The Role of the Microbiota in Shaping Infectious Immunity

Trends in Immunology

Volumn 37, Issue 10, 2016, Pages 647-658

  Hand, Timothy W ^a  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; ANTIBIOTIC RESISTANCE; BACTERIAL COLONIZATION; BACTERIAL IMMUNITY; BACTERIAL INFECTION; COMMENSALISM; HOST; HUMAN; IMMUNOMODULATION; IMMUNOPATHOLOGY; INNATE IMMUNITY; INTESTINE FLORA; INTESTINE MUCOSA; NEXT GENERATION SEQUENCING; NONHUMAN; PATHOGENICITY; REVIEW; ANIMAL; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INFECTION; INFLAMMATION; METAGENOME; MICROBIOLOGY; MICROFLORA; OPPORTUNISTIC INFECTION;

ANIMALS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOMODULATION; INFECTION; INFLAMMATION; INTESTINAL MUCOSA; METAGENOME; MICROBIOTA; OPPORTUNISTIC INFECTIONS;

EID: 84994846019     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2016.08.007     Document Type: Review

References (125)

1. 1 Human Microbiome Project Consortium, Structure, function and diversity of the healthy human microbiome. Nature 486 (2012), 207–214.
2. 2 Sommer, F., Bäckhed, F., The gut microbiota–masters of host development and physiology. Nat. Rev. Microbiol. 11 (2013), 227–238.
3. 3 Belkaid, Y., Hand, T.W., Role of the microbiota in immunity and inflammation. Cell 157 (2014), 121–141.
4. 4 Qin, J., et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464 (2010), 59–65.
5. 5 Casanova, J.L., Abel, L., The genetic theory of infectious diseases: a brief history and selected illustrations. Annu. Rev. Genomics. Hum. Genet. 14 (2013), 215–243.
6. 6 Pirofski, L.A., Casadevall, A., What is infectiveness and how is it involved in infection and immunity?. BMC Immunol., 16, 2015, 13.
7. 7 Puel, A., et al. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 332 (2011), 65–68.
8. 8 Buffie, C.G., Pamer, E.G., Microbiota-mediated colonization resistance against intestinal pathogens. Nat. Rev. Immunol. 13 (2013), 790–801.
9. 9 Belkaid, Y., et al. Effector and memory T cell responses to commensal bacteria. Trends Immunol. 34 (2013), 299–306.
10. 10 Hooper, L.V., et al. Interactions between the microbiota and the immune system. Science 336 (2012), 1268–1273.
11. 11 Stecher, B., Hardt, W.D., Mechanisms controlling pathogen colonization of the gut. Curr. Opin. Microbiol. 14 (2011), 82–91.
12. 12 Martin, J.S., et al. Clostridium difficile infection: epidemiology, diagnosis and understanding transmission. Nat. Rev. Gastroenterol. Hepatol. 13 (2016), 206–216.
13. 13 Bakken, J.S., et al. Treating Clostridium difficile infection with fecal microbiota transplantation. Clin. Gastroenterol. Hepatol. 9 (2011), 1044–1049.
14. 14 Buffie, C.G., et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature 517 (2015), 205–208.
15. 15 Kamada, N., et al. Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science 336 (2012), 1325–1329.
16. 16 Ng, K.M., et al. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502 (2013), 96–99.
17. 17 Dobson, A., et al. Bacteriocin production: a probiotic trait?. Appl. Environ. Microbiol. 78 (2012), 1–6.
18. 18 Kommineni, S., et al. Bacteriocin production augments niche competition by enterococci in the mammalian gastrointestinal tract. Nature 526 (2015), 719–722.
19. 19 Brandl, K., et al. Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 455 (2008), 804–807.
20. 20 Pham, T.A., et al. Epithelial IL-22RA1-mediated fucosylation promotes intestinal colonization resistance to an opportunistic pathogen. Cell Host Microbe 16 (2014), 504–516.
21. 21 Pickard, J.M., et al. Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature 514 (2014), 638–641.
22. 22 Vaishnava, S., et al. The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science 334 (2011), 255–258.
23. 23 Abt, M.C., et al. TLR-7 activation enhances IL-22-mediated colonization resistance against vancomycin-resistant enterococcus. Sci. Transl. Med, 8, 2016, 327ra25.
24. 24 Kaser, A., et al. Inflammatory bowel disease. Annu. Rev. Immunol. 28 (2010), 573–621.
25. 25 Bogunovic, M., et al. Origin of the lamina propria dendritic cell network. Immunity 31 (2009), 513–525.
26. 26 Cheroutre, H., et al. The light and dark sides of intestinal intraepithelial lymphocytes. Nat. Rev. Immunol. 11 (2011), 445–456.
27. + innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota. Nat. Immunol. 12 (2011), 320–326.
28. 28 Bain, C.C., et al. Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat. Immunol. 15 (2014), 929–937.
29. + inflammatory monocytes are required for mucosal resistance to the pathogen Toxoplasma gondii. Immunity 29 (2008), 306–317.
30. 30 Khosravi, A., et al. Gut microbiota promote hematopoiesis to control bacterial infection. Cell Host Microbe 15 (2014), 374–381.
31. 31 Denning, T.L., et al. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat. Immunol. 8 (2007), 1086–1094.
32. 32 Fulde, M., Hornef, M.W., Maturation of the enteric mucosal innate immune system during the postnatal period. Immunol. Rev. 260 (2014), 21–34.
33. 33 Hackam, D.J., et al. Innate immune signaling in the pathogenesis of necrotizing enterocolitis. Clin. Dev. Immunol., 2013, 2013, 475415.
34. 34 Chassin, C., et al. MicroRNA-146a-mediated downregulation of IRAK1 protects mouse and human small intestine against ischemia/reperfusion injury. EMBO Mol. Med. 4 (2012), 1308–1319.
35. 35 Hackam, D.J., et al. Mechanisms of gut barrier failure in the pathogenesis of necrotizing enterocolitis: Toll-like receptors throw the switch. Semin. Pediatr. Surg. 22 (2013), 76–82.
36. 36 Jostins, L., et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491 (2012), 119–124.
37. 37 Macpherson, A.J., et al. The mucosal firewalls against commensal intestinal microbes. Semin. Immunopathol. 31 (2009), 145–149.
38. 38 Pabst, O., et al. Secretory IgA in the coordination of establishment and maintenance of the microbiota. Trends Immunol. 37 (2016), 287–296.
39. 39 Benveniste, J., et al. Serum and secretory IgA in axenic and holoxenic mice. J. Immunol. 107 (1971), 1656–1662.
40. 40 Macpherson, A.J., et al. The bilateral responsiveness between intestinal microbes and IgA. Trends Immunol. 36 (2015), 460–470.
41. 41 Slack, E., et al. Innate and adaptive immunity cooperate flexibly to maintain host-microbiota mutualism. Science 325 (2009), 617–620.
42. 42 Fransen, F., et al. BALB/c and C57BL/6 mice differ in polyreactive IgA abundance, which impacts the generation of antigen-specific IgA and microbiota diversity. Immunity 43 (2015), 527–540.
43. 43 Kadaoui, K.A., Corthesy, B., Secretory IgA mediates bacterial translocation to dendritic cells in mouse Peyer's patches with restriction to mucosal compartment. J. Immunol. 179 (2007), 7751–7757.
44. 44 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, 276ra24.
45. 45 Palm, N.W., et al. Immunoglobulin A coating identifies colitogenic bacteria in inflammatory bowel disease. Cell 158 (2014), 1000–1010.
46. 46 Koch, M.A., et al. Maternal IgG and IgA antibodies dampen mucosal T helper cell responses in early life. Cell 165 (2016), 827–841.
47. 47 Zeng, M.Y., et al. Gut microbiota-induced immunoglobulin G controls systemic infection by symbiotic bacteria and pathogens. Immunity 44 (2016), 647–658.
48. 48 Yilmaz, B., et al. Gut microbiota elicits a protective immune response against malaria transmission. Cell 159 (2014), 1277–1289.
49. 49 Peterson, D.A., et al. IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2 (2007), 328–339.
50. 50 Sanchez, C.J., et al. Biofilm and planktonic pneumococci demonstrate disparate immunoreactivity to human convalescent sera. BMC Microbiol., 11, 2011, 245.
51. 51 Hall, J.A., et al. Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses. Immunity 29 (2008), 637–649 2008.
52. 52 Gaboriau-Routhiau, V., et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 31 (2009), 677–689.
53. 53 Ivanov, I.I., et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139 (2009), 485–498.
54. + dendritic cells in response to bacterial flagellin enhances mucosal innate immune defense. Immunity 36 (2012), 276–287.
55. 55 Mortha, A., et al. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science, 343, 2014, 1249288.
56. 56 Sano, T., et al. An IL-23R/IL-22 circuit regulates epithelial serum amyloid A to promote local effector Th17 responses. Cell 163 (2015), 381–393.
57. 57 Shaw, M.H., et al. Microbiota-induced IL-1β, but not IL-6, is critical for the development of steady-state TH17 cells in the intestine. J. Exp. Med. 209 (2012), 251–258.
58. 58 Yang, Y., et al. Focused specificity of intestinal TH17 cells towards commensal bacterial antigens. Nature 510 (2014), 152–156.
59. 59 Cao, A.T., et al. Th17 cells upregulate polymeric Ig receptor and intestinal IgA and contribute to intestinal homeostasis. J. Immunol. 189 (2012), 4666–4673.
60. 60 Cong, Y., et al. A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 19256–19261.
61. 61 Kumar, P., et al. Intestinal interleukin-17 receptor signaling mediates reciprocal control of the gut microbiota and autoimmune inflammation. Immunity 44 (2016), 659–671.
62. 62 Lécuyer, E., et al. Segmented filamentous bacterium uses secondary and tertiary lymphoid tissues to induce gut IgA and specific T helper 17 cell responses. Immunity 40 (2014), 608–620.
63. + T cells in gut Peyer's patches. Science 323 (2009), 1488–1492.
64. 64 Naik, S., et al. Commensal-dendritic-cell interaction specifies a unique protective skin immune signature. Nature 520 (2015), 104–108.
65. 65 Naik, S., et al. Compartmentalized control of skin immunity by resident commensals. Science 337 (2012), 1115–1119.
66. 66 Wu, H.J., et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 32 (2010), 815–827.
67. 67 McAleer, J.P., et al. Pulmonary Th17 antifungal immunity is regulated by the gut mcrobiome. J. Immunol. 197 (2016), 97–107.
68. 68 Abt, M.C., et al. Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity 37 (2012), 158–170.
69. 69 Ichinohe, T., et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 5354–5359.
70. 70 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.
71. 71 Mazmanian, S.K., et al. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122 (2005), 107–118.
72. 72 An, D., et al. Sphingolipids from a symbiotic microbe regulate homeostasis of host intestinal natural killer T cells. Cell 156 (2014), 123–133.
73. 73 Okada, H., et al. The ‘hygiene hypothesis’ for autoimmune and allergic diseases: an update. Clin. Exp. Immunol. 160 (2010), 1–9.
74. 74 Jiang, W., et al. Recognition of gut microbiota by NOD2 is essential for the homeostasis of intestinal intraepithelial lymphocytes. J. Exp. Med. 210 (2013), 2465–2476.
75. 75 Shalapour, S., et al. Commensal microflora and interferon-gamma promote steady-state interleukin-7 production in vivo. Eur. J. Immunol. 40 (2010), 2391–2400.
76. 76 Verdu, E.F., et al. Novel players in coeliac disease pathogenesis: role of the gut microbiota. Nat. Rev. Gastroenterol. Hepatol. 12 (2015), 497–506.
77. 77 Grainger, J.R., et al. Inflammatory monocytes regulate pathologic responses to commensals during acute gastrointestinal infection. Nat. Med. 19 (2013), 713–721.
78. + Treg cell number and acquisition of effector cell phenotype during lethal infection. Immunity 31 (2009), 772–786.
79. 79 Josefowicz, S.Z., et al. Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 30 (2012), 531–564.
80. 80 Atarashi, K., et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331 (2011), 337–341.
81. 81 Atarashi, K., et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500 (2013), 232–236.
82. + T cells regulate immunoglobulin A selection and facilitate diversification of bacterial species responsible for immune homeostasis. Immunity 41 (2014), 152–165.
83. 83 Arpaia, N., et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504 (2013), 451–455.
84. 84 Furusawa, Y., et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504 (2013), 446–450.
85. 85 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.
86. 86 Maslowski, K.M., et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461 (2009), 1282–1286.
87. 87 Smith, P.M., et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341 (2013), 569–573.
88. 88 Zaiss, M.M., et al. The intestinal microbiota contributes to the ability of helminths to modulate allergic inflammation. Immunity 43 (2015), 998–1010.
89. 89 Ohnmacht, C., et al. Mucosal immunology. The microbiota regulates type 2 immunity through RORγt(+) T cells. Science 349 (2015), 989–993.
90. 90 Sefik, E., et al. Mucosal immunology. Individual intestinal symbionts induce a distinct population of RORγ(+) regulatory T cells. Science 349 (2015), 993–997.
91. 91 Round, J.L., et al. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 332 (2011), 974–977.
92. 92 Wu, W., et al. Commensal A4 bacteria inhibit intestinal Th2-cell responses through induction of dendritic cell TGF-β production. Eur. J. Immunol. 46 (2016), 1162–1167.
93. 93 Medina-Contreras, O., et al. Cutting edge: IL-36 receptor promotes resolution of intestinal damage. J. Immunol. 196 (2016), 34–38.
94. 94 Blanton, L.V., et al. Childhood undernutrition, the gut microbiota, and microbiota-directed therapeutics. Science, 352, 2016, 1533.
95. 95 Xavier, R.J., Microbiota as therapeutic targets. Dig. Dis. 34 (2016), 558–565.
96. 96 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.
97. 97 Pigneur, B., Sokol, H., Fecal microbiota transplantation in inflammatory bowel disease: the quest for the holy grail. Mucosal. Immunol., 2016, 10.1038/mi.2016.67 Published online July 27, 2016.
98. 98 Shin, S., Brodsky, I.E., The inflammasome: learning from bacterial evasion strategies. Semin. Immunol. 27 (2015), 102–110.
99. 99 Vance, R.E., et al. Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6 (2009), 10–21.
100. 100 Hand, T.W., et al. Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses. Science 337 (2012), 1553–1556.
101. 101 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.
102. 102 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.
103. 103 Lupp, C., et al. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2 (2007), 119–129.
104. 104 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.
105. 105 Levy, M., et al. Microbiota-modulated metabolites shape the intestinal microenvironment by regulating NLRP6 inflammasome signaling. Cell 163 (2015), 1428–1443.
106. 106 Egan, C.E., et al. Synergy between intraepithelial lymphocytes and lamina propria T cells drives intestinal inflammation during infection. Mucosal. Immunol. 4 (2011), 658–670.
107. 107 Severance, E.G., et al. Anti-gluten immune response following Toxoplasma gondii infection in mice. PLoS ONE, 7, 2012, e50991.
108. 108 Quereda, J.J., et al. Bacteriocin from epidemic Listeria strains alters the host intestinal microbiota to favor infection. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), 5706–5711.
109. 109 Fonseca, D.M., et al. Microbiota-dependent sequelae of acute infection compromise tissue-specific immunity. Cell 163 (2015), 354–366.
110. 110 Cadwell, K., et al. Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine. Cell 141 (2010), 1135–1145.
111. 111 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.
112. 112 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.
113. 113 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.
114. 114 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.
115. 115 Mann, E.A., Saeed, S.A., Gastrointestinal infection as a trigger for inflammatory bowel disease. Curr. Opin. Gastroenterol. 28 (2012), 24–29.
116. 116 Riddle, M.S., et al. The chronic gastrointestinal consequences associated with campylobacter. Curr. Gastroenterol. Rep. 14 (2012), 395–405.
117. 117 Jess, T., et al. Enteric Salmonella or Campylobacter infections and the risk of inflammatory bowel disease. Gut 60 (2011), 318–324.
118. 118 Riddle, M.S., Porter, C.K., Detection bias and the association between inflammatory bowel disease and Salmonella and Campylobacter infection. Gut, 61, 2012, 635.
119. 119 Jones, M.K., et al. Enteric bacteria promote human and mouse norovirus infection of B cells. Science 346 (2014), 755–759.
120. 120 Kane, M., et al. Successful transmission of a retrovirus depends on the commensal microbiota. Science 334 (2011), 245–249.
121. 121 Kuss, S.K., et al. Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science 334 (2011), 249–252.
122. 122 Robinson, C.M., et al. Bacterial lipopolysaccharide binding enhances virion stability and promotes environmental fitness of an enteric virus. Cell Host Microbe 15 (2014), 36–46.
123. 123 Wilks, J., et al. Mammalian lipopolysaccharide receptors incorporated into the retroviral envelope augment virus transmission. Cell Host Microbe 18 (2015), 456–462.
124. 124 Baldridge, M.T., et al. Commensal microbes and interferon-λ determine persistence of enteric murine norovirus infection. Science 347 (2015), 266–269.
125. 125 Hayes, K.S., et al. Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris. Science 328 (2010), 1391–1394.