Linking the Microbiota, Chronic Disease, and the Immune System

Trends in Endocrinology and Metabolism

Volumn 27, Issue 12, 2016, Pages 831-843

  Hand, Timothy W ^a   Vujkovic Cvijin, Ivan ^b   Ridaura, Vanessa K ^b   Belkaid, Yasmine ^b  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

dysbiosis; inflammasome; metabolic syndrome; microbiota

Indexed keywords

CARDIOVASCULAR DISEASE; CHRONIC DISEASE; CHRONIC INFLAMMATION; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE SYSTEM; METABOLIC SYNDROME X; METABOLITE; MICROFLORA; MORTALITY; NONHUMAN; OBESITY; PRIORITY JOURNAL; REVIEW; ANIMAL; DYSBIOSIS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

INFLAMMASOME;

ANIMALS; CHRONIC DISEASE; DYSBIOSIS; HUMANS; IMMUNE SYSTEM; INFLAMMASOMES; METABOLIC SYNDROME; MICROBIOTA;

EID: 84992702870     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2016.08.003     Document Type: Review

References (131)

1. 1 Chovatiya, R., Medzhitov, R., Stress, inflammation, and defense of homeostasis. Mol. Cell 54 (2014), 281–288.
2. 2 Wynn, T.A., Vannella, K.M., Macrophages in tissue repair, regeneration, and fibrosis. Immunity 44 (2016), 450–462.
3. 3 Frank, D.N., et al. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 13780–13785.
4. 4 Qin, J., et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490 (2012), 55–60.
5. 5 Turnbaugh, P.J., et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444 (2006), 1027–1031.
6. 6 Berni Canani, R., et al. The role of the commensal microbiota in the regulation of tolerance to dietary allergens. Curr. Opin. Allergy Clin. Immunol. 15 (2015), 243–249.
7. 7 Sandler, N.G., Douek, D.C., Microbial translocation in HIV infection: causes, consequences and treatment opportunities. Nat. Rev. Microbiol. 10 (2012), 655–666.
8. 8 Belkaid, Y., Hand, T.W., Role of the microbiota in immunity and inflammation. Cell 157 (2014), 121–141.
9. 9 Longman, R.S., et al. Microbiota: host interactions in mucosal homeostasis and systemic autoimmunity. Cold Spring Harb. Symp. Quant. Biol. 78 (2013), 193–201.
10. 10 Yurkovetskiy, L.A., et al. Microbiota and autoimmunity: exploring new avenues. Cell Host Microbe 17 (2015), 548–552.
11. 11 Blaser, M.J., Falkow, S., What are the consequences of the disappearing human microbiota?. Nat. Rev. Microbiol. 7 (2009), 887–894.
12. 12 Flint, H.J., et al. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat. Rev. Microbiol. 6 (2008), 121–131.
13. 13 Qin, J., et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464 (2010), 59–65.
14. 14 Zeevi, D., et al. Personalized nutrition by prediction of glycemic responses. Cell 163 (2015), 1079–1094.
15. 15 Belkaid, Y., et al. Effector and memory T cell responses to commensal bacteria. Trends Immunol. 34 (2013), 299–306.
16. 16 Hooper, L.V., et al. Interactions between the microbiota and the immune system. Science 336 (2012), 1268–1273.
17. 17 Henao-Mejia, J., et al. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature 482 (2012), 179–185.
18. 18 Amar, J., 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.
19. 19 Kaser, A., et al. Inflammatory bowel disease. Annu. Rev. Immunol. 28 (2010), 573–621.
20. –/– mice. Nature 487 (2012), 104–108.
21. + T cells regulate immunoglobulin a selection and facilitate diversification of bacterial species responsible for immune homeostasis. Immunity 41 (2014), 152–165.
22. 22 Pickard, J.M., et al. Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature 514 (2014), 638–641.
23. 23 Wahlström, A., et al. Intestinal crosstalk between bile acids and microbiota and its impact on host metabolism. Cell Metab. 24 (2016), 41–50.
24. 24 Mazmanian, S.K., et al. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122 (2005), 107–118.
25. 25 An, D., et al. Sphingolipids from a symbiotic microbe regulate homeostasis of host intestinal natural killer T cells. Cell 156 (2014), 123–133.
26. 26 Olszak, T., et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 336 (2012), 489–493.
27. 27 Arpaia, N., et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504 (2013), 451–455.
28. 28 Furusawa, Y., et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504 (2013), 446–450.
29. 29 Smith, P.M., et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341 (2013), 569–573.
30. 30 Macia, L., et al. Metabolite-sensing receptors GPR43 and GPR109A facilitate dietary fibre-induced gut homeostasis through regulation of the inflammasome. Nat. Commun., 6, 2015, 6734.
31. 31 Maslowski, K.M., et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461 (2009), 1282–1286.
32. 32 Hall, J.A., et al. The role of retinoic acid in tolerance and immunity. Immunity 35 (2011), 13–22.
33. 33 Levy, M., et al. Microbiota-modulated metabolites shape the intestinal microenvironment by regulating NLRP6 inflammasome signaling. Cell 163 (2015), 1428–1443.
34. 34 Mathis, D., Immunological goings-on in visceral adipose tissue. Cell Metab. 17 (2013), 851–859.
35. 35 Buffie, C.G., et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature 517 (2015), 205–208.
36. 36 Rolhion, N., Darfeuille-Michaud, A., Adherent-invasive Escherichia coli in inflammatory bowel disease. Inflamm. Bowel Dis. 13 (2007), 1277–1283.
37. 37 Sokol, H., et al. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm. Bowel Dis. 15 (2009), 1183–1189.
38. 38 Garrett, W.S., et al. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe 8 (2010), 292–300.
39. 39 Elinav, E., et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 145 (2011), 745–757.
40. 40 Moayyedi, P., et al. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology, 149, 2015 102–109 e6.
41. 41 Rossen, N.G., et al. Findings from a randomized controlled trial of fecal transplantation for patients with ulcerative colitis. Gastroenterology, 149, 2015 110–118.e4.
42. 42 Sokol, H., Probiotics and antibiotics in IBD. Dig. Dis. 32 (2014), 10–17.
43. 43 Winter, S.E., Bäumler, A.J., Dysbiosis in the inflamed intestine: chance favors the prepared microbe. Gut Microbes 5 (2014), 71–73.
44. 44 Winter, S.E., et al. Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science 339 (2013), 708–711.
45. 45 Craven, M., et al. Inflammation drives dysbiosis and bacterial invasion in murine models of ileal Crohn's disease. PLoS One, 7, 2012, e41594.
46. 46 Heimesaat, M.M., et al. Gram-negative bacteria aggravate murine small intestinal Th1-type immunopathology following oral infection with Toxoplasma gondii. J. Immunol. 177 (2006), 8785–8795.
47. 47 Molloy, M.J., et al. Intraluminal containment of commensal outgrowth in the gut during infection-induced dysbiosis. Cell Host Microbe 14 (2013), 318–328.
48. 48 Berg, A.M., et al. Clostridium difficile infection in the inflammatory bowel disease patient. Inflamm. Bowel Dis. 19 (2013), 194–204.
49. 49 Cullender, T.C., et al. Innate and adaptive immunity interact to quench microbiome flagellar motility in the gut. Cell Host Microbe 14 (2013), 571–581.
50. 50 Palm, N.W., et al. Immunoglobulin A coating identifies colitogenic bacteria in inflammatory bowel disease. Cell 158 (2014), 1000–1010.
51. 51 Huang, Y.J., LiPuma, J.J., The microbiome in cystic fibrosis. Clin. Chest Med. 37 (2016), 59–67.
52. 52 Boguniewicz, M., Leung, D.Y., Atopic dermatitis: a disease of altered skin barrier and immune dysregulation. Immunol. Rev. 242 (2011), 233–246.
53. 53 Gregor, M.F., Hotamisligil, G.S., Inflammatory mechanisms in obesity. Annu. Rev. Immunol. 29 (2011), 415–445.
54. 54 McNelis, J.C., Olefsky, J.M., Macrophages, immunity, and metabolic disease. Immunity 41 (2014), 36–48.
55. 55 Turnbaugh, P.J., et al. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3 (2008), 213–223.
56. 56 Ridaura, V.K., et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science, 341, 2013, 1241214.
57. 57 Everard, A., et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 9066–9071.
58. 58 Schneeberger, M., et al. Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice. Sci. Rep., 5, 2015, 16643.
59. 59 Vijay-Kumar, M., et al. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science 328 (2010), 228–231.
60. 60 Carvalho, F.A., et al. Transient inability to manage proteobacteria promotes chronic gut inflammation in TLR5-deficient mice. Cell Host Microbe 12 (2012), 139–152.
61. 61 Forslund, K., et al. Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature 528 (2015), 262–266.
62. 62 Cotillard, A., et al. Dietary intervention impact on gut microbial gene richness. Nature 500 (2013), 585–588.
63. 63 Le Chatelier, E., et al. Richness of human gut microbiome correlates with metabolic markers. Nature 500 (2013), 541–546.
64. 64 Burcelin, R., et al. Immuno-microbiota cross and talk: the new paradigm of metabolic diseases. Semin. Immunol. 24 (2012), 67–74.
65. 65 Martinez-Medina, M., 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.
66. 66 Cani, P.D., et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56 (2007), 1761–1772.
67. 67 Garidou, L., et al. The gut microbiota regulates intestinal CD4 T cells expressing RORγt and controls metabolic disease. Cell Metab. 22 (2015), 100–112.
68. 68 Balmer, M.L., et al. The liver may act as a firewall mediating mutualism between the host and its gut commensal microbiota. Sci. Transl. Med., 6, 2014, 237ra66.
69. 69 Elinav, E., et al. Analysis of microbiota alterations in inflammasome-deficient mice. Methods Mol. Biol. 1040 (2013), 185–194.
70. 70 Fiorotto, R., et al. Loss of CFTR affects biliary epithelium innate immunity and causes TLR4-NF-κB-mediated inflammatory response in mice. Gastroenterology 141 (2011), 1498–1508, 1508 e1–5.
71. 71 Brenner, D.A., et al. Role of gut microbiota in liver disease. J. Clin. Gastroenterol. 49 (2015), S25–S27.
72. 72 Wang, L., et al. Intestinal REG3 lectins protect against alcoholic steatohepatitis by reducing mucosa-associated microbiota and preventing bacterial translocation. Cell Host Microbe 19 (2016), 227–239.
73. 73 Wu, J., et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150 (2012), 366–376.
74. 74 Cohen, P., Spiegelman, B.M., Brown and beige fat: molecular parts of a thermogenic machine. Diabetes 64 (2015), 2346–2351.
75. 75 Brestoff, J.R., et al. Group 2 innate lymphoid cells promote beiging of white adipose tissue and limit obesity. Nature 519 (2015), 242–246.
76. 76 Lee, M.W., et al. Activated type 2 innate lymphoid cells regulate beige fat biogenesis. Cell 160 (2015), 74–87.
77. 77 Qiu, Y., et al. Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat. Cell 157 (2014), 1292–1308.
78. 78 Suárez-Zamorano, N., et al. Microbiota depletion promotes browning of white adipose tissue and reduces obesity. Nat. Med. 21 (2015), 1497–1501.
79. 79 Chevalier, C., et al. Gut microbiota orchestrates energy homeostasis during cold. Cell 163 (2015), 1360–1374.
80. 80 Zhu, W., et al. Gut microbial metabolite TMAO enhances platelet hyperreactivity and thrombosis risk. Cell 165 (2016), 111–124.
81. 81 Tang, W.H., et al. Prognostic value of elevated levels of intestinal microbe-generated metabolite trimethylamine-N-oxide in patients with heart failure: refining the gut hypothesis. J. Am. Coll. Cardiol. 64 (2014), 1908–1914.
82. 82 Wang, Z., et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472 (2011), 57–63.
83. 83 Koeth, R.A., et al. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat. Med. 19 (2013), 576–585.
84. 84 Stein, J.H., Hsue, P.Y., Inflammation, immune activation, and CVD risk in individuals with HIV infection. JAMA 308 (2012), 405–406.
85. 85 Dillon, S.M., et al. An altered intestinal mucosal microbiome in HIV-1 infection is associated with mucosal and systemic immune activation and endotoxemia. Mucosal. Immunol. 7 (2014), 983–994.
86. 86 Lozupone, C.A., et al. Alterations in the gut microbiota associated with HIV-1 infection. Cell Host Microbe 14 (2013), 329–339.
87. 87 Vujkovic-Cvijin, I., et al. Dysbiosis of the gut microbiota is associated with HIV disease progression and tryptophan catabolism. Sci. Transl. Med., 5, 2013, 193ra91.
88. 88 Brenchley, J.M., et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 12 (2006), 1365–1371.
89. 89 Dinh, D.M., et al. Intestinal microbiota, microbial translocation, and systemic inflammation in chronic HIV infection. J. Infect. Dis. 211 (2015), 19–27.
90. 90 Mutlu, E.A., et al. A compositional look at the human gastrointestinal microbiome and immune activation parameters in HIV infected subjects. PLoS Pathog., 10, 2014, e1003829.
91. 91 Vázquez-Castellanos, J.F., et al. Altered metabolism of gut microbiota contributes to chronic immune activation in HIV-infected individuals. Mucosal. Immunol. 8 (2015), 760–772.
92. 92 Costalonga, M., Herzberg, M.C., The oral microbiome and the immunobiology of periodontal disease and caries. Immunol. Lett. 162 (2014), 22–38.
93. 93 Gmür, R., et al. Double-blind analysis of the relation between adult periodontitis and systemic host response to suspected periodontal pathogens. Infect. Immun. 52 (1986), 768–776.
94. 94 Mustapha, I.Z., et al. Markers of systemic bacterial exposure in periodontal disease and cardiovascular disease risk: a systematic review and meta-analysis. J. Periodontol. 78 (2007), 2289–2302.
95. 95 Gibson, F.C. 3rd, et al. Innate immune recognition of invasive bacteria accelerates atherosclerosis in apolipoprotein E-deficient mice. Circulation 109 (2004), 2801–2806.
96. 96 Koren, O., et al. Human oral, gut, and plaque microbiota in patients with atherosclerosis. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 4592–4598.
97. 97 Lalla, E., et al. Oral infection with a periodontal pathogen accelerates early atherosclerosis in apolipoprotein E-null mice. Arterioscler. Thromb. Vasc. Biol. 23 (2003), 1405–1411.
98. 98 Silbergeld, E.K., et al. Industrial food animal production, antimicrobial resistance, and human health. Annu. Rev. Public Health 29 (2008), 151–169.
99. 99 Cho, I., et al. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 488 (2012), 621–626.
100. 100 Cox, L.M., et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell 158 (2014), 705–721.
101. 101 Stecher, B., et al. Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 1269–1274.
102. 102 Clarke, S.F., et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut 63 (2014), 1913–1920.
103. 103 Sonnenburg, E.D., Sonnenburg, J.L., Starving our microbial self: the deleterious consequences of a diet deficient in microbiota-accessible carbohydrates. Cell Metab. 20 (2014), 779–786.
104. 104 Kamada, N., et al. Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science 336 (2012), 1325–1329.
105. 105 McNeill, W.H., Plagues and peoples. 1976, Anchor Press.
106. 106 Trueba, G., Dunthorn, M., Many neglected tropical diseases may have originated in the Paleolithic or before: new insights from genetics. PLoS Negl. Trop. Dis., 6, 2012, e1393.
107. 107 Hotez, P.J., et al. The global burden of disease study 2010: interpretation and implications for the neglected tropical diseases. PLoS Negl. Trop. Dis., 8, 2014, e2865.
108. 108 Weinstock, J.V., Do we need worms to promote immune health?. Clin. Rev. Allergy Immunol. 49 (2015), 227–231.
109. 109 Allen, J.E., Maizels, R.M., Diversity and dialogue in immunity to helminths. Nat. Rev Immunol. 11 (2011), 375–388.
110. 110 Maizels, R.M., et al. Immune modulation and modulators in Heligmosomoides polygyrus infection. Exp. Parasitol. 132 (2012), 76–89.
111. 111 Grainger, J.R., et al. Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-β pathway. J. Exp. Med. 207 (2010), 2331–2341.
112. 112 Osborne, L.C., et al. Coinfection. Virus-helminth coinfection reveals a microbiota-independent mechanism of immunomodulation. Science 345 (2014), 578–582.
113. 113 Zaiss, M.M., et al. The intestinal microbiota contributes to the ability of helminths to modulate allergic inflammation. Immunity 43 (2015), 998–1010.
114. 114 Leung, J., et al. Heligmosomoides polygyrus abrogates antigen-specific gut injury in a murine model of inflammatory bowel disease. Inflamm. Bowel Dis. 18 (2012), 1447–1455.
115. 115 Broadhurst, M.J., et al. Therapeutic helminth infection of macaques with idiopathic chronic diarrhea alters the inflammatory signature and mucosal microbiota of the colon. PLoS Pathog., 8, 2012, e1003000.
116. 116 Helmby, H., Human helminth therapy to treat inflammatory disorders – where do we stand?. BMC Immunol., 16, 2015, 12.
117. 117 Vernacchio, L., et al. Diarrhea in American infants and young children in the community setting: incidence, clinical presentation and microbiology. Pediatr. Infect. Dis. J. 25 (2006), 2–7.
118. 118 Kosek, M., et al. The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull. World Health Organ. 81 (2003), 197–204.
119. 119 Cadwell, K., et al. Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine. Cell 141 (2010), 1135–1145.
120. 120 Lupp, C., et al. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2 (2007), 119–129.
121. 121 Meinzer, U., et al. Yersinia pseudotuberculosis effector YopJ subverts the Nod2/RICK/TAK1 pathway and activates caspase-1 to induce intestinal barrier dysfunction. Cell Host Microbe 11 (2012), 337–351.
122. 122 Hasegawa, M., et al. Interleukin-22 regulates the complement system to promote resistance against pathobionts after pathogen-induced intestinal damage. Immunity 41 (2014), 620–632.
123. 123 Hand, T.W., et al. Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses. Science 337 (2012), 1553–1556.
124. 124 Fonseca, D.M., et al. Microbiota-dependent sequelae of acute infection compromise tissue-specific immunity. Cell 163 (2015), 354–366.
125. 125 Kamdar, K., et al. Genetic and metabolic signals during acute enteric bacterial infection alter the microbiota and drive progression to chronic inflammatory disease. Cell Host Microbe 19 (2016), 21–31.
126. 126 Peyrin-Biroulet, L., et al. Mesenteric fat as a source of C reactive protein and as a target for bacterial translocation in Crohn's disease. Gut 61 (2012), 78–85.
127. 127 Zulian, A., et al. Differences in visceral fat and fat bacterial colonization between ulcerative colitis and Crohn's disease. An in vivo and in vitro study. PLoS One, 8, 2013, e78495.
128. 128 Korpe, P.S., Petri, W.A. Jr., Environmental enteropathy: critical implications of a poorly understood condition. Trends Mol. Med. 18 (2012), 328–336.
129. 129 Brown, E.M., et al. Diet and specific microbial exposure trigger features of environmental enteropathy in a novel murine model. Nat. Commun., 6, 2015, 7806.
130. 130 Kau, A.L., et al. Functional characterization of IgA-targeted bacterial taxa from undernourished Malawian children that produce diet-dependent enteropathy. Sci. Transl. Med., 7, 2015, 276ra224.
131. 131 Lindenbaum, J., et al. Subclinical malabsorption in developing countries. Am. J. Clin. Nutr. 25 (1972), 1056–1061.