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PMID: 25172617 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Modulation of immune development and function by intestinal microbiota.

Trends in immunology ·Vol. 35 ·No. 11 ·2014-11-00 ·Pages 507-17

Kabat AM, Srinivasan N, Maloy KJ

Abstract

The immune system must constantly monitor the gastrointestinal tract for the presence of pathogens while tolerating trillions of commensal microbiota. It is clear that intestinal microbiota actively modulate the immune system to maintain a mutually beneficial relation, but the mechanisms that maintain homeostasis are not fully understood. Recent advances have begun to shed light on the cellular and molecular factors involved, revealing that a range of microbiota derivatives can influence host immune functions by targeting various cell types, including intestinal epithelial cells, mononuclear phagocytes, innate lymphoid cells, and B and T lymphocytes. Here, we review these findings, highlighting open questions and important challenges to overcome in translating this knowledge into new therapies for intestinal and systemic immune disorders.

Keywords
commensals immune regulation microbiota mucosal immunity
MeSH Terms
Animals Cell Differentiation Homeostasis Humans Immunity, Innate Immunity, Mucosal Immunoglobulin A, Secretory/biosynthesis,immunology Immunomodulation Intestinal Mucosa/immunology,metabolism,microbiology Intestines/immunology,microbiology Lymphocytes/cytology,immunology,metabolism Microbiota Phagocytes/immunology,metabolism,microbiology Signal Transduction
Chemicals
Immunoglobulin A, Secretory
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Kabat Agnieszka M
Sir William Dunn School of Pathology, University of Oxford, Oxford, UK.
Srinivasan Naren
Sir William Dunn School of Pathology, University of Oxford, Oxford, UK; Immunobiology Laboratory, Cancer Research UK, London Research Institute, London, UK.
Maloy Kevin J
Sir William Dunn School of Pathology, University of Oxford, Oxford, UK. Electronic address: kevin.maloy@path.ox.ac.uk.
References (142)
142 references, click to expand
  1. Microbiota and autoimmune disease: the hosted self.
    Cell Host Microbe. 2011 Oct 20;10(4):297-301 PMID: 22018229
  2. Innate immune signaling in defense against intestinal microbes.
    Immunol Rev. 2012 Jan;245(1):113-31 PMID: 22168416
  3. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity.
    Nature. 2012 Feb 01;482(7384):179-85 PMID: 22297845
  4. Interleukin-17-producing gammadelta T cells selectively expand in response to pathogen products and environmental signals.
    Immunity. 2009 Aug 21;31(2):321-30 PMID: 19682928
  5. Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits.
    Nature. 2008 Oct 9;455(7214):804-7 PMID: 18724361
  6. Intestinal tolerance requires gut homing and expansion of FoxP3+ regulatory T cells in the lamina propria.
    Immunity. 2011 Feb 25;34(2):237-46 PMID: 21333554
  7. Epithelial barrier: an interface for the cross-communication between gut flora and immune system.
    Immunol Rev. 2012 Jan;245(1):147-63 PMID: 22168418
  8. Regulatory T cells: mechanisms of differentiation and function.
    Annu Rev Immunol. 2012;30:531-64 PMID: 22224781
  9. Immune adaptations that maintain homeostasis with the intestinal microbiota.
    Nat Rev Immunol. 2010 Mar;10(3):159-69 PMID: 20182457
  10. Regulated expression of nuclear receptor RORγt confers distinct functional fates to NK cell receptor-expressing RORγt(+) innate lymphocytes.
    Immunity. 2010 Nov 24;33(5):736-51 PMID: 21093318
  11. Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology.
    Nature. 2010 Apr 29;464(7293):1371-5 PMID: 20393462
  12. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses.
    Immunity. 2009 Oct 16;31(4):677-89 PMID: 19833089
  13. Intestinal dendritic cells specialize to activate transforming growth factor-β and induce Foxp3+ regulatory T cells via integrin αvβ8.
    Gastroenterology. 2011 Nov;141(5):1802-12 PMID: 21723222
  14. Like will to like: abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria.
    PLoS Pathog. 2010 Jan;6(1):e1000711 PMID: 20062525
  15. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens.
    Nat Med. 2008 Mar;14(3):282-9 PMID: 18264109
  16. Intestinal bacterial colonization induces mutualistic regulatory T cell responses.
    Immunity. 2011 May 27;34(5):794-806 PMID: 21596591
  17. Transgenic overexpression of Reg protein caused gastric cell proliferation and differentiation along parietal cell and chief cell lineages.
    Oncogene. 2004 Apr 29;23(20):3572-9 PMID: 15116092
  18. Preferential generation of follicular B helper T cells from Foxp3+ T cells in gut Peyer's patches.
    Science. 2009 Mar 13;323(5920):1488-92 PMID: 19286559
  19. Helminth infections and host immune regulation.
    Clin Microbiol Rev. 2012 Oct;25(4):585-608 PMID: 23034321
  20. The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells.
    Immunity. 2012 Jan 27;36(1):92-104 PMID: 22177117
  21. Exogenous stimuli maintain intraepithelial lymphocytes via aryl hydrocarbon receptor activation.
    Cell. 2011 Oct 28;147(3):629-40 PMID: 21999944
  22. How glycan metabolism shapes the human gut microbiota.
    Nat Rev Microbiol. 2012 Apr 11;10(5):323-35 PMID: 22491358
  23. Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis.
    Gut. 2014 Feb;63(2):281-91 PMID: 23426893
  24. Innate lymphoid cells--a proposal for uniform nomenclature.
    Nat Rev Immunol. 2013 Feb;13(2):145-9 PMID: 23348417
  25. STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing.
    J Exp Med. 2009 Jul 6;206(7):1465-72 PMID: 19564350
  26. Vancomycin-resistant Enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans.
    J Clin Invest. 2010 Dec;120(12):4332-41 PMID: 21099116
  27. Peripheral education of the immune system by colonic commensal microbiota.
    Nature. 2011 Sep 21;478(7368):250-4 PMID: 21937990
  28. Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses.
    Science. 2010 Jun 25;328(5986):1705-9 PMID: 20576892
  29. Familial transmission rather than defective innate immunity shapes the distinct intestinal microbiota of TLR-deficient mice.
    J Exp Med. 2012 Jul 30;209(8):1445-56 PMID: 22826298
  30. Loss of intestinal core 1-derived O-glycans causes spontaneous colitis in mice.
    J Clin Invest. 2011 Apr;121(4):1657-66 PMID: 21383503
  31. The effects of commensal microbiota on immune cell subsets and inflammatory responses.
    Immunol Rev. 2012 Jan;245(1):45-55 PMID: 22168413
  32. The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine.
    Science. 2011 Oct 14;334(6053):255-8 PMID: 21998396
  33. A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota.
    Proc Natl Acad Sci U S A. 2009 Nov 17;106(46):19256-61 PMID: 19889972
  34. Colorectal cancer in mice genetically deficient in the mucin Muc2.
    Science. 2002 Mar 1;295(5560):1726-9 PMID: 11872843
  35. Innate response activator B cells protect against microbial sepsis.
    Science. 2012 Feb 3;335(6068):597-601 PMID: 22245738
  36. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis.
    Proc Natl Acad Sci U S A. 2011 Mar 15;108 Suppl 1:4615-22 PMID: 20660719
  37. Successful transmission of a retrovirus depends on the commensal microbiota.
    Science. 2011 Oct 14;334(6053):245-9 PMID: 21998394
  38. Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria.
    Nature. 2013 Jun 6;498(7452):113-7 PMID: 23698371
  39. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis.
    Nature. 2008 Nov 27;456(7221):507-10 PMID: 18987631
  40. Outer membrane vesicles of a human commensal mediate immune regulation and disease protection.
    Cell Host Microbe. 2012 Oct 18;12(4):509-20 PMID: 22999859
  41. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis.
    Science. 2013 Aug 2;341(6145):569-73 PMID: 23828891
  42. Oral tolerance to food protein.
    Mucosal Immunol. 2012 May;5(3):232-9 PMID: 22318493
  43. Intestinal microbiota promote enteric virus replication and systemic pathogenesis.
    Science. 2011 Oct 14;334(6053):249-52 PMID: 21998395
  44. Microbiota regulates immune defense against respiratory tract influenza A virus infection.
    Proc Natl Acad Sci U S A. 2011 Mar 29;108(13):5354-9 PMID: 21402903
  45. Th17 cells upregulate polymeric Ig receptor and intestinal IgA and contribute to intestinal homeostasis.
    J Immunol. 2012 Nov 1;189(9):4666-73 PMID: 22993206
  46. A human gut microbial gene catalogue established by metagenomic sequencing.
    Nature. 2010 Mar 4;464(7285):59-65 PMID: 20203603
  47. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota.
    Semin Immunol. 2007 Apr;19(2):59-69 PMID: 17118672
  48. Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis.
    Science. 2012 Jun 8;336(6086):1314-7 PMID: 22674328
  49. Securing the immune tightrope: mononuclear phagocytes in the intestinal lamina propria.
    Nat Rev Immunol. 2010 Jun;10(6):415-26 PMID: 20498668
  50. Resurrection of endogenous retroviruses in antibody-deficient mice.
    Nature. 2012 Nov 29;491(7426):774-8 PMID: 23103862
  51. Plasmacytoid dendritic cells mediate anti-inflammatory responses to a gut commensal molecule via both innate and adaptive mechanisms.
    Cell Host Microbe. 2014 Apr 9;15(4):413-23 PMID: 24721570
  52. Regulation of cytokine secretion in human CD127(+) LTi-like innate lymphoid cells by Toll-like receptor 2.
    Immunity. 2010 Nov 24;33(5):752-64 PMID: 21055975
  53. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid.
    J Exp Med. 2007 Aug 6;204(8):1775-85 PMID: 17620362
  54. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance.
    Science. 2005 Jan 14;307(5707):254-8 PMID: 15653504
  55. Control of intestinal homeostasis, colitis, and colitis-associated colorectal cancer by the inflammatory caspases.
    Immunity. 2010 Mar 26;32(3):367-78 PMID: 20226691
  56. Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria.
    Science. 2012 Jun 8;336(6086):1321-5 PMID: 22674331
  57. Oral tolerance can be established via gap junction transfer of fed antigens from CX3CR1⁺ macrophages to CD103⁺ dendritic cells.
    Immunity. 2014 Feb 20;40(2):248-61 PMID: 24462723
  58. CD4(+) lymphoid tissue-inducer cells promote innate immunity in the gut.
    Immunity. 2011 Jan 28;34(1):122-34 PMID: 21194981
  59. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation.
    Nature. 2013 Dec 19;504(7480):451-5 PMID: 24226773
  60. Epithelial antimicrobial defence of the skin and intestine.
    Nat Rev Immunol. 2012 Jun 25;12(7):503-16 PMID: 22728527
  61. Microbiota, disease, and back to health: a metastable journey.
    Sci Transl Med. 2012 Jun 6;4(137):137rv7 PMID: 22674557
  62. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota.
    Nature. 2013 Aug 8;500(7461):232-6 PMID: 23842501
  63. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis.
    Science. 2014 Mar 28;343(6178):1249288 PMID: 24625929
  64. TSLP regulates intestinal immunity and inflammation in mouse models of helminth infection and colitis.
    J Exp Med. 2009 Mar 16;206(3):655-67 PMID: 19273626
  65. Dendritic cells in intestinal immune regulation.
    Nat Rev Immunol. 2008 Jun;8(6):435-46 PMID: 18500229
  66. Glycan foraging in vivo by an intestine-adapted bacterial symbiont.
    Science. 2005 Mar 25;307(5717):1955-9 PMID: 15790854
  67. Toll-like receptor 2 signaling in CD4(+) T lymphocytes promotes T helper 17 responses and regulates the pathogenesis of autoimmune disease.
    Immunity. 2010 May 28;32(5):692-702 PMID: 20434372
  68. The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions.
    Proc Natl Acad Sci U S A. 2011 Mar 15;108 Suppl 1:4659-65 PMID: 20615996
  69. Sphingolipids from a symbiotic microbe regulate homeostasis of host intestinal natural killer T cells.
    Cell. 2014 Jan 16;156(1-2):123-33 PMID: 24439373
  70. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity.
    Science. 2013 Mar 1;339(6123):1084-8 PMID: 23328391
  71. The genome of th17 cell-inducing segmented filamentous bacteria reveals extensive auxotrophy and adaptations to the intestinal environment.
    Cell Host Microbe. 2011 Sep 15;10(3):260-72 PMID: 21925113
  72. Acquisition of a multifunctional IgA+ plasma cell phenotype in the gut.
    Nature. 2011 Dec 11;481(7380):199-203 PMID: 22158124
  73. Microbial colonization influences early B-lineage development in the gut lamina propria.
    Nature. 2013 Sep 5;501(7465):112-5 PMID: 23965619
  74. Innate and adaptive immunity cooperate flexibly to maintain host-microbiota mutualism.
    Science. 2009 Jul 31;325(5940):617-20 PMID: 19644121
  75. Focused specificity of intestinal TH17 cells towards commensal bacterial antigens.
    Nature. 2014 Jun 5;510(7503):152-6 PMID: 24739972
  76. Intestinal macrophages and dendritic cells: what's the difference?
    Trends Immunol. 2014 Jun;35(6):270-7 PMID: 24794393
  77. Enhanced production of IL-18 in butyrate-treated intestinal epithelium by stimulation of the proximal promoter region.
    Eur J Immunol. 2002 Sep;32(9):2635-43 PMID: 12207348
  78. AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch.
    Nat Immunol. 2011 Nov 20;13(2):144-51 PMID: 22101730
  79. The sensing of environmental stimuli by follicular dendritic cells promotes immunoglobulin A generation in the gut.
    Immunity. 2010 Jul 23;33(1):71-83 PMID: 20643338
  80. The lifestyle of the segmented filamentous bacterium: a non-culturable gut-associated immunostimulating microbe inferred by whole-genome sequencing.
    DNA Res. 2011 Aug;18(4):291-303 PMID: 21791478
  81. Commensal bacteria calibrate the activation threshold of innate antiviral immunity.
    Immunity. 2012 Jul 27;37(1):158-70 PMID: 22705104
  82. Mucus enhances gut homeostasis and oral tolerance by delivering immunoregulatory signals.
    Science. 2013 Oct 25;342(6157):447-53 PMID: 24072822
  83. Alteration of the murine gut microbiota during infection with the parasitic helminth Heligmosomoides polygyrus.
    Inflamm Bowel Dis. 2010 Nov;16(11):1841-9 PMID: 20848461
  84. Segmented filamentous bacteria antigens presented by intestinal dendritic cells drive mucosal Th17 cell differentiation.
    Immunity. 2014 Apr 17;40(4):594-607 PMID: 24684957
  85. Gammadelta intraepithelial lymphocytes are essential mediators of host-microbial homeostasis at the intestinal mucosal surface.
    Proc Natl Acad Sci U S A. 2011 May 24;108(21):8743-8 PMID: 21555560
  86. Bacterial lipopolysaccharide binding enhances virion stability and promotes environmental fitness of an enteric virus.
    Cell Host Microbe. 2014 Jan 15;15(1):36-46 PMID: 24439896
  87. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota.
    Proc Natl Acad Sci U S A. 2010 Jul 6;107(27):12204-9 PMID: 20566854
  88. Gut immune maturation depends on colonization with a host-specific microbiota.
    Cell. 2012 Jun 22;149(7):1578-93 PMID: 22726443
  89. Segmented filamentous bacterium uses secondary and tertiary lymphoid tissues to induce gut IgA and specific T helper 17 cell responses.
    Immunity. 2014 Apr 17;40(4):608-20 PMID: 24745335
  90. Intestinal bacteria and the regulation of immune cell homeostasis.
    Annu Rev Immunol. 2010;28:623-67 PMID: 20192812
  91. Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine.
    Nature. 2012 Mar 14;483(7389):345-9 PMID: 22422267
  92. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota.
    Science. 2011 May 20;332(6032):974-7 PMID: 21512004
  93. Induction of colonic regulatory T cells by indigenous Clostridium species.
    Science. 2011 Jan 21;331(6015):337-41 PMID: 21205640
  94. Microbiota-induced IL-1β, but not IL-6, is critical for the development of steady-state TH17 cells in the intestine.
    J Exp Med. 2012 Feb 13;209(2):251-8 PMID: 22291094
  95. Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor.
    EMBO J. 2006 Nov 1;25(21):5071-82 PMID: 17036048
  96. Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles.
    Science. 2011 Dec 16;334(6062):1561-5 PMID: 22033518
  97. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination.
    Nature. 2011 Oct 26;479(7374):538-41 PMID: 22031325
  98. The microbiome in inflammatory bowel disease: current status and the future ahead.
    Gastroenterology. 2014 May;146(6):1489-99 PMID: 24560869
  99. Microbial exposure during early life has persistent effects on natural killer T cell function.
    Science. 2012 Apr 27;336(6080):489-93 PMID: 22442383
  100. All-trans retinoic acid mediates enhanced T reg cell growth, differentiation, and gut homing in the face of high levels of co-stimulation.
    J Exp Med. 2007 Aug 6;204(8):1765-74 PMID: 17620363
  101. ATP drives lamina propria T(H)17 cell differentiation.
    Nature. 2008 Oct 9;455(7214):808-12 PMID: 18716618
  102. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection.
    Gastroenterology. 2006 Jul;131(1):117-29 PMID: 16831596
  103. The inhibitory receptor PD-1 regulates IgA selection and bacterial composition in the gut.
    Science. 2012 Apr 27;336(6080):485-9 PMID: 22539724
  104. A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes.
    Gastroenterology. 2010 Dec;139(6):1844-1854.e1 PMID: 20816835
  105. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis.
    Cell. 2004 Jul 23;118(2):229-41 PMID: 15260992
  106. Thymus-derived regulatory T cells contribute to tolerance to commensal microbiota.
    Nature. 2013 May 9;497(7448):258-62 PMID: 23624374
  107. Innate lymphoid cells sustain colon cancer through production of interleukin-22 in a mouse model.
    J Exp Med. 2013 May 6;210(5):917-31 PMID: 23589566
  108. Complete genome sequences of rat and mouse segmented filamentous bacteria, a potent inducer of th17 cell differentiation.
    Cell Host Microbe. 2011 Sep 15;10(3):273-84 PMID: 21925114
  109. B cell-intrinsic MyD88 signaling prevents the lethal dissemination of commensal bacteria during colonic damage.
    Immunity. 2012 Feb 24;36(2):228-38 PMID: 22306056
  110. Microbial colonization drives expansion of IL-1 receptor 1-expressing and IL-17-producing gamma/delta T cells.
    Cell Host Microbe. 2010 Feb 18;7(2):140-50 PMID: 20159619
  111. Bifidobacteria can protect from enteropathogenic infection through production of acetate.
    Nature. 2011 Jan 27;469(7331):543-7 PMID: 21270894
  112. Interleukin 23 production by intestinal CD103(+)CD11b(+) dendritic cells in response to bacterial flagellin enhances mucosal innate immune defense.
    Immunity. 2012 Feb 24;36(2):276-87 PMID: 22306017
  113. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22.
    Immunity. 2013 Aug 22;39(2):372-85 PMID: 23973224
  114. Innate lymphoid cell interactions with microbiota: implications for intestinal health and disease.
    Immunity. 2012 Oct 19;37(4):601-10 PMID: 23084357
  115. Bacterial flagellin stimulates Toll-like receptor 5-dependent defense against vancomycin-resistant Enterococcus infection.
    J Infect Dis. 2010 Feb 15;201(4):534-43 PMID: 20064069
  116. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases.
    Proc Natl Acad Sci U S A. 2007 Aug 21;104(34):13780-5 PMID: 17699621
  117. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells.
    Immunity. 2010 Jun 25;32(6):815-27 PMID: 20620945
  118. Identifying gut microbe-host phenotype relationships using combinatorial communities in gnotobiotic mice.
    Sci Transl Med. 2014 Jan 22;6(220):220ra11 PMID: 24452263
  119. Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris.
    Science. 2010 Jun 11;328(5984):1391-4 PMID: 20538949
  120. Enterotypes of the human gut microbiome.
    Nature. 2011 May 12;473(7346):174-80 PMID: 21508958
  121. Microbiota-induced tertiary lymphoid tissues aggravate inflammatory disease in the absence of RORgamma t and LTi cells.
    J Exp Med. 2011 Jan 17;208(1):125-34 PMID: 21173107
  122. Plasticity of Th17 cells in Peyer's patches is responsible for the induction of T cell-dependent IgA responses.
    Nat Immunol. 2013 Apr;14(4):372-9 PMID: 23475182
  123. Nonredundant function of soluble LTα3 produced by innate lymphoid cells in intestinal homeostasis.
    Science. 2013 Dec 6;342(6163):1243-6 PMID: 24311691
  124. 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. 2007 Aug 6;204(8):1757-64 PMID: 17620361
  125. Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis.
    Nat Immunol. 2009 Nov;10(11):1178-84 PMID: 19783988
  126. Therapeutic potential of fecal microbiota transplantation.
    Gastroenterology. 2013 Nov;145(5):946-53 PMID: 24018052
  127. The NLRP3 inflammasome protects against loss of epithelial integrity and mortality during experimental colitis.
    Immunity. 2010 Mar 26;32(3):379-91 PMID: 20303296
  128. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense.
    Immunity. 2008 Dec 19;29(6):958-70 PMID: 19084435
  129. The habitat, double life, citizenship, and forgetfulness of IgA.
    Immunol Rev. 2012 Jan;245(1):132-46 PMID: 22168417
  130. Group 3 innate lymphoid cells inhibit T-cell-mediated intestinal inflammation through aryl hydrocarbon receptor signaling and regulation of microflora.
    Immunity. 2013 Aug 22;39(2):386-99 PMID: 23954130
  131. Alterations in the microbiota drive interleukin-17C production from intestinal epithelial cells to promote tumorigenesis.
    Immunity. 2014 Jan 16;40(1):140-52 PMID: 24412611
  132. Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis.
    Immunity. 2014 Jan 16;40(1):128-39 PMID: 24412617
  133. NLRC4-driven production of IL-1β discriminates between pathogenic and commensal bacteria and promotes host intestinal defense.
    Nat Immunol. 2012 May;13(5):449-56 PMID: 22484733
  134. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells.
    Nature. 2013 Dec 19;504(7480):446-50 PMID: 24226770
  135. RORgammat and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells.
    Nat Immunol. 2009 Jan;10(1):83-91 PMID: 19029903
  136. Diversity of the human intestinal microbial flora.
    Science. 2005 Jun 10;308(5728):1635-8 PMID: 15831718
  137. TLR5 signaling stimulates the innate production of IL-17 and IL-22 by CD3(neg)CD127+ immune cells in spleen and mucosa.
    J Immunol. 2010 Jul 15;185(2):1177-85 PMID: 20566828
  138. Intestinal homeostasis and its breakdown in inflammatory bowel disease.
    Nature. 2011 Jun 15;474(7351):298-306 PMID: 21677746
  139. Mice carrying a knock-in mutation of Aicda resulting in a defect in somatic hypermutation have impaired gut homeostasis and compromised mucosal defense.
    Nat Immunol. 2011 Mar;12(3):264-70 PMID: 21258321
  140. Induction of intestinal Th17 cells by segmented filamentous bacteria.
    Cell. 2009 Oct 30;139(3):485-98 PMID: 19836068
  141. IL-1β mediates chronic intestinal inflammation by promoting the accumulation of IL-17A secreting innate lymphoid cells and CD4(+) Th17 cells.
    J Exp Med. 2012 Aug 27;209(9):1595-609 PMID: 22891275
  142. RORγt+ innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota.
    Nat Immunol. 2011 Apr;12(4):320-6 PMID: 21336274
Article Info
Journal
Trends in immunology
Abbr.
Trends Immunol
ISSN
1471-4981
Published
2014-11-00
Epub
2014-00-27
Pages
507-17
Language
English
Region
England
NLM ID
100966032
PMCID
PMC6485503
Subset
IM
Grants
Wellcome Trust · United Kingdom
Wellcome Trust · 102972 · United Kingdom
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