Gut microbiota and immune crosstalk in metabolic disease

Molecular Metabolism

Volumn 5, Issue 9, 2016, Pages 771-781

  Burcelin, Rémy ^a,b  

^a INSERM   (France)

^b Departments of Clinical Biochemistry and Sports Medicine   (France)

Author keywords

Bacterial translocation; Intestinal immune system; Microbiota; Obesity; Type 2 diabetes

Indexed keywords

ADAPTIVE IMMUNITY; BACTERIAL TRANSLOCATION; CYTOKINE PRODUCTION; DYSBIOSIS; HOST PATHOGEN INTERACTION; HUMAN; HYPERGLYCEMIA; IMMUNE SYSTEM; IMMUNOREGULATION; INFLAMMATION; INNATE IMMUNITY; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; METABOLIC DISORDER; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE;

EID: 84991043156     PISSN: None     EISSN: 22128778     Source Type: Journal    
DOI: 10.1016/j.molmet.2016.05.016     Document Type: Review

References (122)

1. [1] Turnbaugh, P., Ridaura, V., Faith, J., et al. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Science Translational Medicine 1 (2009), 6–14.
2. [2] Vrieze, A., Van Nood, E., Holleman, F., et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143 (2012), 913 e7–916 e7.
3. [3] Lu, Y., Loos, R.J., Obesity genomics: assessing the transferability of susceptibility loci across diverse populations. Genome Medicine, 5, 2013, 55.
4. [4] Ley, R.E., Backhed, F., Turnbaugh, P., et al. Obesity alters gut microbial ecology. Proceedings of the National Academy of Sciences of the United States of America 102 (2005), 11070–11075.
5. [5] Cani, P.D., Amar, J., Iglesias, M.A., et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56 (2007), 1761–1772.
6. [6] Cani, P.D., Bibiloni, R., Knauf, C., et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57 (2008), 1470–1481.
7. [7] Le Chatelier, E., Nielsen, T., Qin, J., et al. Richness of human gut microbiome correlates with metabolic markers. Nature 500 (2013), 541–546.
8. [8] Arumugam, M., Raes, J., Pelletier, E., et al. Enterotypes of the human gut microbiome. Nature 473 (2011), 174–180.
9. [9] Li, J., Jia, H., Cai, X., et al. An integrated catalog of reference genes in the human gut microbiome. Nature Biotechnology 32 (2014), 834–841.
10. [10] Qin, J., Li, R., Raes, J., et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464 (2010), 59–65.
11. [11] Qin, J., Li, Y., Cai, Z., et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490 (2012), 55–60.
12. [12] Cummings, J.H., Macfarlane, G.T., Role of intestinal bacteria in nutrient metabolism. JPEN (Journal of Parenteral and Enteral Nutrition) 21 (1997), 357–365.
13. [13] Gibson, G.R., Dietary modulation of the human gut microflora using prebiotics. The British Journal of Nutrition 80 (1998), S209–S212.
14. [14] Clavel, T., Borrmann, D., Braune, A., et al. Occurrence and activity of human intestinal bacteria involved in the conversion of dietary lignans. Anaerobe 12 (2006), 140–147.
15. [15] Cani, P.D., Neyrinck, A.M., Fava, F., et al. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 50 (2007), 2374–2383.
16. [16] Flint, H.J., Duncan, S.H., Scott, K.P., Louis, P., Interactions and competition within the microbial community of the human colon: links between diet and health. Environmental Microbiology 9 (2007), 1101–1111.
17. [17] Turnbaugh, P.J., Backhed, F., Fulton, L., Gordon, J.I., Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host & Microbe 3 (2008), 213–223.
18. [18] Amar, J., Chabo, C., Waget, A., et al. Intestinal mucosal adherence and translocation of commensal bacteria at the early onset of type 2 diabetes: molecular mechanisms and probiotic treatment. EMBO Molecular Medicine 3 (2011), 559–572.
19. [19] Raso, G.M., Simeoli, R., Iacono, A., et al. Effects of a Lactobacillus paracasei B21060 based synbiotic on steatosis, insulin signaling and toll-like receptor expression in rats fed a high-fat diet. The Journal of Nutritional Biochemistry 25 (2014), 81–90.
20. [20] Martinez-Medina, M., Denizot, J., Dreux, N., et al. Western diet induces dysbiosis with increased E. coli in CEABAC10 mice, alters host barrier function favouring AIEC colonisation. Gut 63 (2014), 116–124.
21. [21] Wang, X., Ota, N., Manzanillo, P., et al. Interleukin-22 alleviates metabolic disorders and restores mucosal immunity in diabetes. Nature, 2014.
22. [22] Backhed, F., Ding, H., Wang, T., et al. The gut microbiota as an environmental factor that regulates fat storage. Proceedings of the National Academy of Sciences of the United States of America 101 (2004), 15718–15723.
23. [23] Turnbaugh, P.J., Ley, R.E., Mahowald, M.A., et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444 (2006), 1027–1031.
24. [24] Hotamisligil, G.S., Inflammation and metabolic disorders. Nature 444 (2006), 860–867.
25. [25] Shoelson, S.E., Lee, J., Goldfine, A.B., Inflammation and insulin resistance. Journal of Clinical Investigation 116 (2006), 1793–1801.
26. [26] Bouloumie, A., Curat, C.A., Sengenes, C., et al. Role of macrophage tissue infiltration in metabolic diseases. Current Opinion in Clinical Nutrition and Metabolic Care 8 (2005), 347–354.
27. [27] Weisberg, S.P., Hunter, D., Huber, R., et al. CCR2 modulates inflammatory and metabolic effects of high-fat feeding. Journal of Clinical Investigation 116 (2006), 115–124.
28. [28] Tanti, J., Gual, P., Gremeaux, T., et al. Alteration in insulin action: role of IRS-1 serine phsophorylation in the retroregulation of insulin signalling. Annales d'Endocrinologie 65 (2004), 43–48.
29. [29] Bloch-Damti, A., Potashnik, R., Gual, P., et al. Differential effects of IRS1 phosphorylated on Ser307 or Ser632 in the induction of insulin resistance by oxidative stress. Diabetologia 49 (2006), 2463–2473.
30. [30] Lumeng, C.N., Bodzin, J.L., Saltiel, A.R., Obesity induces a phenotypic switch in adipose tissue macrophage polarization. Journal of Clinical Investigation 117 (2007), 175–184.
31. [31] Winer, D.A., Winer, S., Shen, L., et al. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nature Medicine 17 (2011), 610–617.
32. [32] Winer, S., Chan, Y., Paltser, G., et al. Normalization of obesity-associated insulin resistance through immunotherapy. Nature Medicine 15 (2009), 921–929.
33. [33] Nishimura, S., Manabe, I., Nagasaki, M., et al. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nature Medicine 15 (2009), 914–920.
34. [34] Cavallari, J.F., Denou, E., Foley, K.P., et al. Different Th17 immunity in gut, liver, and adipose tissues during obesity: the role of diet, genetics, and microbes. Gut Microbes 7 (2016), 82–89.
35. [35] Ohmura, K., Ishimori, N., Ohmura, Y., et al. Natural killer T cells are involved in adipose tissues inflammation and glucose intolerance in diet-induced obese mice. Arteriosclerosis Thrombosis and Vascular Biology 30 (2010), 193–199.
36. [36] Garidou, L., Pomie, C., Klopp, P., et al. The gut microbiota regulates intestinal CD4 T cells expressing RORgammat and controls metabolic disease. Cell Metabolism 22 (2015), 100–112.
37. [37] DeFuria, J., Belkina, A.C., Jagannathan-Bogdan, M., et al. B cells promote inflammation in obesity and type 2 diabetes through regulation of T-cell function and an inflammatory cytokine profile. Proceedings of the National Academy of Sciences of the United States of America 110 (2013), 5133–5138.
38. [38] Cousin, B., Andre, M., Arnaud, E., et al. Reconstitution of lethally irradiated mice by cells isolated from adipose tissue. Biochemical and Biophysical Research 301 (2003), 1016–1022.
39. [39] Burcelin, R., Garidou, L., Pomie, C., Immuno-microbiota cross and talk: the new paradigm of metabolic diseases. Seminars in Immunology 24 (2012), 67–74.
40. [40] Amar, J., Burcelin, R., Ruidavets, J.B., et al. Energy intake is associated with endotoxemia in apparently healthy men. American Journal of Clinical Nutrition 87 (2008), 1219–1223.
41. [41] Lassenius, M.I., Pietilainen, K.H., Kaartinen, K., et al. Bacterial endotoxin activity in human serum is associated with dyslipidemia, insulin resistance, obesity, and chronic inflammation. Diabetes Care 34 (2011), 1809–1815.
42. [42] Luche, E., Cousin, B., Garidou, L., et al. Metabolic endotoxemia directly increases the proliferation of adipocyte precursors at the onset of metabolic diseases through a CD14-dependent mechanism. Molecular Metabolism 2 (2013), 281–291.
43. [43] Ghoshal, S., Witta, J., Zhong, J., et al. Chylomicrons promote intestinal absorption of lipopolysaccharides. Journal of Lipid Research 50 (2009), 90–97.
44. [44] Schnaitman, C.A., Klena, J.D., Genetics of lipopolysaccharide biosynthesis in enteric bacteria. Microbiological Reviews 57 (1993), 655–682.
45. [45] D'Hauteville, H., Khan, S., Maskell, D.J., et al. Two msbB genes encoding maximal acylation of lipid A are required for invasive Shigella flexneri to mediate inflammatory rupture and destruction of the intestinal epithelium. Journal of Immunology 168 (2002), 5240–5251.
46. [46] Haziot, A., Rong, G.W., Lin, X.Y., et al. Recombinant soluble CD14 prevents mortality in mice treated with endotoxin (lipopolysaccharide). Journal of Immunology 154 (1995), 6529–6532.
47. [47] Wright, S.D., Ramos, R.A., Tobias, P.S., et al. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249 (1990), 1431–1433.
48. [48] Schutt, C., Schilling, T., Grunwald, U., et al. Endotoxin-neutralizing capacity of soluble CD14. Research in Immunology 143 (1992), 71–78.
49. [49] Grunwald, U., Kruger, C., Schutt, C., Endotoxin-neutralizing capacity of soluble CD14 is a highly conserved specific function. Circulatory Shock 39 (1993), 220–225.
50. [50] Schumann, R.R., Leong, S.R., Flaggs, G.W., et al. Structure and function of lipopolysaccharide binding protein. Science 249 (1990), 1429–1431.
51. [51] Kitchens, R.L., Thompson, P.A., Modulatory effects of sCD14 and LBP on LPS-host cell interactions. Journal of Endotoxin Research 11 (2005), 225–229.
52. [52] Jialal, I., Devaraj, S., Bettaieb, A., et al. Increased adipose tissue secretion of Fetuin-A, lipopolysaccharide-binding protein and high-mobility group box protein 1 in metabolic syndrome. Atherosclerosis 241 (2015), 130–137.
53. [53] Fernandez-Real, J.M., Broch, M., Richart, C., et al. CD14 monocyte receptor, involved in the inflammatory cascade, and insulin sensitivity. The Journal of Cinical Endocrinology and Metabolism 88 (2003), 1780–1784.
54. [54] Moreno-Navarrete, J.M., Ortega, F., Serino, M., et al. Circulating lipopolysaccharide-binding protein (LBP) as a marker of obesity-related insulin resistance. International Journal of Obesity (London) 36 (2012), 1442–1449.
55. [55] Morel, D.W., DiCorleto, P.E., Chisolm, G.M., Modulation of endotoxin-induced endothelial cell toxicity by low density lipoprotein. Laboratory Investigation; a Journal of Technical Methods and Pathology 55 (1986), 419–426.
56. [56] Maziere, C., Conte, M.A., Dantin, F., Maziere, J.C., Lipopolysaccharide enhances oxidative modification of low density lipoprotein by copper ions, endothelial and smooth muscle cells. Atherosclerosis 143 (1999), 75–80.
57. [57] Kitchens, R.L., Thompson, P.A., Viriyakosol, S., et al. Plasma CD14 decreases monocyte responses to LPS by transferring cell-bound LPS to plasma lipoproteins. Journal of Clinical Investigation 108 (2001), 485–493.
58. [58] Harris, H.W., Gosnell, J.E., Kumwenda, Z.L., The lipemia of sepsis: triglyceride-rich lipoproteins as agents of innate immunity. Journal of Endotoxin Research 6 (2000), 421–430.
59. [59] Gupta, H., Dai, L., Datta, G., et al. Inhibition of lipopolysaccharide-induced inflammatory responses by an apolipoprotein AI mimetic peptide. Circulation Research 97 (2005), 236–243.
60. [60] Chaby, R., Lipopolysaccharide-binding molecules: transporters, blockers and sensors. Cellular and Molecular Life Sciences 61 (2004), 1697–1713.
61. [61] Rensen, P.C., Oosten, M., Bilt, E., et al. Human recombinant apolipoprotein E redirects lipopolysaccharide from Kupffer cells to liver parenchymal cells in rats in vivo. Journal of Clinical Investigation 99 (1997), 2438–2445.
62. [62] Yan, Y.J., Li, Y., Lou, B., Wu, M.P., Beneficial effects of ApoA-I on LPS-induced acute lung injury and endotoxemia in mice. Life Sciences 79 (2006), 210–215.
63. [63] Kasravi, F.B., Welch, W.J., Peters-Lideu, C.A., et al. Induction of cytokine tolerance in rodent hepatocytes by chylomicron-bound LPS is low-density lipoprotein receptor dependent. Shock 19 (2003), 157–162.
64. [64] Vreugdenhil, A.C., Rousseau, C.H., Hartung, T., et al. Lipopolysaccharide (LPS)-binding protein mediates LPS detoxification by chylomicrons. Journal of Immunology 170 (2003), 1399–1405.
65. [65] Verges, B., Duvillard, L., Lagrost, L., et al. Changes in lipoprotein kinetics associated with type 2 diabetes affect the distribution of lipopolysaccharides among lipoproteins. The Journal of Cinical Endocrinology and Metabolism, 2014, jc20133463.
66. [66] Paulos, C.M., Wrzesinski, C., Kaiser, A., et al. Microbial translocation augments the function of adoptively transferred self/tumor-specific CD8+ T cells via TLR4 signaling. Journal of Clinical Investigation 117 (2007), 2197–2204.
67. [67] Bassols, J., Ortega, F.J., Moreno-Navarrete, J.M., et al. Study of the proinflammatory role of human differentiated omental adipocytes. Journal of Cellular Biochemistry 107 (2009), 1107–1117.
68. [68] Moreira, A.P., Texeira, T.F., Ferreira, A.B., et al. Influence of a high-fat diet on gut microbiota, intestinal permeability and metabolic endotoxaemia. The British Journal of Nutrition 108 (2012), 801–809.
69. [69] Sakakibara, A., Furuse, M., Saitou, M., et al. Possible involvement of phosphorylation of occludin in tight junction formation. Journal of Cell Biology 137 (1997), 1393–1401.
70. [70] Cao, M., Wang, P., Sun, C., et al. Amelioration of IFN-gamma and TNF-alpha-induced intestinal epithelial barrier dysfunction by berberine via suppression of MLCK-MLC phosphorylation signaling pathway. PLoS One, 8, 2013, e61944.
71. [71] Rescigno, M., Urbano, M., Valzasina, B., et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nature Immunology 2 (2001), 361–367.
72. [72] Berg, R.D., Bacterial translocation from the gastrointestinal tract. Trends in Microbiology 3 (1995), 149–154.
73. [73] Berg, R.D., Wommack, E., Deitch, E.A., Immunosuppression and intestinal bacterial overgrowth synergistically promote bacterial translocation. Archives of Surgery 123 (1988), 1359–1364.
74. [74] Moore, F., Moore, E., Poggetti, R., et al. Gut bacterial translocation via the portal vein: a clinical perspective with major torso trauma. Journal of Trauma 31 (1991), 629–636.
75. [75] Stoidis, C.N., Misiakos, E.P., Patapis, P., et al. Potential benefits of pro- and prebiotics on intestinal mucosal immunity and intestinal barrier in short bowel syndrome. Nutrition Research Reviews, 2010, 1–9.
76. [76] Koh, I.H., Liberatore, A.M., Menchaca-Diaz, J.L., et al. Bacterial translocation, microcirculation injury and sepsis. Endocrine, Metabolic & Immune Disorders Drug Targets 6 (2006), 143–150.
77. [77] Imai, A., Kurihara, Y., Endogenous infection in mice with streptozotocin-induced diabetes. A feature of bacterial translocation. Canadian Journal of Microbiology 30 (1984), 1344–1348.
78. [78] Suzuki, T., Itoh, K., Hagiwara, T., et al. Inhibition of bacterial translocation from the gastrointestinal tract of mice injected with cyclophosphamide. Current Microbiology 33 (1996), 78–83.
79. [79] Salzedas-Netto, A.A., Silva, R.M., Martins, J.L., et al. Can bacterial translocation be a beneficial event?. Transplantation Proceedings 38 (2006), 1836–1837.
80. [80] Abe, F., Muto, M., Yaeshima, T., et al. Safety evaluation of probiotic bifidobacteria by analysis of mucin degradation activity and translocation ability. Anaerobe 16 (2010), 131–136.
81. [81] Barreau, F., Madre, C., Meinzer, U., et al. Nod2 regulates the host response towards microflora by modulating T cell function and epithelial permeability in mouse Peyer's patches. Gut 59 (2010), 207–217.
82. [82] Denou, E., Lolmede, K., Garidou, L., et al. Defective NOD2 peptidoglycan sensing promotes diet-induced inflammation, dysbiosis, and insulin resistance. EMBO Molecular Medicine, 2015.
83. [83] Stenman, L.K., Waget, A., Garret, C., et al. Potential probiotic Bifidobacterium animalis ssp. lactis 420 prevents weight gain and glucose intolerance in diet-induced obese mice. Beneficial Microbes 5 (2014), 437–445.
84. [84] Osman, N., Adawi, D., Molin, G., et al. Bifidobacterium infantis strains with and without a combination of oligofructose and inulin (OFI) attenuate inflammation in DSS-induced colitis in rats. BMC Gastroenterology, 6, 2006, 31.
85. [85] Wang, Z., Xiao, G., Yao, Y., et al. The role of bifidobacteria in gut barrier function after thermal injury in rats. Journal of Trauma 61 (2006), 650–657.
86. [86] Lluch, J., Servant, F., Paisse, S., et al. The characterization of novel tissue microbiota using an optimized 16S metagenomic sequencing pipeline. PLoS One, 10, 2015, e0142334.
87. [87] Paisse, S., Valle, C., Servant, F., et al. Comprehensive description of blood microbiome from healthy donors assessed by 16S targeted metagenomic sequencing. Transfusion, 2016.
88. [88] Amar, J., Serino, M., Lange, C., et al. Involvement of tissue bacteria in the onset of diabetes in humans: evidence for a concept. Diabetologia 54 (2011), 3055–3061.
89. [89] Amar, J., Lange, C., Payros, G., et al. Blood microbiota dysbiosis is associated with the onset of cardiovascular events in a large general population: the D.E.S.I.R. study. PLoS One, 8, 2013, e54461.
90. [90] Burcelin, R., Serino, M., Chabo, C., et al. Metagenome and metabolism: the tissue microbiota hypothesis. Diabetes, Obesity & Metabolism 15:Suppl 3 (2013), 61–70.
91. [91] Vora, P., Youdim, A., Thomas, L.S., et al. Beta-defensin-2 expression is regulated by TLR signaling in intestinal epithelial cells. Journal of Immunology 173 (2004), 5398–5405.
92. [92] Menendez, A., Willing, B.P., Montero, M., et al. Bacterial stimulation of the TLR-MyD88 pathway modulates the homeostatic expression of ileal Paneth cell alpha-defensins. Journal of Innate Immunity 5 (2013), 39–49.
93. [93] Hodin, C.M., Verdam, F.J., Grootjans, J., et al. Reduced Paneth cell antimicrobial protein levels correlate with activation of the unfolded protein response in the gut of obese individuals. The Journal of Pathology 225 (2011), 276–284.
94. [94] Yilmaz, D., Guncu, G.N., Kononen, E., et al. Overexpressions of hBD-2, hBD-3, and hCAP18/LL-37 in Gingiva of diabetics with periodontitis. Immunobiology 220 (2015), 1219–1226.
95. [95] Everard, A., Geurts, L., Caesar, R., et al. Intestinal epithelial MyD88 is a sensor switching host metabolism towards obesity according to nutritional status. Nature Communications, 5, 2014, 5648.
96. [96] Pabst, O., Cerovic, V., Hornef, M., Secretory IgA in the coordination of establishment and maintenance of the microbiota. Trends in Immunology, 2016.
97. [97] Culbreath, C., Tanner, S.M., Yeramilli, V.A., et al. Environmental-mediated intestinal homeostasis in neonatal mice. The Journal of Surgical Research 198 (2015), 494–501.
98. [98] Rogier, E.W., Frantz, A.L., Bruno, M.E., et al. Secretory antibodies in breast milk promote long-term intestinal homeostasis by regulating the gut microbiota and host gene expression. Proceedings of the National Academy of Sciences of the United States of America 111 (2014), 3074–3079.
99. [99] Taira, T., Yamaguchi, S., Takahashi, A., et al. Dietary polyphenols increase fecal mucin and immunoglobulin A and ameliorate the disturbance in gut microbiota caused by a high fat diet. Journal of Clinical Biochemistry and Nutrition 57 (2015), 212–216.
100. [100] McPhee, J.B., Schertzer, J.D., Immunometabolism of obesity and diabetes: microbiota link compartmentalized immunity in the gut to metabolic tissue inflammation. Clinical Science (London) 129 (2015), 1083–1096.
101. [101] Niess, J.H., Brand, S., Gu, X., et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307 (2005), 254–258.
102. [102] Hapfelmeier, S., Muller, A.J., Stecher, B., et al. Microbe sampling by mucosal dendritic cells is a discrete, MyD88-independent step in DeltainvG S. Typhimurium colitis. Journal of Experimental Medicine 205 (2008), 437–450.
103. [103] McKenzie, A.N., Spits, H., Eberl, G., Innate lymphoid cells in inflammation and immunity. Immunity 41 (2014), 366–374.
104. [104] Eberl, G., Colonna, M., Di Santo, J.P., McKenzie, A.N., Innate lymphoid cells. Innate lymphoid cells: a new paradigm in immunology. Science, 348, 2015, aaa6566.
105. [105] Eberl, G., Development and evolution of RORgammat+ cells in a microbe's world. Immunological Reviews 245 (2012), 177–188.
106. [106] Hepworth, M.R., Monticelli, L.A., Fung, T.C., et al. Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature 498 (2013), 113–117.
107. [107] Luck, H., Tsai, S., Chung, J., et al. Regulation of obesity-related insulin resistance with gut anti-inflammatory agents. Cell Metabolism 21 (2015), 527–542.
108. [108] Qiu, J., Zhou, L., Aryl hydrocarbon receptor promotes RORgammat(+) group 3 ILCs and controls intestinal immunity and inflammation. Seminars in Immunopathology 35 (2013), 657–670.
109. [109] van den Hout, M.F., Sluijter, B.J., Santegoets, S.J., et al. Local delivery of CpG-B and GM-CSF induces concerted activation of effector and regulatory T cells in the human melanoma sentinel lymph node. Cancer Immunology Immunotherapy 65 (2016), 405–415.
110. [110] Pearson, C., Thornton, E.E., McKenzie, B., et al. ILC3 GM-CSF production and mobilisation orchestrate acute intestinal inflammation. Elife, 5, 2016, e10066.
111. [111] Mortha, A., Chudnovskiy, A., Hashimoto, D., et al. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science, 343, 2014, 1249288.
112. [112] Murphy, K.M., Transcriptional control of dendritic cell development. Advances in Immunology 120 (2013), 239–267.
113. [113] Kim, M.H., Taparowsky, E.J., Kim, C.H., Retinoic acid differentially regulates the migration of innate lymphoid cell subsets to the gut. Immunity 43 (2015), 107–119.
114. [114] Huang, S., Martin, E., Kim, S., et al. MR1 antigen presentation to mucosal-associated invariant T cells was highly conserved in evolution. Proceedings of the National Academy of Sciences of the United States of America 106 (2009), 8290–8295.
115. [115] Salerno-Goncalves, R., Rezwan, T., Sztein, M.B., B cells modulate mucosal associated invariant T cell immune responses. Frontiers in Immunology, 4, 2014, 511.
116. [116] Magalhaes, I., Pingris, K., Poitou, C., et al. Mucosal-associated invariant T cell alterations in obese and type 2 diabetic patients. Journal of Clinical Investigation 125 (2015), 1752–1762.
117. [117] Apostolopoulos, V., de Courten, M.P., Stojanovska, L., et al. The complex immunological and inflammatory network of adipose tissue in obesity. Molecular Nutrition & Food Research 60 (2016), 43–57.
118. [118] Monteiro-Sepulveda, M., Touch, S., Mendes-Sa, C., et al. Jejunal T cell inflammation in human obesity correlates with decreased enterocyte insulin signaling. Cell Metabolism 22 (2015), 113–124.
119. [119] Bagci, B., Bagci, G., Huzmeli, C., et al. Associations of fractalkine receptor (CX3CR1) and CCR5 gene variants with hypertension, diabetes and atherosclerosis in chronic renal failure patients undergoing hemodialysis. International Urology and Nephrology, 2016.
120. [120] Golbus, J.R., Stitziel, N.O., Zhao, W., et al. Common and rare genetic variation in CCR2, CCR5, or CX3CR1 and risk of atherosclerotic coronary heart disease and glucometabolic traits. Circulation Cardiovascular Genetics, 2016.
121. [121] Shah, R., O'Neill, S.M., Hinkle, C., et al. Metabolic effects of CX3CR1 deficiency in diet-induced obese mice. PLoS One, 10, 2015, e0138317.
122. [122] Pomié, C., Blasco-Baque, V., Klopp, P., et al. Triggering the adaptive immune system with commensal gut bacteria protects against insulin resistance and dysglycemia. Molecular Metabolism 5 (2016), 392–403.