1932

Abstract

Mammalian immune systems evolved within a diverse world dominated by microbes, making interactions between these two life-forms inevitable. Adaptive immunity protects against microbes through antigen-specific responses. In classical studies, these responses were investigated in the context of pathogenicity; however, we now know that they have significant effects on our resident microbes. In turn, microbes employ an arsenal of mechanisms to influence development and specificity of host immunity. Understanding these complex reactions will be necessary to develop microbiota-based strategies to prevent or treat disease. Here we review the literature detailing the cross talk between resident microbes with a focus on the specificity of host responses and the microbial molecules that influence them.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-090817-062307
2018-09-08
2024-12-10
Loading full text...

Full text loading...

/deliver/fulltext/micro/72/1/annurev-micro-090817-062307.html?itemId=/content/journals/10.1146/annurev-micro-090817-062307&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Abt MC, Artis D 2009. The intestinal microbiota in health and disease: the influence of microbial products on immune cell homeostasis. Curr. Opin. Gastroenterol. 25:496–502
    [Google Scholar]
  2. 2.  Abt MC, Osborne LC, Monticelli LA, Doering TA, Alenghat T et al. 2012. Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity 37:158–70
    [Google Scholar]
  3. 3.  An D, Oh SF, Olszak T, Neves JF, Avci FY et al. 2014. Sphingolipids from a symbiotic microbe regulate homeostasis of host intestinal natural killer T cells. Cell 156:123–33
    [Google Scholar]
  4. 4.  Aricioglu F, Regunathan S 2005. Agmatine attenuates stress- and lipopolysaccharide-induced fever in rats. Physiol. Behav. 85:370–75
    [Google Scholar]
  5. 5.  Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J et al. 2013. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504:451–55
    [Google Scholar]
  6. 6.  Atarashi K, Nishimura J, Shima T, Umesaki Y, Yamamoto M et al. 2008. ATP drives lamina propria TH17 cell differentiation. Nature 455:808–12
    [Google Scholar]
  7. 7.  Atarashi K, Tanoue T, Ando M, Kamada N, Nagano Y et al. 2015. Th17 cell induction by adhesion of microbes to intestinal epithelial cells. Cell 163:367–80
    [Google Scholar]
  8. 8.  Bank S, Skytt Andersen P, Burisch J, Pedersen N, Roug S et al. 2014. Polymorphisms in the inflammatory pathway genes TLR2, TLR4, TLR9, LY96, NFKBIA, NFKB1, TNFA, TNFRSF1A, IL6R, IL10, IL23R, PTPN22, and PPARG are associated with susceptibility of inflammatory bowel disease in a Danish cohort. PLOS ONE 9:e98815
    [Google Scholar]
  9. 9.  Beaucage KL, Xiao A, Pollmann SI, Grol MW, Beach RJ et al. 2014. Loss of P2X7 nucleotide receptor function leads to abnormal fat distribution in mice. Purinergic. Signal. 10:291–304
    [Google Scholar]
  10. 10.  Bogunovic M, Ginhoux F, Helft J, Shang L, Hashimoto D et al. 2009. Origin of the lamina propria dendritic cell network. Immunity 31:513–25
    [Google Scholar]
  11. 11.  Bogunovic M, Mortha A, Muller PA, Merad M 2012. Mononuclear phagocyte diversity in the intestine. Immunol. Res. 54:37–49
    [Google Scholar]
  12. 12.  Bolnick DI, Snowberg LK, Caporaso JG, Lauber C, Knight R, Stutz WE 2014. Major histocompatibility complex class IIb polymorphism influences gut microbiota composition and diversity. Mol. Ecol. 23:4831–45
    [Google Scholar]
  13. 13.  Bradley CP, Teng F, Felix KM, Sano T, Naskar D et al. 2017. Segmented filamentous bacteria provoke lung autoimmunity by inducing gut-lung axis Th17 cells expressing dual TCRs. Cell Host Microbe 22:697–704.e4
    [Google Scholar]
  14. 14.  Breyner NM, Michon C, de Sousa CS, Vilas Boas PB, Chain F et al. 2017. Microbial anti-inflammatory molecule (MAM) from Faecalibacteriumprausnitzii shows a protective effect on DNBS and DSS-induced colitis model in mice through inhibition of NF-κB pathway. Front. Microbiol. 8:114
    [Google Scholar]
  15. 15.  Bunker JJ, Erickson SA, Flynn TM, Henry C, Koval JC et al. 2017. Natural polyreactive IgA antibodies coat the intestinal microbiota. Science 358:eaan6619
    [Google Scholar]
  16. 16.  Bunker JJ, Flynn TM, Koval JC, Shaw DG, Meisel M et al. 2015. Innate and adaptive humoral responses coat distinct commensal bacteria with immunoglobulin A. Immunity 43:541–53
    [Google Scholar]
  17. 17.  Caricilli AM, Picardi PK, de Abreu LL, Ueno M, Prada PO et al. 2011. Gut microbiota is a key modulator of insulin resistance in TLR 2 knockout mice. PLOS Biol 9:e1001212
    [Google Scholar]
  18. 18.  Castagliuolo I, Riegler MF, Valenick L, LaMont JT, Pothoulakis C 1999. Saccharomycesboulardii protease inhibits the effects of Clostridiumdifficile toxins A and B in human colonic mucosa. Infect. Immun. 67:302–7
    [Google Scholar]
  19. 19.  Cebula A, Seweryn M, Rempala GA, Pabla SS, McIndoe RA et al. 2013. Thymus-derived regulatory T cells contribute to tolerance to commensal microbiota. Nature 497:258–62
    [Google Scholar]
  20. 20.  Chu H, Mazmanian SK 2013. Innate immune recognition of the microbiota promotes host-microbial symbiosis. Nat. Immunol. 14:668–75
    [Google Scholar]
  21. 21.  Clarke TB, Davis KM, Lysenko ES, Zhou AY, Yu Y, Weiser JN 2010. Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat. Med. 16:228–31
    [Google Scholar]
  22. 22.  Coombes JL, Siddiqui KR, Arancibia-Carcamo CV, Hall J, Sun CM et al. 2007. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J. Exp. Med. 204:1757–64
    [Google Scholar]
  23. 23.  Couturier-Maillard A, Secher T, Rehman A, Normand S, De Arcangelis A et al. 2013. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J. Clin. Investig. 123:700–11
    [Google Scholar]
  24. 24.  Craciun S, Balskus EP 2012. Microbial conversion of choline to trimethylamine requires a glycyl radical enzyme. PNAS 109:21307–12
    [Google Scholar]
  25. 25.  Cullender TC, Chassaing B, Janzon A, Kumar K, Muller CE et al. 2013. Innate and adaptive immunity interact to quench microbiome flagellar motility in the gut. Cell Host Microbe 14:571–81
    [Google Scholar]
  26. 26.  Cuskin F, Lowe EC, Temple MJ, Zhu Y, Cameron EA et al. 2015. Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism. Nature 517:165–69
    [Google Scholar]
  27. 27.  Dambrova M, Latkovskis G, Kuka J, Strele I, Konrade I et al. 2016. Diabetes is associated with higher trimethylamine N-oxide plasma levels. Exp. Clin. Endocrinol. Diabetes 124:251–56
    [Google Scholar]
  28. 28.  Danne C, Ryzhakov G, Martinez-Lopez M, Ilott NE, Franchini F et al. 2017. A large polysaccharide produced by Helicobacterhepaticus induces an anti-inflammatory gene signature in macrophages. Cell Host Microbe 22:733–45.e5
    [Google Scholar]
  29. 29.  de Mello VD, Paananen J, Lindstrom J, Lankinen MA, Shi L et al. 2017. Indolepropionic acid and novel lipid metabolites are associated with a lower risk of type 2 diabetes in the Finnish Diabetes Prevention Study. Sci. Rep. 7:46337
    [Google Scholar]
  30. 30.  Denning TL, Norris BA, Medina-Contreras O, Manicassamy S, Geem D et al. 2011. Functional specialization of intestinal dendritic cell and macrophage subsets that control Th17 and regulatory T cell responses are dependent on the T cell/APC ratio, source of mouse strain, and regional localization. J. Immunol. 187:2733–47
    [Google Scholar]
  31. 31.  Desai MS, Seekatz AM, Koropatkin NM, Kamada N, Hickey CA et al. 2016. A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell 167:1339–53.e21
    [Google Scholar]
  32. 32.  Diehl GE, Longman RS, Zhang JX, Breart B, Galan C et al. 2013. Microbiota restricts trafficking of bacteria to mesenteric lymph nodes by CX3CR1hi cells. Nature 494:116–20
    [Google Scholar]
  33. 33.  Dodd D, Spitzer MH, Van Treuren W, Merrill BD, Hryckowian AJ et al. 2017. A gut bacterial pathway metabolizes aromatic amino acids into nine circulating metabolites. Nature 551:648–52
    [Google Scholar]
  34. 34.  Donaldson GP, Lee SM, Mazmanian SK 2016. Gut biogeography of the bacterial microbiota. Nat. Rev. Microbiol. 14:20–32
    [Google Scholar]
  35. 35.  Fagarasan S, Kawamoto S, Kanagawa O, Suzuki K 2010. Adaptive immune regulation in the gut: T cell–dependent and T cell–independent IgA synthesis. Annu. Rev. Immunol. 28:243–73
    [Google Scholar]
  36. 36.  Fan P, Li L, Rezaei A, Eslamfam S, Che D, Ma X 2015. Metabolites of dietary protein and peptides by intestinal microbes and their impacts on gut. Curr. Protein Pept. Sci. 16:646–54
    [Google Scholar]
  37. 37.  Franchimont D, Vermeire S, El Housni H, Pierik M, Van Steen K et al. 2004. Deficient host-bacteria interactions in inflammatory bowel disease? The Toll-like receptor (TLR)-4 Asp299gly polymorphism is associated with Crohn's disease and ulcerative colitis. Gut 53:987–92
    [Google Scholar]
  38. 38.  Frei R, Ferstl R, Konieczna P, Ziegler M, Simon T et al. 2013. Histamine receptor 2 modifies dendritic cell responses to microbial ligands. J. Allergy Clin. Immunol. 132:194–204
    [Google Scholar]
  39. 39.  Geuking MB, Cahenzli J, Lawson MA, Ng DC, Slack E et al. 2011. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity 34:794–806
    [Google Scholar]
  40. 40.  Gionchetti P, Rizzello F, Morselli C, Poggioli G, Tambasco R et al. 2007. High-dose probiotics for the treatment of active pouchitis. Dis. Colon. Rectum. 50:2075–82; discussion 82–84
    [Google Scholar]
  41. 41.  Gomes-Neto JC, Kittana H, Mantz S, Segura Munoz RR, Schmaltz RJ et al. 2017. A gut pathobiont synergizes with the microbiota to instigate inflammatory disease marked by immunoreactivity against other symbionts but not itself. Sci. Rep. 7:17707
    [Google Scholar]
  42. 42.  Goto Y, Panea C, Nakato G, Cebula A, Lee C et al. 2014. Segmented filamentous bacteria antigens presented by intestinal dendritic cells drive mucosal Th17 cell differentiation. Immunity 40:594–607
    [Google Scholar]
  43. 43.  Guo C, Zhang L, Nie L, Zhang N, Xiao D et al. 2016. Association of polymorphisms in the MyD88, IRAK4 and TRAF6 genes and susceptibility to type 2 diabetes mellitus and diabetic nephropathy in a southern Han Chinese population. Mol. Cell Endocrinol. 429:114–19
    [Google Scholar]
  44. 44.  Hand TW, Dos Santos LM, Bouladoux N, Molloy MJ, Pagan AJ et al. 2012. Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses. Science 337:1553–56
    [Google Scholar]
  45. 45.  Hebbandi Nanjundappa R, Ronchi F, Wang J, Clemente-Casares X, Yamanouchi J et al. 2017. A gut microbial mimic that hijacks diabetogenic autoreactivity to suppress colitis. Cell 171:655–67.e17
    [Google Scholar]
  46. 46.  Hepworth MR, Fung TC, Masur SH, Kelsen JR, McConnell FM et al. 2015. Immune tolerance: Group 3 innate lymphoid cells mediate intestinal selection of commensal bacteria-specific CD4+ T cells. Science 348:1031–35
    [Google Scholar]
  47. 47.  Hepworth MR, Monticelli LA, Fung TC, Ziegler CG, Grunberg S et al. 2013. Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature 498:113–17
    [Google Scholar]
  48. 48.  Hoermannsperger G, Clavel T, Hoffmann M, Reiff C, Kelly D et al. 2009. Post-translational inhibition of IP-10 secretion in IEC by probiotic bacteria: impact on chronic inflammation. PLOS ONE 4:e4365
    [Google Scholar]
  49. 49.  Honda K, Littman DR 2016. The microbiota in adaptive immune homeostasis and disease. Nature 535:75–84
    [Google Scholar]
  50. 50.  Hormannsperger G, von Schillde MA, Haller D 2013. Lactocepin as a protective microbial structure in the context of IBD. Gut Microbes 4:152–57
    [Google Scholar]
  51. 51.  Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T et al. 2009. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139:485–98
    [Google Scholar]
  52. 52.  Ivanov II, Frutos R de Llanos, Manel N, Yoshinaga K, Rifkin DB et al. 2008. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4:337–49
    [Google Scholar]
  53. 53.  Jiang TT, Shao TY, Ang WXG, Kinder JM, Turner LH et al. 2017. Commensal fungi recapitulate the protective benefits of intestinal bacteria. Cell Host Microbe 22:809–16.e4
    [Google Scholar]
  54. 54.  Jiang W, Wang X, Zeng B, Liu L, Tardivel A et al. 2013. Recognition of gut microbiota by NOD2 is essential for the homeostasis of intestinal intraepithelial lymphocytes. J. Exp. Med. 210:2465–76
    [Google Scholar]
  55. 55.  Jin UH, Lee SO, Sridharan G, Lee K, Davidson LA et al. 2014. Microbiome-derived tryptophan metabolites and their aryl hydrocarbon receptor-dependent agonist and antagonist activities. Mol. Pharmacol. 85:777–88
    [Google Scholar]
  56. 56.  Joeris T, Muller-Luda K, Agace WW, Mowat AM 2017. Diversity and functions of intestinal mononuclear phagocytes. Mucosal Immunol 10:845–64
    [Google Scholar]
  57. 57.  Johansson-Lindbom B, Svensson M, Pabst O, Palmqvist C, Marquez G et al. 2005. Functional specialization of gut CD103+ dendritic cells in the regulation of tissue-selective T cell homing. J. Exp. Med. 202:1063–73
    [Google Scholar]
  58. 58.  Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW et al. 2000. Analysis of fractalkine receptor CX3CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol. 20:4106–14
    [Google Scholar]
  59. 59.  Kawamoto S, Maruya M, Kato LM, Suda W, Atarashi K et al. 2014. Foxp3+ T cells regulate immunoglobulin A selection and facilitate diversification of bacterial species responsible for immune homeostasis. Immunity 41:152–65
    [Google Scholar]
  60. 60.  Kim M, Qie Y, Park J, Kim CH 2016. Gut microbial metabolites fuel host antibody responses. Cell Host Microbe 20:202–14
    [Google Scholar]
  61. 61.  Kiss EA, Vonarbourg C, Kopfmann S, Hobeika E, Finke D et al. 2011. Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 334:1561–65
    [Google Scholar]
  62. 62.  Koeth RA, Wang Z, Levison BS, Buffa JA, Org E et al. 2013. Intestinal microbiota metabolism of l-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat. Med. 19:576–85
    [Google Scholar]
  63. 63.  Kubinak JL, Petersen C, Stephens WZ, Soto R, Bake E et al. 2015. MyD88 signaling in T cells directs IgA-mediated control of the microbiota to promote health. Cell Host Microbe 17:153–63
    [Google Scholar]
  64. 64.  Kubinak JL, Round JL 2012. Toll-like receptors promote mutually beneficial commensal-host interactions. PLOS Pathog 8:e1002785
    [Google Scholar]
  65. 65.  Kubinak JL, Round JL 2016. Do antibodies select a healthy microbiota?. Nat. Rev. Immunol. 16:767–74
    [Google Scholar]
  66. 66.  Kubinak JL, Stephens WZ, Soto R, Petersen C, Chiaro T et al. 2015. MHC variation sculpts individualized microbial communities that control susceptibility to enteric infection. Nat. Commun. 6:8642
    [Google Scholar]
  67. 67.  Kullberg MC, Ward JM, Gorelick PL, Caspar P, Hieny S et al. 1998. Helicobacterhepaticus triggers colitis in specific-pathogen-free interleukin-10 (IL-10)-deficient mice through an IL-12- and gamma interferon-dependent mechanism. Infect. Immun. 66:5157–66
    [Google Scholar]
  68. 68.  Lai Y, Di Nardo A, Nakatsuji T, Leichtle A, Yang Y et al. 2009. Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat. Med. 15:1377–82
    [Google Scholar]
  69. 69.  Lamas B, Richard ML, Leducq V, Pham HP, Michel ML et al. 2016. CARD9 impacts colitis by altering gut microbiota metabolism of tryptophan into aryl hydrocarbon receptor ligands. Nat. Med. 22:598–605
    [Google Scholar]
  70. 70.  Lathrop SK, Bloom SM, Rao SM, Nutsch K, Lio CW et al. 2011. Peripheral education of the immune system by colonic commensal microbiota. Nature 478:250–54
    [Google Scholar]
  71. 71.  Lee JS, Cella M, McDonald KG, Garlanda C, Kennedy GD et al. 2011. AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nat. Immunol. 13:144–51
    [Google Scholar]
  72. 72.  Lee YK, Menezes JS, Umesaki Y, Mazmanian SK 2011. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. PNAS 108:Suppl. 14615–22
    [Google Scholar]
  73. 73.  Levy M, Thaiss CA, Zeevi D, Dohnalova L, Zilberman-Schapira G et al. 2015. Microbiota-modulated metabolites shape the intestinal microenvironment by regulating NLRP6 inflammasome signaling. Cell 163:1428–43
    [Google Scholar]
  74. 74.  Li Y, Innocentin S, Withers DR, Roberts NA, Gallagher AR et al. 2011. Exogenous stimuli maintain intraepithelial lymphocytes via aryl hydrocarbon receptor activation. Cell 147:629–40
    [Google Scholar]
  75. 75.  Liang J, Huang HI, Benzatti FP, Karlsson AB, Zhang JJ et al. 2016. Inflammatory Th1 and Th17 in the intestine are each driven by functionally specialized dendritic cells with distinct requirements for MyD88. Cell Rep 17:1330–43
    [Google Scholar]
  76. 76.  Lodes MJ, Cong Y, Elson CO, Mohamath R, Landers CJ et al. 2004. Bacterial flagellin is a dominant antigen in Crohn disease. J. Clin. Investig. 113:1296–306
    [Google Scholar]
  77. 77.  Luda KM, Joeris T, Persson EK, Rivollier A, Demiri M et al. 2016. IRF8 transcription-factor-dependent classical dendritic cells are essential for intestinal T cell homeostasis. Immunity 44:860–74
    [Google Scholar]
  78. 78.  Macpherson AJ, Uhr T 2004. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303:1662–65
    [Google Scholar]
  79. 79.  Mangan PR, Harrington LE, O'Quinn DB, Helms WS, Bullard DC et al. 2006. Transforming growth factor-beta induces development of the TH17 lineage. Nature 441:231–34
    [Google Scholar]
  80. 80.  Mathis DJ, Benoist C, Williams VE, Kanter M, McDevitt HO 1983. Several mechanisms can account for defective E alpha gene expression in different mouse haplotypes. PNAS 80:273–77
    [Google Scholar]
  81. 81.  Matsuda JL, Gapin L, Fazilleau N, Warren K, Naidenko OV, Kronenberg M 2001. Natural killer T cells reactive to a single glycolipid exhibit a highly diverse T cell receptor beta repertoire and small clone size. PNAS 98:12636–41
    [Google Scholar]
  82. 82.  Mazmanian SK, Round JL, Kasper DL 2008. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453:620–25
    [Google Scholar]
  83. 83.  Mazzini E, Massimiliano L, Penna G, Rescigno M 2014. Oral tolerance can be established via gap junction transfer of fed antigens from CX3CR1+ macrophages to CD103+ dendritic cells. Immunity 40:248–61
    [Google Scholar]
  84. 84.  McDole JR, Wheeler LW, McDonald KG, Wang B, Konjufca V et al. 2012. Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine. Nature 483:345–49
    [Google Scholar]
  85. 85.  Misch EA, Hawn TR 2008. Toll-like receptor polymorphisms and susceptibility to human disease. Clin. Sci. 114:347–60
    [Google Scholar]
  86. 86.  Moor K, Diard M, Sellin ME, Felmy B, Wotzka SY et al. 2017. High-avidity IgA protects the intestine by enchaining growing bacteria. Nature 544:498–502
    [Google Scholar]
  87. 87.  Mowat AM 2010. Does TLR2 regulate intestinal inflammation?. Eur. J. Immunol. 40:318–20
    [Google Scholar]
  88. 88.  Nakatsuji T, Chen TH, Narala S, Chun KA, Two AM et al. 2017. Antimicrobials from human skin commensal bacteria protect against Staphylococcusaureus and are deficient in atopic dermatitis. Sci. Transl. Med. 9:eaah4680
    [Google Scholar]
  89. 89.  Niess JH, Brand S, Gu X, Landsman L, Jung S et al. 2005. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307:254–58
    [Google Scholar]
  90. 90.  Noble JA, Valdes AM 2011. Genetics of the HLA region in the prediction of type 1 diabetes. Curr. Diabetes Rep. 11:533–42
    [Google Scholar]
  91. 91.  Ochoa-Reparaz J, Mielcarz DW, Wang Y, Begum-Haque S, Dasgupta S et al. 2010. A polysaccharide from the human commensal Bacteroidesfragilis protects against CNS demyelinating disease. Mucosal Immunol 3:487–95
    [Google Scholar]
  92. 92.  Okada S, Markle JG, Deenick EK, Mele F, Averbuch D et al. 2015. Impairment of immunity to Candida and Mycobacterium in humans with bi-allelic RORC mutations. Science 349:606–13
    [Google Scholar]
  93. 93.  Olsen I, Jantzen E 2001. Sphingolipids in bacteria and fungi. Anaerobe 7:103–12
    [Google Scholar]
  94. 94.  Otto M 2017. Staphylococcusepidermidis: a major player in bacterial sepsis?. Future Microbiol 12:1031–33
    [Google Scholar]
  95. 95.  Pabst O 2012. New concepts in the generation and functions of IgA. Nat. Rev. Immunol. 12:821–32
    [Google Scholar]
  96. 96.  Palm NW, de Zoete MR, Cullen TW, Barry NA, Stefanowski J et al. 2014. Immunoglobulin A coating identifies colitogenic bacteria in inflammatory bowel disease. Cell 158:1000–10
    [Google Scholar]
  97. 97.  Panea C, Farkas AM, Goto Y, Abdollahi-Roodsaz S, Lee C et al. 2015. Intestinal monocyte-derived macrophages control commensal-specific Th17 responses. Cell Rep 12:1314–24
    [Google Scholar]
  98. 98.  Peng L, He Z, Chen W, Holzman IR, Lin J 2007. Effects of butyrate on intestinal barrier function in a Caco-2 cell monolayer model of intestinal barrier. Pediatr. Res. 61:37–41
    [Google Scholar]
  99. 99.  Perruzza L, Gargari G, Proietti M, Fosso B, D'Erchia AM et al. 2017. T follicular helper cells promote a beneficial gut ecosystem for host metabolic homeostasis by sensing microbiota-derived extracellular ATP. Cell Rep 18:2566–75
    [Google Scholar]
  100. 100.  Persson EK, Uronen-Hansson H, Semmrich M, Rivollier A, Hagerbrand K et al. 2013. IRF4 transcription-factor-dependent CD103+CD11b+ dendritic cells drive mucosal T helper 17 cell differentiation. Immunity 38:958–69
    [Google Scholar]
  101. 101.  Peterson DA, McNulty NP, Guruge JL, Gordon JI 2007. IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2:328–39
    [Google Scholar]
  102. 102.  Piccioni M, Monari C, Kenno S, Pericolini E, Gabrielli E et al. 2013. A purified capsular polysaccharide markedly inhibits inflammatory response during endotoxic shock. Infect. Immun. 81:90–98
    [Google Scholar]
  103. 103.  Planer JD, Peng Y, Kau AL, Blanton LV, Ndao IM et al. 2016. Development of the gut microbiota and mucosal IgA responses in twins and gnotobiotic mice. Nature 534:263–66
    [Google Scholar]
  104. 104.  Plato A, Hardison SE, Brown GD 2015. Pattern recognition receptors in antifungal immunity. Semin. Immunopathol. 37:97–106
    [Google Scholar]
  105. 105.  Postler TS, Ghosh S 2017. Understanding the holobiont: how microbial metabolites affect human health and shape the immune system. Cell Metab 26:110–30
    [Google Scholar]
  106. 106.  Puel A, Cypowyj S, Bustamante J, Wright JF, Liu L et al. 2011. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 332:65–68
    [Google Scholar]
  107. 107.  Quevrain E, Maubert MA, Michon C, Chain F, Marquant R et al. 2016. Identification of an anti-inflammatory protein from Faecalibacteriumprausnitzii, a commensal bacterium deficient in Crohn's disease. Gut 65:415–25
    [Google Scholar]
  108. 108.  Raghavendran K, Nemzek J, Napolitano LM, Knight PR 2011. Aspiration-induced lung injury. Crit. Care Med. 39:818–26
    [Google Scholar]
  109. 109.  Romano KA, Martinez-Del Campo A, Kasahara K, Chittim CL, Vivas EI et al. 2017. Metabolic, epigenetic, and transgenerational effects of gut bacterial choline consumption. Cell Host Microbe 22:279–90.e7
    [Google Scholar]
  110. 110.  Rosenbaum JT, Davey MP 2011. Time for a gut check: evidence for the hypothesis that HLA-B27 predisposes to ankylosing spondylitis by altering the microbiome. Arthritis Rheum 63:3195–98
    [Google Scholar]
  111. 111.  Rothhammer V, Mascanfroni ID, Bunse L, Takenaka MC, Kenison JE et al. 2016. Type I interferons and microbial metabolites of tryptophan modulate astrocyte activity and central nervous system inflammation via the aryl hydrocarbon receptor. Nat. Med. 22:586–97
    [Google Scholar]
  112. 112.  Round JL, Lee SM, Li J, Tran G, Jabri B et al. 2011. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 332:974–77
    [Google Scholar]
  113. 113.  Round JL, Mazmanian SK 2010. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. PNAS 107:12204–9
    [Google Scholar]
  114. 114.  Round JL, Palm NW 2018. Causal effects of the microbiota on immune-mediated diseases. Sci. Immunol. 3:20eaao1603
    [Google Scholar]
  115. 115.  Ruff WE, Kriegel MA 2015. Autoimmune host-microbiota interactions at barrier sites and beyond. Trends Mol. Med. 21:233–44
    [Google Scholar]
  116. 116.  Saha S, Jing X, Park SY, Wang S, Li X et al. 2010. Peptidoglycan recognition proteins protect mice from experimental colitis by promoting normal gut flora and preventing induction of interferon-gamma. Cell Host Microbe 8:147–62
    [Google Scholar]
  117. 117.  Sano T, Huang W, Hall JA, Yang Y, Chen A et al. 2015. An IL-23R/IL-22 circuit regulates epithelial serum amyloid A to promote local effector Th17 responses. Cell 163:381–93
    [Google Scholar]
  118. 118.  Schnupf P, Gaboriau-Routhiau V, Sansonetti PJ, Cerf-Bensussan N 2017. Segmented filamentous bacteria, Th17 inducers and helpers in a hostile world. Curr. Opin. Microbiol. 35:100–9
    [Google Scholar]
  119. 119.  Schulz O, Jaensson E, Persson EK, Liu X, Worbs T et al. 2009. Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J. Exp. Med. 206:3101–14
    [Google Scholar]
  120. 120.  Secher T, Normand S, Chamaillard M 2013. NOD2 prevents emergence of disease-predisposing microbiota. Gut Microbes 4:353–56
    [Google Scholar]
  121. 121.  Sharon G, Garg N, Debelius J, Knight R, Dorrestein PC, Mazmanian SK 2014. Specialized metabolites from the microbiome in health and disease. Cell Metab 20:719–30
    [Google Scholar]
  122. 122.  Silverman M, Kua L, Tanca A, Pala M, Palomba A et al. 2017. Protective major histocompatibility complex allele prevents type 1 diabetes by shaping the intestinal microbiota early in ontogeny. PNAS 114:9671–76
    [Google Scholar]
  123. 123.  Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA et al. 2013. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341:569–73
    [Google Scholar]
  124. 124.  Sokol H, Conway KL, Zhang M, Choi M, Morin B et al. 2013. Card9 mediates intestinal epithelial cell restitution, T-helper 17 responses, and control of bacterial infection in mice. Gastroenterology 145:591–601.e3
    [Google Scholar]
  125. 125.  Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG et al. 2008. Faecalibacteriumprausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. PNAS 105:16731–36
    [Google Scholar]
  126. 126.  Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I et al. 2009. Low counts of Faecalibacteriumprausnitzii in colitis microbiota. Inflamm. Bowel Dis. 15:1183–89
    [Google Scholar]
  127. 127.  Sonnenberg GF, Artis D 2015. Innate lymphoid cells in the initiation, regulation and resolution of inflammation. Nat. Med. 21:698–708
    [Google Scholar]
  128. 128.  Tang AT, Choi JP, Kotzin JJ, Yang Y, Hong CC et al. 2017. Endothelial TLR4 and the microbiome drive cerebral cavernous malformations. Nature 545:305–10
    [Google Scholar]
  129. 129.  Tang WH, Wang Z, Kennedy DJ, Wu Y, Buffa JA et al. 2015. Gut microbiota-dependent trimethylamine N-oxide (TMAO) pathway contributes to both development of renal insufficiency and mortality risk in chronic kidney disease. Circ. Res. 116:448–55
    [Google Scholar]
  130. 130.  Teng F, Klinger CN, Felix KM, Bradley CP, Wu E et al. 2016. Gut microbiota drive autoimmune arthritis by promoting differentiation and migration of Peyer's patch T follicular helper cells. Immunity 44:875–88
    [Google Scholar]
  131. 131.  Thaiss CA, Zmora N, Levy M, Elinav E 2016. The microbiome and innate immunity. Nature 535:65–74
    [Google Scholar]
  132. 132.  Toivanen P, Vaahtovuo J, Eerola E 2001. Influence of major histocompatibility complex on bacterial composition of fecal flora. Infect. Immun. 69:2372–77
    [Google Scholar]
  133. 133.  Underhill D, Braun J 2008. Current understanding of fungal microflora in inflammatory bowel disease pathogenesis. Inflamm. Bowel Dis. 14:1147–53
    [Google Scholar]
  134. 134.  Uranchimeg D, Kim JH, Kim JY, Lee WT, Park KA et al. 2010. Recovered changes in the spleen by agmatine treatment after transient cerebral ischemia. Anat. Cell Biol. 43:44–53
    [Google Scholar]
  135. 135.  Varol C, Vallon-Eberhard A, Elinav E, Aychek T, Shapira Y et al. 2009. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 31:502–12
    [Google Scholar]
  136. 136.  Vecchiarelli A, Pericolini E, Gabrielli E, Kenno S, Perito S et al. 2013. Elucidating the immunological function of the Cryptococcusneoformans capsule. Future Microbiol 8:1107–16
    [Google Scholar]
  137. 137.  Venkatesh M, Mukherjee S, Wang H, Li H, Sun K et al. 2014. Symbiotic bacterial metabolites regulate gastrointestinal barrier function via the xenobiotic sensor PXR and Toll-like receptor 4. Immunity 41:296–310
    [Google Scholar]
  138. 138.  Vijay-Kumar M, Aitken JD, Carvalho FA, Cullender TC, Mwangi S et al. 2010. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science 328:228–31
    [Google Scholar]
  139. 139.  von Schillde MA, Hormannsperger G, Weiher M, Alpert CA, Hahne H et al. 2012. Lactocepin secreted by Lactobacillus exerts anti-inflammatory effects by selectively degrading proinflammatory chemokines. Cell Host Microbe 11:387–96
    [Google Scholar]
  140. 140.  Wagener J, Malireddi RK, Lenardon MD, Koberle M, Vautier S et al. 2014. Fungal chitin dampens inflammation through IL-10 induction mediated by NOD2 and TLR9 activation. PLOS Pathog 10:e1004050
    [Google Scholar]
  141. 141.  Wang Z, Wang J, Cheng Y, Liu X, Huang Y 2011. Secreted factors from Bifidobacteriumanimalis subsp. lactis inhibit NF-κB-mediated interleukin-8 gene expression in Caco-2 cells. Appl. Environ. Microbiol. 77:8171–74
    [Google Scholar]
  142. 142.  Whiteside SK, Snook JP, Ma Y, Sonderegger FL, Fisher C et al. 2018. IL-10 deficiency reveals a role for TLR2-dependent bystander activation of T cells in Lyme arthritis. J. Immunol. 200:1457–70
    [Google Scholar]
  143. 143.  Wlodarska M, Luo C, Kolde R, d'Hennezel E, Annand JW et al. 2017. Indoleacrylic acid produced by commensal Peptostreptococcus species suppresses inflammation. Cell Host Microbe 22:25–37.e6
    [Google Scholar]
  144. 144.  Wolf AJ, Reyes CN, Liang W, Becker C, Shimada K et al. 2016. Hexokinase is an innate immune receptor for the detection of bacterial peptidoglycan. Cell 166:624–36
    [Google Scholar]
  145. 145.  Wu HJ, Ivanov II, Darce J, Hattori K, Shima T et al. 2010. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 32:815–27
    [Google Scholar]
  146. 146.  Yang Y, Torchinsky MB, Gobert M, Xiong H, Xu M et al. 2014. Focused specificity of intestinal TH17 cells towards commensal bacterial antigens. Nature 510:152–56
    [Google Scholar]
  147. 147.  Zelante T, Iannitti RG, Cunha C, De Luca A, Giovannini G et al. 2013. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 39:372–85
    [Google Scholar]
  148. 148.  Zhu S, Ashok M, Li J, Li W, Yang H et al. 2009. Spermine protects mice against lethal sepsis partly by attenuating surrogate inflammatory markers. Mol. Med. 15:275–82
    [Google Scholar]
/content/journals/10.1146/annurev-micro-090817-062307
Loading
/content/journals/10.1146/annurev-micro-090817-062307
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error