L.C. Kong, E. Prifti, N. Pons, E. Le Chatelier, M. Almeida, B. Quinquis, F. Levenez, N. Galleron, et al. ANR MicroObes consortium Dietary intervention impact on gut microbial gene richness Nature 500 2013 585 588
24. L.M. Cox, S. Yamanishi, J. Sohn, A.V. Alekseyenko, J.M. Leung, I. Cho, S.G. Kim, H. Li, Z. Gao, D. Mahana, and et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences Cell 158 2014 705 721
25. J.D. Crane, R. Palanivel, E.P. Mottillo, A.L. Bujak, H. Wang, R.J. Ford, A. Collins, R.M. Blümer, M.D. Fullerton, J.M. Yabut, and et al. Inhibiting peripheral serotonin synthesis reduces obesity and metabolic dysfunction by promoting brown adipose tissue thermogenesis Nat. Med. 21 2015 166 172
26. C.B. de La Serre, C.L. Ellis, J. Lee, A.L. Hartman, J.C. Rutledge, and H.E. Raybould Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation Am. J. Physiol. Gastrointest. Liver Physiol. 299 2010 G440 G448
27. N.J. de Wit, H. Bosch-Vermeulen, P.J. de Groot, G.J. Hooiveld, M.M. Bromhaar, J. Jansen, M. Müller, and R. van der Meer The role of the small intestine in the development of dietary fat-induced obesity and insulin resistance in C57BL/6J mice BMC Med. Genomics 1 2008 14
28. P. Dehghan, B. Pourghassem Gargari, and M. Asghari Jafar-abadi Oligofructose-enriched inulin improves some inflammatory markers and metabolic endotoxemia in women with type 2 diabetes mellitus: a randomized controlled clinical trial Nutrition 30 2014 418 423
29. E. Denou, K. Lolmède, L. Garidou, C. Pomie, C. Chabo, T.C. Lau, M.D. Fullerton, G. Nigro, A. Zakaroff-Girard, E. Luche, and et al. Defective NOD2 peptidoglycan sensing promotes diet-induced inflammation, dysbiosis, and insulin resistance EMBO Mol. Med. 7 2015 259 274
30. S. Ding, M.M. Chi, B.P. Scull, R. Rigby, N.M. Schwerbrock, S. Magness, C. Jobin, and P.K. Lund High-fat diet: bacteria interactions promote intestinal inflammation which precedes and correlates with obesity and insulin resistance in mouse PLoS ONE 5 2010 e12191
31. A. Everard, C. Belzer, L. Geurts, J.P. Ouwerkerk, C. Druart, L.B. Bindels, Y. Guiot, M. Derrien, G.G. Muccioli, N.M. Delzenne, and et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity Proc. Natl. Acad. Sci. USA 110 2013 9066 9071
32. A. Everard, L. Geurts, R. Caesar, M. Van Hul, S. Matamoros, T. Duparc, R.G. Denis, P. Cochez, F. Pierard, J. Castel, and et al. Intestinal epithelial MyD88 is a sensor switching host metabolism towards obesity according to nutritional status Nat. Commun. 5 2014 5648
33. S. Fang, J.M. Suh, S.M. Reilly, E. Yu, O. Osborn, D. Lackey, E. Yoshihara, A. Perino, S. Jacinto, Y. Lukasheva, and et al. Intestinal FXR agonism promotes adipose tissue browning and reduces obesity and insulin resistance Nat. Med. 21 2015 159 165
34. 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
35. O.M. Finucane, C.M. Reynolds, F.C. McGillicuddy, K.A. Harford, M. Morrison, J. Baugh, and H.M. Roche Macrophage migration inhibitory factor deficiency ameliorates high-fat diet induced insulin resistance in mice with reduced adipose inflammation and hepatic steatosis PLoS ONE 9 2014 e113369
36. S. Fukuda, H. Toh, K. Hase, K. Oshima, Y. Nakanishi, K. Yoshimura, T. Tobe, J.M. Clarke, D.L. Topping, T. Suzuki, and et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate Nature 469 2011 543 547
37. Y. Furusawa, Y. Obata, S. Fukuda, T.A. Endo, G. Nakato, D. Takahashi, Y. Nakanishi, C. Uetake, K. Kato, T. Kato, and et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells Nature 504 2013 446 450
38. N. Gagliani, M.C. Vesely, A. Iseppon, L. Brockmann, H. Xu, N.W. Palm, M.R. de Zoete, P. Licona-Limón, R.S. Paiva, T. Ching, and et al. Th17 cells transdifferentiate into regulatory T cells during resolution of inflammation Nature 523 2015 221 225
39. J. Gagnon, M. Sauvé, W. Zhao, H.M. Stacey, S.C. Wiber, S.S. Bolz, and P.L. Brubaker Chronic Exposure to TNFα Impairs Secretion of Glucagon-Like Peptide-1 Endocrinology 156 2015 3950 3960
40. Z. Gao, J. Yin, J. Zhang, R.E. Ward, R.J. Martin, M. Lefevre, W.T. Cefalu, and J. Ye Butyrate improves insulin sensitivity and increases energy expenditure in mice Diabetes 58 2009 1509 1517
41. L. Garidou, C. Pomié, P. Klopp, A. Waget, J. Charpentier, M. Aloulou, A. Giry, M. Serino, L. Stenman, S. Lahtinen, and et al. The Gut Microbiota Regulates Intestinal CD4 T Cells Expressing RORγt and Controls Metabolic Disease Cell Metab. 22 2015 100 112
42. S. Ghoshal, J. Witta, J. Zhong, W. de Villiers, and E. Eckhardt Chylomicrons promote intestinal absorption of lipopolysaccharides J. Lipid Res. 50 2009 90 97
43. S.R. Gill, M. Pop, R.T. Deboy, P.B. Eckburg, P.J. Turnbaugh, B.S. Samuel, J.I. Gordon, D.A. Relman, C.M. Fraser-Liggett, and K.E. Nelson Metagenomic analysis of the human distal gut microbiome Science 312 2006 1355 1359
44. U. Hadis, B. Wahl, O. Schulz, M. Hardtke-Wolenski, A. Schippers, N. Wagner, W. Müller, T. Sparwasser, R. Förster, and O. Pabst Intestinal tolerance requires gut homing and expansion of FoxP3+ regulatory T cells in the lamina propria Immunity 34 2011 237 246
45. M.K. Hamilton, G. Boudry, D.G. Lemay, and H.E. Raybould Changes in intestinal barrier function and gut microbiota in high-fat diet-fed rats are dynamic and region dependent Am. J. Physiol. Gastrointest. Liver Physiol. 308 2015 G840 G851
46. J. Henao-Mejia, E. Elinav, C. Jin, L. Hao, W.Z. Mehal, T. Strowig, C.A. Thaiss, A.L. Kau, S.C. Eisenbarth, M.J. Jurczak, and et al. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity Nature 482 2012 179 185
47. T. Hisamatsu, M. Suzuki, H.C. Reinecker, W.J. Nadeau, B.A. McCormick, and D.K. Podolsky CARD15/NOD2 functions as an antibacterial factor in human intestinal epithelial cells Gastroenterology 124 2003 993 1000
48. 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
49. Y. Hua, J. Shen, Y. Song, Y. Xing, and X. Ye Interleukin-10 -592C/A, -819C/T and -1082A/G Polymorphisms with Risk of Type 2 Diabetes Mellitus: A HuGE Review and Meta-analysis PLoS ONE 8 2013 e66568
50. 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
51. I.I. Ivanov, K. Atarashi, N. Manel, E.L. Brodie, T. Shima, U. Karaoz, D. Wei, K.C. Goldfarb, C.A. Santee, S.V. Lynch, and et al. Induction of intestinal Th17 cells by segmented filamentous bacteria Cell 139 2009 485 498
52. A.M. Johnson, A. Costanzo, M.G. Gareau, A.M. Armando, O. Quehenberger, J.M. Jameson, and J.M. Olefsky High fat diet causes depletion of intestinal eosinophils associated with intestinal permeability PLoS ONE 10 2015 e0122195
53. F.H. Karlsson, V. Tremaroli, I. Nookaew, G. Bergström, C.J. Behre, B. Fagerberg, J. Nielsen, and F. Bäckhed Gut metagenome in European women with normal, impaired and diabetic glucose control Nature 498 2013 99 103
54. L. Kjer-Nielsen, O. Patel, A.J. Corbett, J. Le Nours, B. Meehan, L. Liu, M. Bhati, Z. Chen, L. Kostenko, R. Reantragoon, and et al. MR1 presents microbial vitamin B metabolites to MAIT cells Nature 491 2012 717 723
55. J.A. Kummer, R. Broekhuizen, H. Everett, L. Agostini, L. Kuijk, F. Martinon, R. van Bruggen, and J. Tschopp Inflammasome components NALP 1 and 3 show distinct but separate expression profiles in human tissues suggesting a site-specific role in the inflammatory response J. Histochem. Cytochem. 55 2007 443 452
56. G. Lalazar, M. Mizrahi, I. Turgeman, T. Adar, A. Ben Ya'acov, Y. Shabat, A. Nimer, N. Hemed, L. Zolotarovya, Y. Lichtenstein, and et al. Oral Administration of OKT3 MAb to Patients with NASH, Promotes Regulatory T-cell Induction, and Alleviates Insulin Resistance: Results of a Phase IIa Blinded Placebo-Controlled Trial J. Clin. Immunol. 35 2015 399 407
57. Y.Y. Lam, C.W. Ha, C.R. Campbell, A.J. Mitchell, A. Dinudom, J. Oscarsson, D.I. Cook, N.H. Hunt, I.D. Caterson, A.J. Holmes, and L.H. Storlien Increased gut permeability and microbiota change associate with mesenteric fat inflammation and metabolic dysfunction in diet-induced obese mice PLoS ONE 7 2012 e34233
58. Y.Y. Lam, C.W. Ha, J.M. Hoffmann, J. Oscarsson, A. Dinudom, T.J. Mather, D.I. Cook, N.H. Hunt, I.D. Caterson, A.J. Holmes, and L.H. Storlien Effects of dietary fat profile on gut permeability and microbiota and their relationships with metabolic changes in mice Obesity (Silver Spring) 23 2015 1429 1439
59. E. Le Chatelier, T. Nielsen, J. Qin, E. Prifti, F. Hildebrand, G. Falony, M. Almeida, M. Arumugam, J.M. Batto, S. Kennedy, et al. MetaHIT consortium Richness of human gut microbiome correlates with metabolic markers Nature 500 2013 541 546
60. R.E. Ley, F. Bäckhed, P. Turnbaugh, C.A. Lozupone, R.D. Knight, and J.I. Gordon Obesity alters gut microbial ecology Proc. Natl. Acad. Sci. USA 102 2005 11070 11075
61. H. Li, C. Lelliott, P. Håkansson, K. Ploj, A. Tuneld, M. Verolin-Johansson, L. Benthem, B. Carlsson, L. Storlien, and E. Michaëlsson Intestinal, adipose, and liver inflammation in diet-induced obese mice Metabolism 57 2008 1704 1710
62. Z. Liu, R.S. Brooks, E.D. Ciappio, S.J. Kim, J.W. Crott, G. Bennett, A.S. Greenberg, and J.B. Mason Diet-induced obesity elevates colonic TNF-α in mice and is accompanied by an activation of Wnt signaling: a mechanism for obesity-associated colorectal cancer J. Nutr. Biochem. 23 2012 1207 1213
63. H. Luck, S. Tsai, J. Chung, X. Clemente-Casares, M. Ghazarian, X.S. Revelo, H. Lei, C.T. Luk, S.Y. Shi, A. Surendra, and et al. Regulation of obesity-related insulin resistance with gut anti-inflammatory agents Cell Metab. 21 2015 527 542
64. S. Lukovac, C. Belzer, L. Pellis, B.J. Keijser, W.M. de Vos, R.C. Montijn, and G. Roeselers Differential modulation by Akkermansia muciniphila and Faecalibacterium prausnitzii of host peripheral lipid metabolism and histone acetylation in mouse gut organoids MBio 5 2014 5
65. 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
66. I. Magalhaes, K. Pingris, C. Poitou, S. Bessoles, N. Venteclef, B. Kiaf, L. Beaudoin, J. Da Silva, O. Allatif, J. Rossjohn, and et al. Mucosal-associated invariant T cell alterations in obese and type 2 diabetic patients J. Clin. Invest. 125 2015 1752 1762
67. K.M. Maslowski, A.T. Vieira, A. Ng, J. Kranich, F. Sierro, D. Yu, H.C. Schilter, M.S. Rolph, F. Mackay, D. Artis, and et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43 Nature 461 2009 1282 1286
68. C.L. Maynard, C.O. Elson, R.D. Hatton, and C.T. Weaver Reciprocal interactions of the intestinal microbiota and immune system Nature 489 2012 231 241
69. + dendritic cells Immunity 40 2014 248 261
70. M. Membrez, F. Blancher, M. Jaquet, R. Bibiloni, P.D. Cani, R.G. Burcelin, I. Corthesy, K. Mace, and C.J. Chou Gut microbiota modulation with norfloxacin and ampicillin enhances glucose tolerance in mice FASEB J. 22 2008 2416 2426
71. N. Mito, T. Kaburagi, H. Yoshino, A. Imai, and K. Sato Oral-tolerance induction in diet-induced obese mice Life Sci. 79 2006 1056 1061
72. 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
73. M. Monteiro-Sepulveda, S. Touch, C. Mendes-Sá, S. André, C. Poitou, O. Allatif, A. Cotillard, H. Fohrer-Ting, E.L. Hubert, R. Remark, and et al. Jejunal T Cell Inflammation in Human Obesity Correlates with Decreased Enterocyte Insulin Signaling Cell Metab. 22 2015 113 124
74. A.M. Morton, E. Sefik, R. Upadhyay, R. Weissleder, C. Benoist, and D. Mathis Endoscopic photoconversion reveals unexpectedly broad leukocyte trafficking to and from the gut Proc. Natl. Acad. Sci. USA 111 2014 6696 6701
75. A. Moya-Pérez, A. Neef, and Y. Sanz Bifidobacterium pseudocatenulatum CECT 7765 Reduces Obesity-Associated Inflammation by Restoring the Lymphocyte-Macrophage Balance and Gut Microbiota Structure in High-Fat Diet-Fed Mice PLoS ONE 10 2015 e0126976
76. 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
77. J.M. Olefsky, and C.K. Glass Macrophages, inflammation, and insulin resistance Annu. Rev. Physiol. 72 2010 219 246
78. O. Pabst, and A.M. Mowat Oral tolerance to food protein Mucosal Immunol. 5 2012 232 239
79. S. Pendyala, L.M. Neff, M. Suárez-Fariñas, and P.R. Holt Diet-induced weight loss reduces colorectal inflammation: implications for colorectal carcinogenesis Am. J. Clin. Nutr. 93 2011 234 242
80. J. Qin, Y. Li, Z. Cai, S. Li, J. Zhu, F. Zhang, S. Liang, W. Zhang, Y. Guan, D. Shen, and et al. A metagenome-wide association study of gut microbiota in type 2 diabetes Nature 490 2012 55 60
81. E. Quévrain, M.A. Maubert, C. Michon, F. Chain, R. Marquant, J. Tailhades, S. Miquel, L. Carlier, L.G. Bermúdez-Humarán, B. Pigneur, and et al. Identification of an anti-inflammatory protein from Faecalibacterium prausnitzii, a commensal bacterium deficient in Crohn's disease Gut 2015 gutjnl-2014-307649
82. X.S. Revelo, S. Tsai, H. Lei, H. Luck, M. Ghazarian, H. Tsui, S.Y. Shi, S. Schroer, C. Luk, G.H. Lin, and et al. Perforin is a novel immune regulator of obesity-related insulin resistance Diabetes 64 2014 90 103
83. A. Rivollier, J. He, A. Kole, V. Valatas, and B.L. Kelsall Inflammation switches the differentiation program of Ly6Chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon J. Exp. Med. 209 2012 139 155
84. C. Rousseaux, B. Lefebvre, L. Dubuquoy, P. Lefebvre, O. Romano, J. Auwerx, D. Metzger, W. Wahli, B. Desvergne, G.C. Naccari, and et al. Intestinal antiinflammatory effect of 5-aminosalicylic acid is dependent on peroxisome proliferator-activated receptor-gamma J. Exp. Med. 201 2005 1205 1215
85. M. Saxena, N. Srivastava, and M. Banerjee Association of IL-6, TNF-α and IL-10 gene polymorphisms with type 2 diabetes mellitus Mol. Biol. Rep. 40 2013 6271 6279
86. J.D. Schertzer, A.K. Tamrakar, J.G. Magalhães, S. Pereira, P.J. Bilan, M.D. Fullerton, Z. Liu, G.R. Steinberg, A. Giacca, D.J. Philpott, and A. Klip NOD1 activators link innate immunity to insulin resistance Diabetes 60 2011 2206 2215
87. O. Schulz, E. Jaensson, E.K. Persson, X. Liu, T. Worbs, W.W. Agace, and O. Pabst Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions J. Exp. Med. 206 2009 3101 3114
88. A. Schwiertz, D. Taras, K. Schäfer, S. Beijer, N.A. Bos, C. Donus, and P.D. Hardt Microbiota and SCFA in lean and overweight healthy subjects Obesity (Silver Spring) 18 2010 190 195
89. G.F. Sonnenberg, L.A. Monticelli, T. Alenghat, T.C. Fung, N.A. Hutnick, J. Kunisawa, N. Shibata, S. Grunberg, R. Sinha, A.M. Zahm, and et al. Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria Science 336 2012 1321 1325
90. H. Spits, D. Artis, M. Colonna, A. Diefenbach, J.P. Di Santo, G. Eberl, S. Koyasu, R.M. Locksley, A.N. McKenzie, R.E. Mebius, and et al. Innate lymphoid cells - a proposal for uniform nomenclature Nat. Rev. Immunol. 13 2013 145 149
91. C.M. Sun, J.A. Hall, R.B. Blank, N. Bouladoux, M. Oukka, J.R. Mora, and Y. Belkaid Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid J. Exp. Med. 204 2007 1775 1785
92. J.R. Swann, E.J. Want, F.M. Geier, K. Spagou, I.D. Wilson, J.E. Sidaway, J.K. Nicholson, and E. Holmes Systemic gut microbial modulation of bile acid metabolism in host tissue compartments Proc. Natl. Acad. Sci. USA 108 Suppl 1 2011 4523 4530
93. S. Talukdar, Y. Oh, G. Bandyopadhyay, D. Li, J. Xu, J. McNelis, M. Lu, P. Li, Q. Yan, Y. Zhu, and et al. Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase Nat. Med. 18 2012 1407 1412
94. C. Thomas, A. Gioiello, L. Noriega, A. Strehle, J. Oury, G. Rizzo, A. Macchiarulo, H. Yamamoto, C. Mataki, M. Pruzanski, and et al. TGR5-mediated bile acid sensing controls glucose homeostasis Cell Metab. 10 2009 167 177
95. A.W. Thomson, and P.A. Knolle Antigen-presenting cell function in the tolerogenic liver environment Nat. Rev. Immunol. 10 2010 753 766
96. K. Tiihonen, A.C. Ouwehand, and N. Rautonen Effect of overweight on gastrointestinal microbiology and immunology: correlation with blood biomarkers Br. J. Nutr. 103 2010 1070 1078
97. V. Tremaroli, and F. Bäckhed Functional interactions between the gut microbiota and host metabolism Nature 489 2012 242 249
98. V. Tremaroli, F. Karlsson, M. Werling, M. Ståhlman, P. Kovatcheva-Datchary, T. Olbers, L. Fändriks, C.W. le Roux, J. Nielsen, and F. Bäckhed Roux-en-Y Gastric Bypass and Vertical Banded Gastroplasty Induce Long-Term Changes on the Human Gut Microbiome Contributing to Fat Mass Regulation Cell Metab. 22 2015 228 238
99. P.J. Turnbaugh, R.E. Ley, M.A. Mahowald, V. Magrini, E.R. Mardis, and J.I. Gordon An obesity-associated gut microbiome with increased capacity for energy harvest Nature 444 2006 1027 1031
100. P.J. Turnbaugh, V.K. Ridaura, J.J. Faith, F.E. Rey, R. Knight, and J.I. Gordon The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice Sci. Transl. Med. 1 2009 6ra14
101. S. Ussar, N.W. Griffin, O. Bezy, S. Fujisaka, S. Vienberg, S. Softic, L. Deng, L. Bry, J.I. Gordon, and C.R. Kahn Interactions between Gut Microbiota, Host Genetics and Diet Modulate the Predisposition to Obesity and Metabolic Syndrome Cell Metab. 22 2015 516 530
102. S. Vaishnava, M. Yamamoto, K.M. Severson, K.A. Ruhn, X. Yu, O. Koren, R. Ley, E.K. Wakeland, and L.V. Hooper The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine Science 334 2011 255 258
103. 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
104. A. Veilleux, S. Mayeur, J.C. Bérubé, J.F. Beaulieu, E. Tremblay, F.S. Hould, Y. Bossé, D. Richard, and E. Levy Altered intestinal functions and increased local inflammation in insulin-resistant obese subjects: a gene-expression profile analysis BMC Gastroenterol. 15 2015 119
105. M. Vijay-Kumar, J.D. Aitken, F.A. Carvalho, T.C. Cullender, S. Mwangi, S. Srinivasan, S.V. Sitaraman, R. Knight, R.E. Ley, and A.T. Gewirtz Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5 Science 328 2010 228 231
106. A. Vrieze, E. Van Nood, F. Holleman, J. Salojarvi, R.S. Kootte, J.F. Bartelsman, G.M. Dallinga-Thie, M.T. Ackermans, M.J. Serlie, R. Oozeer, and et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome Gastroenterology 143 2012 913 916 e7
107. N. Wagner, J. Löhler, E.J. Kunkel, K. Ley, E. Leung, G. Krissansen, K. Rajewsky, and W. Müller Critical role for beta7 integrins in formation of the gut-associated lymphoid tissue Nature 382 1996 366 370
108. Y. Wang, J. Li, L. Tang, Y. Wang, R. Charnigo, W. de Villiers, and E. Eckhardt T-lymphocyte responses to intestinally absorbed antigens can contribute to adipose tissue inflammation and glucose intolerance during high fat feeding PLoS ONE 5 2010 e13951
109. 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
110. 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
111. 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
112. F.M. Wensveen, V. Jelenčić, S. Valentić, M. Šestan, T.T. Wensveen, S. Theurich, A. Glasner, D. Mendrila, D. Štimac, F.T. Wunderlich, and et al. NK cells link obesity-induced adipose stress to inflammation and insulin resistance Nat. Immunol. 16 2015 376 385
113. S. Winer, Y. Chan, G. Paltser, D. Truong, H. Tsui, J. Bahrami, R. Dorfman, Y. Wang, J. Zielenski, F. Mastronardi, and et al. Normalization of obesity-associated insulin resistance through immunotherapy Nat. Med. 15 2009 921 929
114. D.A. Winer, S. Winer, L. Shen, P.P. Wadia, J. Yantha, G. Paltser, H. Tsui, P. Wu, M.G. Davidson, M.N. Alonso, and et al. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies Nat. Med. 17 2011 610 617
115. M. Wlodarska, C.A. Thaiss, R. Nowarski, J. Henao-Mejia, J.P. Zhang, E.M. Brown, G. Frankel, M. Levy, M.N. Katz, W.M. Philbrick, and et al. NLRP6 inflammasome orchestrates the colonic host-microbial interface by regulating goblet cell mucus secretion Cell 156 2014 1045 1059
116. J.J. Worthington, B.I. Czajkowska, A.C. Melton, and M.A. Travis Intestinal dendritic cells specialize to activate transforming growth factor-β and induce Foxp3+ regulatory T cells via integrin αvβ8 Gastroenterology 141 2011 1802 1812
117. 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
118. G.D. Wu, J. Chen, C. Hoffmann, K. Bittinger, Y.Y. Chen, S.A. Keilbaugh, M. Bewtra, D. Knights, W.A. Walters, R. Knight, and et al. Linking long-term dietary patterns with gut microbial enterotypes Science 334 2011 105 108
119. 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
120. Y. Yan, W. Jiang, T. Spinetti, A. Tardivel, R. Castillo, C. Bourquin, G. Guarda, Z. Tian, J. Tschopp, and R. Zhou Omega-3 fatty acids prevent inflammation and metabolic disorder through inhibition of NLRP3 inflammasome activation Immunity 38 2013 1154 1163
121. H. Zhang, J.K. DiBaise, A. Zuccolo, D. Kudrna, M. Braidotti, Y. Yu, P. Parameswaran, M.D. Crowell, R. Wing, B.E. Rittmann, and R. Krajmalnik-Brown Human gut microbiota in obesity and after gastric bypass Proc. Natl. Acad. Sci. USA 106 2009 2365 2370
122. Y. Zheng, P.A. Valdez, D.M. Danilenko, Y. Hu, S.M. Sa, Q. Gong, A.R. Abbas, Z. Modrusan, N. Ghilardi, F.J. de Sauvage, and W. Ouyang Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens Nat. Med. 14 2008 282 289
123. B.H. Zinselmeyer, J. Dempster, A.M. Gurney, D. Wokosin, M. Miller, H. Ho, O.R. Millington, K.M. Smith, C.M. Rush, I. Parker, and et al. In situ characterization of CD4+ T cell behavior in mucosal and systemic lymphoid tissues during the induction of oral priming and tolerance J. Exp. Med. 201 2005 1815 1823