Home LiteratureArticle Details
PMID: 28856738 Published · ppublish English Journal Article Review

Gut microbiota: Role in pathogen colonization, immune responses, and inflammatory disease.

Immunological reviews ·Vol. 279 ·No. 1 ·2017-09-00 ·Pages 70-89

Pickard JM, Zeng MY, Caruso R, Núñez G

Abstract

The intestinal tract of mammals is colonized by a large number of microorganisms including trillions of bacteria that are referred to collectively as the gut microbiota. These indigenous microorganisms have co-evolved with the host in a symbiotic relationship. In addition to metabolic benefits, symbiotic bacteria provide the host with several functions that promote immune homeostasis, immune responses, and protection against pathogen colonization. The ability of symbiotic bacteria to inhibit pathogen colonization is mediated via several mechanisms including direct killing, competition for limited nutrients, and enhancement of immune responses. Pathogens have evolved strategies to promote their replication in the presence of the gut microbiota. Perturbation of the gut microbiota structure by environmental and genetic factors increases the risk of pathogen infection, promotes the overgrowth of harmful pathobionts, and the development of inflammatory disease. Understanding the interaction of the microbiota with pathogens and the immune system will provide critical insight into the pathogenesis of disease and the development of strategies to prevent and treat inflammatory disease.

Keywords
bacterial colonization resistance gut microbiota inflammatory bowel disease mucosa
MeSH Terms
Animals Dysbiosis/immunology Gastrointestinal Microbiome/immunology Homeostasis Humans Immunity Inflammation/microbiology Inflammatory Bowel Diseases/immunology Intestinal Mucosa/immunology,microbiology Symbiosis
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Pickard Joseph M
Department of Pathology and Comprehensive Cancer Center, The University of Michigan Medical School, Ann Arbor, MI, USA.
Zeng Melody Y
Department of Pathology and Comprehensive Cancer Center, The University of Michigan Medical School, Ann Arbor, MI, USA.
Caruso Roberta
Department of Pathology and Comprehensive Cancer Center, The University of Michigan Medical School, Ann Arbor, MI, USA.
Núñez Gabriel ORCID
Department of Pathology and Comprehensive Cancer Center, The University of Michigan Medical School, Ann Arbor, MI, USA.
References (230)
230 references, click to expand
  1. Linking long-term dietary patterns with gut microbial enterotypes.
    Science. 2011 Oct 7;334(6052):105-8 PMID: 21885731
  2. Absence of epithelial immunoglobulin A transport, with increased mucosal leakiness, in polymeric immunoglobulin receptor/secretory component-deficient mice.
    J Exp Med. 1999 Oct 4;190(7):915-22 PMID: 10510081
  3. A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem.
    Proc Natl Acad Sci U S A. 1999 Aug 17;96(17):9833-8 PMID: 10449780
  4. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells.
    Nature. 2013 Dec 19;504(7480):446-50 PMID: 24226770
  5. Mucosal flora in inflammatory bowel disease.
    Gastroenterology. 2002 Jan;122(1):44-54 PMID: 11781279
  6. Host-mediated sugar oxidation promotes post-antibiotic pathogen expansion.
    Nature. 2016 Jun 30;534(7609):697-9 PMID: 27309805
  7. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection.
    Gastroenterology. 2006 Jul;131(1):117-29 PMID: 16831596
  8. Human symbionts inject and neutralize antibacterial toxins to persist in the gut.
    Proc Natl Acad Sci U S A. 2016 Mar 29;113(13):3639-44 PMID: 26957597
  9. 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
  10. RESISTANCE OF THE MOUSE'S INTESTINAL TRACT TO EXPERIMENTAL SALMONELLA INFECTION. II. FACTORS RESPONSIBLE FOR ITS LOSS FOLLOWING STREPTOMYCIN TREATMENT.
    J Exp Med. 1964 Nov 1;120:817-28 PMID: 14247722
  11. A Dietary Fiber-Deprived Gut Microbiota Degrades the Colonic Mucus Barrier and Enhances Pathogen Susceptibility.
    Cell. 2016 Nov 17;167(5):1339-1353.e21 PMID: 27863247
  12. Humoral Immunity in the Gut Selectively Targets Phenotypically Virulent Attaching-and-Effacing Bacteria for Intraluminal Elimination.
    Cell Host Microbe. 2015 May 13;17(5):617-27 PMID: 25936799
  13. Healthy human gut phageome.
    Proc Natl Acad Sci U S A. 2016 Sep 13;113(37):10400-5 PMID: 27573828
  14. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria.
    Science. 2000 Jun 23;288(5474):2222-6 PMID: 10864873
  15. Differences between tissue-associated intestinal microfloras of patients with Crohn's disease and ulcerative colitis.
    J Clin Microbiol. 2006 Nov;44(11):4136-41 PMID: 16988016
  16. CEACAM6 acts as a receptor for adherent-invasive E. coli, supporting ileal mucosa colonization in Crohn disease.
    J Clin Invest. 2007 Jun;117(6):1566-74 PMID: 17525800
  17. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment.
    Genome Biol. 2012 Apr 16;13(9):R79 PMID: 23013615
  18. Eating for two: how metabolism establishes interspecies interactions in the gut.
    Cell Host Microbe. 2011 Oct 20;10(4):336-47 PMID: 22018234
  19. Virulence factors enhance Citrobacter rodentium expansion through aerobic respiration.
    Science. 2016 Sep 16;353(6305):1249-53 PMID: 27634526
  20. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile.
    Nature. 2015 Jan 8;517(7533):205-8 PMID: 25337874
  21. Regulation and function of innate and adaptive interleukin-17-producing cells.
    EMBO Rep. 2012 Feb 01;13(2):113-20 PMID: 22193778
  22. Innate lymphoid cells regulate intestinal epithelial cell glycosylation.
    Science. 2014 Sep 12;345(6202):1254009 PMID: 25214634
  23. Dominant and diet-responsive groups of bacteria within the human colonic microbiota.
    ISME J. 2011 Feb;5(2):220-30 PMID: 20686513
  24. Role of volatile fatty acids in colonization resistance to Clostridium difficile.
    Infect Immun. 1984 Jul;45(1):185-91 PMID: 6735467
  25. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation.
    Nature. 2013 Dec 19;504(7480):451-5 PMID: 24226773
  26. Interleukin-10-deficient mice develop chronic enterocolitis.
    Cell. 1993 Oct 22;75(2):263-74 PMID: 8402911
  27. The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells.
    Immunity. 2012 Jan 27;36(1):92-104 PMID: 22177117
  28. Intestinal inflammation targets cancer-inducing activity of the microbiota.
    Science. 2012 Oct 5;338(6103):120-3 PMID: 22903521
  29. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system.
    Cell. 2007 Oct 5;131(1):33-45 PMID: 17923086
  30. Inflammation boosts bacteriophage transfer between Salmonella spp.
    Science. 2017 Mar 17;355(6330):1211-1215 PMID: 28302859
  31. Selective IgA deficiency.
    J Clin Immunol. 2010 Jan;30(1):10-6 PMID: 20101521
  32. Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis.
    Infect Immun. 2011 Apr;79(4):1536-45 PMID: 21321077
  33. Inflammation fuels colicin Ib-dependent competition of Salmonella serovar Typhimurium and E. coli in enterobacterial blooms.
    PLoS Pathog. 2014 Jan;10(1):e1003844 PMID: 24391500
  34. Antibiotics increase functional abdominal symptoms.
    Am J Gastroenterol. 2002 Jan;97(1):104-8 PMID: 11808932
  35. Ciprofloxacin or metronidazole for the treatment of perianal fistulas in patients with Crohn's disease: a randomized, double-blind, placebo-controlled pilot study.
    Inflamm Bowel Dis. 2009 Jan;15(1):17-24 PMID: 18668682
  36. Dysbiosis, inflammation, and response to treatment: a longitudinal study of pediatric subjects with newly diagnosed inflammatory bowel disease.
    Genome Med. 2016 Jul 13;8(1):75 PMID: 27412252
  37. Microbial community analysis reveals high level phylogenetic alterations in the overall gastrointestinal microbiota of diarrhoea-predominant irritable bowel syndrome sufferers.
    BMC Gastroenterol. 2009 Dec 17;9:95 PMID: 20015409
  38. Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice.
    Nat Immunol. 2014 Oct;15(10 ):929-937 PMID: 25151491
  39. The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats.
    J Exp Med. 1994 Dec 1;180(6):2359-64 PMID: 7964509
  40. Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors.
    Biochim Biophys Acta. 1997 Jul 4;1320(3):217-34 PMID: 9230919
  41. Role of the gut microbiota in immunity and inflammatory disease.
    Nat Rev Immunol. 2013 May;13(5):321-35 PMID: 23618829
  42. Development and regulation of RORγt(+) innate lymphoid cells.
    FEBS Lett. 2014 Nov 17;588(22):4176-81 PMID: 24681095
  43. Salmonella uses energy taxis to benefit from intestinal inflammation.
    PLoS Pathog. 2013;9(4):e1003267 PMID: 23637594
  44. Lethal inflammasome activation by a multidrug-resistant pathobiont upon antibiotic disruption of the microbiota.
    Nat Med. 2012 May;18(5):799-806 PMID: 22522562
  45. Point mutations in FimH adhesin of Crohn's disease-associated adherent-invasive Escherichia coli enhance intestinal inflammatory response.
    PLoS Pathog. 2013 Jan;9(1):e1003141 PMID: 23358328
  46. Stable Engraftment of Bifidobacterium longum AH1206 in the Human Gut Depends on Individualized Features of the Resident Microbiome.
    Cell Host Microbe. 2016 Oct 12;20(4):515-526 PMID: 27693307
  47. Regulated virulence controls the ability of a pathogen to compete with the gut microbiota.
    Science. 2012 Jun 8;336(6086):1325-9 PMID: 22582016
  48. Nod2-mediated recognition of the microbiota is critical for mucosal adjuvant activity of cholera toxin.
    Nat Med. 2016 May;22(5):524-30 PMID: 27064448
  49. Innate Immune Defenses Mediated by Two ILC Subsets Are Critical for Protection against Acute Clostridium difficile Infection.
    Cell Host Microbe. 2015 Jul 8;18(1):27-37 PMID: 26159718
  50. Immunobiology and immunopathology of human gut mucosa: humoral immunity and intraepithelial lymphocytes.
    Gastroenterology. 1989 Dec;97(6):1562-84 PMID: 2684725
  51. Antibiotic use, childhood affluence and irritable bowel syndrome (IBS).
    Eur J Gastroenterol Hepatol. 1998 Jan;10(1):59-62 PMID: 9512954
  52. A microbial symbiosis factor prevents intestinal inflammatory disease.
    Nature. 2008 May 29;453(7195):620-5 PMID: 18509436
  53. Neonatal acquisition of Clostridia species protects against colonization by bacterial pathogens.
    Science. 2017 Apr 21;356(6335):315-319 PMID: 28428425
  54. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens.
    Nature. 2013 Oct 3;502(7469):96-9 PMID: 23995682
  55. Short-chain organic acids at ph 5.0 kill Escherichia coli and Salmonella spp. without causing membrane perturbation.
    J Appl Bacteriol. 1991 Feb;70(2):161-5 PMID: 1902205
  56. Lactoferrin and host defense.
    Biochem Cell Biol. 2002;80(1):95-102 PMID: 11908649
  57. Normalization of Host Intestinal Mucus Layers Requires Long-Term Microbial Colonization.
    Cell Host Microbe. 2015 Nov 11;18(5):582-92 PMID: 26526499
  58. Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut.
    Cell Host Microbe. 2012 Mar 15;11(3):227-39 PMID: 22423963
  59. Ethanolamine utilization in bacterial pathogens: roles and regulation.
    Nat Rev Microbiol. 2010 Apr;8(4):290-5 PMID: 20234377
  60. Nutrient metal sequestration by calprotectin inhibits bacterial superoxide defense, enhancing neutrophil killing of Staphylococcus aureus.
    Cell Host Microbe. 2011 Aug 18;10(2):158-64 PMID: 21843872
  61. Gut inflammation provides a respiratory electron acceptor for Salmonella.
    Nature. 2010 Sep 23;467(7314):426-9 PMID: 20864996
  62. Bile salt biotransformations by human intestinal bacteria.
    J Lipid Res. 2006 Feb;47(2):241-59 PMID: 16299351
  63. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria.
    Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15064-9 PMID: 18806221
  64. Intestinal bacterial colonization induces mutualistic regulatory T cell responses.
    Immunity. 2011 May 27;34(5):794-806 PMID: 21596591
  65. Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness.
    Nature. 2014 Oct 30;514(7524):638-41 PMID: 25274297
  66. Common gamma-chain-dependent signals confer selective survival of eosinophils in the murine small intestine.
    J Immunol. 2009 Nov 1;183(9):5600-7 PMID: 19843944
  67. Host-derived sialic acid is incorporated into Haemophilus influenzae lipopolysaccharide and is a major virulence factor in experimental otitis media.
    Proc Natl Acad Sci U S A. 2003 Jul 22;100(15):8898-903 PMID: 12855765
  68. RESISTANCE OF THE MOUSE'S INTESTINAL TRACT TO EXPERIMENTAL SALMONELLA INFECTION. I. FACTORS WHICH INTERFERE WITH THE INITIATION OF INFECTION BY ORAL INOCULATION.
    J Exp Med. 1964 Nov 1;120:805-16 PMID: 14247721
  69. Role of competition for nutrients in suppression of Clostridium difficile by the colonic microflora.
    Infect Immun. 1988 Oct;56(10):2610-4 PMID: 3417352
  70. Strain competition restricts colonization of an enteric pathogen and prevents colitis.
    EMBO Rep. 2016 Sep;17 (9):1281-91 PMID: 27432285
  71. Postnatal acquisition of endotoxin tolerance in intestinal epithelial cells.
    J Exp Med. 2006 Apr 17;203(4):973-84 PMID: 16606665
  72. The microbiota regulates neutrophil homeostasis and host resistance to Escherichia coli K1 sepsis in neonatal mice.
    Nat Med. 2014 May;20(5):524-30 PMID: 24747744
  73. Role of intestinal bacteria in gliadin-induced changes in intestinal mucosa: study in germ-free rats.
    PLoS One. 2011 Jan 13;6(1):e16169 PMID: 21249146
  74. NOD1 and NOD2: signaling, host defense, and inflammatory disease.
    Immunity. 2014 Dec 18;41(6):898-908 PMID: 25526305
  75. Mucosal antibodies in inflammatory bowel disease are directed against intestinal bacteria.
    Gut. 1996 Mar;38(3):365-75 PMID: 8675088
  76. Microevolution in fimH gene of mucosa-associated Escherichia coli strains isolated from pediatric patients with inflammatory bowel disease.
    Infect Immun. 2012 Apr;80(4):1408-17 PMID: 22290143
  77. Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations.
    Cell. 2010 Jun 25;141(7):1241-52 PMID: 20603004
  78. Role of competition for substrate in bacterial antagonism in the gut.
    Infect Immun. 1982 Dec;38(3):887-92 PMID: 6759411
  79. 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
  80. Microbiota-derived compounds drive steady-state granulopoiesis via MyD88/TICAM signaling.
    J Immunol. 2014 Nov 15;193(10):5273-83 PMID: 25305320
  81. Composition and temporal stability of gastrointestinal microbiota in irritable bowel syndrome--a longitudinal study in IBS and control subjects.
    FEMS Immunol Med Microbiol. 2005 Feb 1;43(2):213-22 PMID: 15747442
  82. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach.
    Gut. 2006 Feb;55(2):205-11 PMID: 16188921
  83. The battle for iron between bacterial pathogens and their vertebrate hosts.
    PLoS Pathog. 2010 Aug 12;6(8):e1000949 PMID: 20711357
  84. Transient inability to manage proteobacteria promotes chronic gut inflammation in TLR5-deficient mice.
    Cell Host Microbe. 2012 Aug 16;12(2):139-52 PMID: 22863420
  85. Generation of polymeric immunoglobulin receptor-deficient mouse with marked reduction of secretory IgA.
    J Immunol. 1999 Nov 15;163(10):5367-73 PMID: 10553061
  86. Bacterial colonization factors control specificity and stability of the gut microbiota.
    Nature. 2013 Sep 19;501(7467):426-9 PMID: 23955152
  87. The mucin Muc2 limits pathogen burdens and epithelial barrier dysfunction during Salmonella enterica serovar Typhimurium colitis.
    Infect Immun. 2013 Oct;81(10):3672-83 PMID: 23876803
  88. A type VI secretion-related pathway in Bacteroidetes mediates interbacterial antagonism.
    Cell Host Microbe. 2014 Aug 13;16(2):227-236 PMID: 25070807
  89. Association of antibody responses to microbial antigens and complications of small bowel Crohn's disease.
    Gastroenterology. 2004 Feb;126(2):414-24 PMID: 14762777
  90. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease.
    Nature. 2001 May 31;411(6837):603-6 PMID: 11385577
  91. Antibiotics impair murine hematopoiesis by depleting the intestinal microbiota.
    Blood. 2017 Feb 9;129(6):729-739 PMID: 27879260
  92. A synonymous variant in IRGM alters a binding site for miR-196 and causes deregulation of IRGM-dependent xenophagy in Crohn's disease.
    Nat Genet. 2011 Mar;43(3):242-5 PMID: 21278745
  93. Inflammation-associated adherent-invasive Escherichia coli are enriched in pathways for use of propanediol and iron and M-cell translocation.
    Inflamm Bowel Dis. 2014 Nov;20(11):1919-32 PMID: 25230163
  94. Induction of intestinal Th17 cells by segmented filamentous bacteria.
    Cell. 2009 Oct 30;139(3):485-98 PMID: 19836068
  95. Effects of diet on resource utilization by a model human gut microbiota containing Bacteroides cellulosilyticus WH2, a symbiont with an extensive glycobiome.
    PLoS Biol. 2013;11(8):e1001637 PMID: 23976882
  96. Molecular analysis of faecal and duodenal samples reveals significantly higher prevalence and numbers of Pseudomonas aeruginosa in irritable bowel syndrome.
    J Med Microbiol. 2011 Feb;60(Pt 2):236-45 PMID: 20947663
  97. Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection.
    Nat Commun. 2014;5:3114 PMID: 24445449
  98. 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
  99. Influence of intestinal anaerobes and organic acids on the growth of enterohaemorrhagic Escherichia coli O157:H7.
    J Med Microbiol. 2002 Mar;51(3):201-6 PMID: 11871614
  100. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota.
    PLoS Biol. 2007 Oct;5(10):2177-89 PMID: 17760501
  101. CRISPR targeting reveals a reservoir of common phages associated with the human gut microbiome.
    Genome Res. 2012 Oct;22(10):1985-94 PMID: 22732228
  102. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease.
    Gastroenterology. 2004 Aug;127(2):412-21 PMID: 15300573
  103. Streptomycin-induced inflammation enhances Escherichia coli gut colonization through nitrate respiration.
    MBio. 2013 Jul 02;4(4):null PMID: 23820397
  104. Microcins mediate competition among Enterobacteriaceae in the inflamed gut.
    Nature. 2016 Dec 8;540(7632):280-283 PMID: 27798599
  105. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae.
    Cell Host Microbe. 2007 Aug 16;2(2):119-29 PMID: 18005726
  106. Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis.
    Nat Genet. 2007 May;39(5):596-604 PMID: 17435756
  107. Rifaximin-extended intestinal release induces remission in patients with moderately active Crohn's disease.
    Gastroenterology. 2012 Mar;142(3):473-481.e4 PMID: 22155172
  108. Profound alterations of intestinal microbiota following a single dose of clindamycin results in sustained susceptibility to Clostridium difficile-induced colitis.
    Infect Immun. 2012 Jan;80(1):62-73 PMID: 22006564
  109. How glycan metabolism shapes the human gut microbiota.
    Nat Rev Microbiol. 2012 Apr 11;10(5):323-35 PMID: 22491358
  110. Genome sequence of adherent-invasive Escherichia coli and comparative genomic analysis with other E. coli pathotypes.
    BMC Genomics. 2010 Nov 25;11:667 PMID: 21108814
  111. Homeland security: IgA immunity at the frontiers of the body.
    Trends Immunol. 2012 Apr;33(4):160-7 PMID: 22410243
  112. Alterations of the dominant faecal bacterial groups in patients with Crohn's disease of the colon.
    Gut. 2003 Feb;52(2):237-42 PMID: 12524406
  113. Early lesions of recurrent Crohn's disease caused by infusion of intestinal contents in excluded ileum.
    Gastroenterology. 1998 Feb;114(2):262-7 PMID: 9453485
  114. Maternal IgG and IgA Antibodies Dampen Mucosal T Helper Cell Responses in Early Life.
    Cell. 2016 May 5;165(4):827-41 PMID: 27153495
  115. Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut.
    Immunity. 2008 Aug 15;29(2):261-71 PMID: 18656387
  116. Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria.
    Science. 2012 Jun 8;336(6086):1321-5 PMID: 22674331
  117. Enteric salmonellosis disrupts the microbial ecology of the murine gastrointestinal tract.
    Infect Immun. 2008 Mar;76(3):907-15 PMID: 18160481
  118. Persistence of colicinogenic Escherichia coli in the mouse gastrointestinal tract.
    BMC Microbiol. 2009 Aug 12;9:165 PMID: 19674447
  119. Predicting a human gut microbiota's response to diet in gnotobiotic mice.
    Science. 2011 Jul 1;333(6038):101-4 PMID: 21596954
  120. Immunoglobulin A coating identifies colitogenic bacteria in inflammatory bowel disease.
    Cell. 2014 Aug 28;158(5):1000-1010 PMID: 25171403
  121. Intestinal Microbiota Signatures Associated with Inflammation History in Mice Experiencing Recurring Colitis.
    Front Microbiol. 2015 Dec 15;6:1408 PMID: 26697002
  122. Interleukin-22 regulates the complement system to promote resistance against pathobionts after pathogen-induced intestinal damage.
    Immunity. 2014 Oct 16;41(4):620-32 PMID: 25367575
  123. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis.
    Science. 2013 Aug 2;341(6145):569-73 PMID: 23828891
  124. Bacteriocin production augments niche competition by enterococci in the mammalian gastrointestinal tract.
    Nature. 2015 Oct 29;526(7575):719-22 PMID: 26479034
  125. A composite bacteriophage alters colonization by an intestinal commensal bacterium.
    Proc Natl Acad Sci U S A. 2012 Oct 23;109(43):17621-6 PMID: 23045666
  126. Intestinal Muc2 mucin O-glycosylation is affected by microbiota and regulated by differential expression of glycosyltranferases.
    Glycobiology. 2017 Apr 1;27(4):318-328 PMID: 28122822
  127. Mechanisms by which anaerobic microbiota inhibit the establishment in mice of intestinal colonization by vancomycin-resistant Enterococcus.
    J Infect Dis. 2005 Mar 15;191(6):949-56 PMID: 15717271
  128. Gut microbiota promote hematopoiesis to control bacterial infection.
    Cell Host Microbe. 2014 Mar 12;15(3):374-81 PMID: 24629343
  129. Enhanced Escherichia coli adherence and invasion in Crohn's disease and colon cancer.
    Gastroenterology. 2004 Jul;127(1):80-93 PMID: 15236175
  130. Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles.
    Science. 2011 Dec 16;334(6062):1561-5 PMID: 22033518
  131. Infection mobilizes hematopoietic stem cells through cooperative NOD-like receptor and Toll-like receptor signaling.
    Cell Host Microbe. 2014 Jun 11;15(6):779-91 PMID: 24882704
  132. Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma.
    EMBO Rep. 2012 May 01;13(5):440-7 PMID: 22422004
  133. 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
  134. An IL-23R/IL-22 Circuit Regulates Epithelial Serum Amyloid A to Promote Local Effector Th17 Responses.
    Cell. 2015 Oct 8;163(2):381-93 PMID: 26411290
  135. Consumption of human milk oligosaccharides by gut-related microbes.
    J Agric Food Chem. 2010 May 12;58(9):5334-40 PMID: 20394371
  136. Bacterial flagellin is a dominant antigen in Crohn disease.
    J Clin Invest. 2004 May;113(9):1296-306 PMID: 15124021
  137. Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn's disease involving the ileum.
    ISME J. 2007 Sep;1(5):403-18 PMID: 18043660
  138. Oral treatment with live Lactobacillus reuteri inhibits the allergic airway response in mice.
    Am J Respir Crit Care Med. 2007 Mar 15;175(6):561-9 PMID: 17204726
  139. Salmonella Mitigates Oxidative Stress and Thrives in the Inflamed Gut by Evading Calprotectin-Mediated Manganese Sequestration.
    Cell Host Microbe. 2016 Jun 8;19(6):814-25 PMID: 27281571
  140. 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
  141. Small intestinal eosinophils regulate Th17 cells by producing IL-1 receptor antagonist.
    J Exp Med. 2016 Apr 4;213(4):555-67 PMID: 26951334
  142. Regulatory Eosinophils in Inflammation and Metabolic Disorders.
    Immune Netw. 2017 Feb;17 (1):41-47 PMID: 28261019
  143. Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118.
    Proc Natl Acad Sci U S A. 2007 May 1;104(18):7617-21 PMID: 17456596
  144. Intestinal microbiota shifts towards elevated commensal Escherichia coli loads abrogate colonization resistance against Campylobacter jejuni in mice.
    PLoS One. 2012;7(5):e35988 PMID: 22563475
  145. Microbial colonization influences early B-lineage development in the gut lamina propria.
    Nature. 2013 Sep 5;501(7465):112-5 PMID: 23965619
  146. The treatment-naive microbiome in new-onset Crohn's disease.
    Cell Host Microbe. 2014 Mar 12;15(3):382-392 PMID: 24629344
  147. Gene-microbiota interactions contribute to the pathogenesis of inflammatory bowel disease.
    Science. 2016 May 27;352(6289):1116-20 PMID: 27230380
  148. Bacteriophage therapy.
    Antimicrob Agents Chemother. 2001 Mar;45(3):649-59 PMID: 11181338
  149. Gut Microbiota-Induced Immunoglobulin G Controls Systemic Infection by Symbiotic Bacteria and Pathogens.
    Immunity. 2016 Mar 15;44(3):647-658 PMID: 26944199
  150. Diversity of the human intestinal microbial flora.
    Science. 2005 Jun 10;308(5728):1635-8 PMID: 15831718
  151. Dysbiotic gut microbiota causes transmissible Crohn's disease-like ileitis independent of failure in antimicrobial defence.
    Gut. 2016 Feb;65(2):225-37 PMID: 25887379
  152. Mucosal lipocalin 2 has pro-inflammatory and iron-sequestering effects in response to bacterial enterobactin.
    PLoS Pathog. 2009 Oct;5(10 ):e1000622 PMID: 19834550
  153. The bacterial LexA transcriptional repressor.
    Cell Mol Life Sci. 2009 Jan;66(1):82-93 PMID: 18726173
  154. Fucose sensing regulates bacterial intestinal colonization.
    Nature. 2012 Dec 6;492(7427):113-7 PMID: 23160491
  155. Immune tolerance. Group 3 innate lymphoid cells mediate intestinal selection of commensal bacteria-specific CD4⁺ T cells.
    Science. 2015 May 29;348(6238):1031-5 PMID: 25908663
  156. Distinct Commensals Induce Interleukin-1β via NLRP3 Inflammasome in Inflammatory Monocytes to Promote Intestinal Inflammation in Response to Injury.
    Immunity. 2015 Apr 21;42(4):744-55 PMID: 25862092
  157. Appearance of fucolipid after conventionalization of germ-free mice.
    J Biochem. 1981 Aug;90(2):559-61 PMID: 7298602
  158. Identifying gut microbe-host phenotype relationships using combinatorial communities in gnotobiotic mice.
    Sci Transl Med. 2014 Jan 22;6(220):220ra11 PMID: 24452263
  159. Butyrate specifically down-regulates salmonella pathogenicity island 1 gene expression.
    Appl Environ Microbiol. 2006 Jan;72(1):946-9 PMID: 16391141
  160. Colicin biology.
    Microbiol Mol Biol Rev. 2007 Mar;71(1):158-229 PMID: 17347522
  161. Depletion of Butyrate-Producing Clostridia from the Gut Microbiota Drives an Aerobic Luminal Expansion of Salmonella.
    Cell Host Microbe. 2016 Apr 13;19(4):443-54 PMID: 27078066
  162. Sialic acid catabolism drives intestinal inflammation and microbial dysbiosis in mice.
    Nat Commun. 2015 Aug 25;6:8141 PMID: 26303108
  163. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice.
    Sci Transl Med. 2009 Nov 11;1(6):6ra14 PMID: 20368178
  164. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota.
    Nature. 2013 Aug 8;500(7461):232-6 PMID: 23842501
  165. Susceptibility to Campylobacter infection is associated with the species composition of the human fecal microbiota.
    MBio. 2014 Sep 16;5(5):e01212-14 PMID: 25227462
  166. Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity.
    J Clin Invest. 2005 Jan;115(1):66-75 PMID: 15630445
  167. Viruses in the faecal microbiota of monozygotic twins and their mothers.
    Nature. 2010 Jul 15;466(7304):334-8 PMID: 20631792
  168. Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease.
    Proc Natl Acad Sci U S A. 2012 Jan 10;109(2):594-9 PMID: 22184244
  169. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls.
    Nature. 2007 Jun 7;447(7145):661-78 PMID: 17554300
  170. The dynamics of gut-associated microbial communities during inflammation.
    EMBO Rep. 2013 Apr;14(4):319-27 PMID: 23478337
  171. Phage-mediated acquisition of a type III secreted effector protein boosts growth of salmonella by nitrate respiration.
    MBio. 2012 Jun 12;3(3):null PMID: 22691391
  172. IL-22 Controls Iron-Dependent Nutritional Immunity Against Systemic Bacterial Infections.
    Sci Immunol. 2017 Feb;2(8): PMID: 28286877
  173. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis.
    Cell Host Microbe. 2010 Sep 16;8(3):292-300 PMID: 20833380
  174. Mechanisms that control bacterial populations in continuous-flow culture models of mouse large intestinal flora.
    Infect Immun. 1983 Feb;39(2):676-85 PMID: 6339388
  175. Gram-positive bacteria are held at a distance in the colon mucus by the lectin-like protein ZG16.
    Proc Natl Acad Sci U S A. 2016 Nov 29;113(48):13833-13838 PMID: 27849619
  176. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease.
    Nature. 2001 May 31;411(6837):599-603 PMID: 11385576
  177. Colorectal cancer in mice genetically deficient in the mucin Muc2.
    Science. 2002 Mar 1;295(5560):1726-9 PMID: 11872843
  178. Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the murine gut mucosal immune system.
    Infect Immun. 1999 Apr;67(4):1992-2000 PMID: 10085047
  179. Dysregulation of allergic airway inflammation in the absence of microbial colonization.
    Am J Respir Crit Care Med. 2011 Jul 15;184(2):198-205 PMID: 21471101
  180. Epithelial hypoxia-inducible factor-1 is protective in murine experimental colitis.
    J Clin Invest. 2004 Oct;114(8):1098-106 PMID: 15489957
  181. Metagenomic approaches for defining the pathogenesis of inflammatory bowel diseases.
    Cell Host Microbe. 2008 Jun 12;3(6):417-27 PMID: 18541218
  182. A strain of Enterococcus faecium (18C23) inhibits adhesion of enterotoxigenic Escherichia coli K88 to porcine small intestine mucus.
    Appl Environ Microbiol. 2000 Oct;66(10):4200-4 PMID: 11010860
  183. Tissue-resident macrophages: then and now.
    Immunology. 2015 Apr;144(4):541-8 PMID: 25684236
  184. Formate acts as a diffusible signal to induce Salmonella invasion.
    J Bacteriol. 2008 Jun;190(12 ):4233-41 PMID: 18424519
  185. Gut microbiota-produced succinate promotes C. difficile infection after antibiotic treatment or motility disturbance.
    Cell Host Microbe. 2014 Dec 10;16(6):770-7 PMID: 25498344
  186. Th17 Cell Induction by Adhesion of Microbes to Intestinal Epithelial Cells.
    Cell. 2015 Oct 8;163(2):367-80 PMID: 26411289
  187. 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
  188. Effect of faecal stream diversion on recurrence of Crohn's disease in the neoterminal ileum.
    Lancet. 1991 Sep 28;338(8770):771-4 PMID: 1681159
  189. The fatal enteric cholera infection in the guinea pig, achieved by inhibition of normal enteric flora.
    J Infect Dis. 1955 Jul-Aug;97(1):57-65 PMID: 13242854
  190. Neutrophil ageing is regulated by the microbiome.
    Nature. 2015 Sep 24;525(7570):528-32 PMID: 26374999
  191. Intestinal microbiota modulates gluten-induced immunopathology in humanized mice.
    Am J Pathol. 2015 Nov;185(11):2969-82 PMID: 26456581
  192. Interplay between enterobactin, myeloperoxidase and lipocalin 2 regulates E. coli survival in the inflamed gut.
    Nat Commun. 2015 May 12;6:7113 PMID: 25964185
  193. Responses to self and non-self intestinal microflora in health and inflammatory bowel disease.
    Res Immunol. 1997 Oct-Dec;148(8-9):589-94 PMID: 9588839
  194. T cell receptor-alpha beta-deficient mice fail to develop colitis in the absence of a microbial environment.
    Am J Pathol. 1997 Jan;150(1):91-7 PMID: 9006326
  195. 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
  196. Probiotic bacteria reduce salmonella typhimurium intestinal colonization by competing for iron.
    Cell Host Microbe. 2013 Jul 17;14(1):26-37 PMID: 23870311
  197. MyD88 is involved in myeloid as well as lymphoid hematopoiesis independent of the presence of a pathogen.
    Am J Blood Res. 2013 May 05;3(2):124-40 PMID: 23675564
  198. Muc2 protects against lethal infectious colitis by disassociating pathogenic and commensal bacteria from the colonic mucosa.
    PLoS Pathog. 2010 May 13;6(5):e1000902 PMID: 20485566
  199. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine.
    Cell Host Microbe. 2008 Oct 16;4(4):337-49 PMID: 18854238
  200. The human gut virome: inter-individual variation and dynamic response to diet.
    Genome Res. 2011 Oct;21(10):1616-25 PMID: 21880779
  201. Effect of streptomycin on susceptibility of intestinal tract to experimental Salmonella infection.
    Proc Soc Exp Biol Med. 1954 May;86(1):132-7 PMID: 13177610
  202. Host-derived nitrate boosts growth of E. coli in the inflamed gut.
    Science. 2013 Feb 8;339(6120):708-11 PMID: 23393266
  203. What is type VI secretion doing in all those bugs?
    Trends Microbiol. 2010 Dec;18(12):531-7 PMID: 20961764
  204. 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
  205. Gastrointestinal microbiome signatures of pediatric patients with irritable bowel syndrome.
    Gastroenterology. 2011 Nov;141(5):1782-91 PMID: 21741921
  206. Ecology of prokaryotic viruses.
    FEMS Microbiol Rev. 2004 May;28(2):127-81 PMID: 15109783
  207. Crohn's disease-associated adherent-invasive E. coli are selectively favoured by impaired autophagy to replicate intracellularly.
    Cell Microbiol. 2010 Jan;12 (1):99-113 PMID: 19747213
  208. Mechanisms of inflammation-driven bacterial dysbiosis in the gut.
    Mucosal Immunol. 2017 Jan;10 (1):18-26 PMID: 27554295
  209. Anti-infective properties of bacteriocins: an update.
    Cell Mol Life Sci. 2013 Aug;70(16):2947-67 PMID: 23109101
  210. Intestinal dysbiosis in preterm infants preceding necrotizing enterocolitis: a systematic review and meta-analysis.
    Microbiome. 2017 Mar 9;5(1):31 PMID: 28274256
  211. Innate lymphoid cell interactions with microbiota: implications for intestinal health and disease.
    Immunity. 2012 Oct 19;37(4):601-10 PMID: 23084357
  212. Interleukin-1beta selectively expands and sustains interleukin-22+ immature human natural killer cells in secondary lymphoid tissue.
    Immunity. 2010 Jun 25;32(6):803-14 PMID: 20620944
  213. 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
  214. Regulation of antibacterial defense in the small intestine by the nuclear bile acid receptor.
    Proc Natl Acad Sci U S A. 2006 Mar 7;103(10 ):3920-5 PMID: 16473946
  215. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide.
    Science. 2013 Nov 22;342(6161):971-6 PMID: 24264990
  216. Parasite-induced TH1 cells and intestinal dysbiosis cooperate in IFN-γ-dependent elimination of Paneth cells.
    Nat Immunol. 2013 Feb;14(2):136-42 PMID: 23263554
  217. The Escherichia coli K-12 gntP gene allows E. coli F-18 to occupy a distinct nutritional niche in the streptomycin-treated mouse large intestine.
    Infect Immun. 1996 Sep;64(9):3497-503 PMID: 8751890
  218. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice.
    Infect Immun. 1998 Nov;66(11):5224-31 PMID: 9784526
  219. Metagenomic analyses of an uncultured viral community from human feces.
    J Bacteriol. 2003 Oct;185(20):6220-3 PMID: 14526037
  220. Intestinal, segmented, filamentous bacteria in a wide range of vertebrate species.
    Lab Anim. 1993 Apr;27(2):141-50 PMID: 8501895
  221. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients.
    Proc Natl Acad Sci U S A. 2008 Oct 28;105(43):16731-6 PMID: 18936492
  222. 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
  223. Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA.
    Mol Microbiol. 2002 Dec;46(5):1451-64 PMID: 12453229
  224. Epithelial IL-22RA1-mediated fucosylation promotes intestinal colonization resistance to an opportunistic pathogen.
    Cell Host Microbe. 2014 Oct 8;16(4):504-16 PMID: 25263220
  225. Reactivity of infiltrating T lymphocytes with microbial antigens in Crohn's disease.
    Lancet. 1991 Nov 16;338(8777):1238-9 PMID: 1682646
  226. The biological functions of T helper 17 cell effector cytokines in inflammation.
    Immunity. 2008 Apr;28(4):454-67 PMID: 18400188
  227. Antibiotic-mediated antagonism leads to a bacterial game of rock-paper-scissors in vivo.
    Nature. 2004 Mar 25;428(6981):412-4 PMID: 15042087
  228. IgE in allergy and asthma today.
    Nat Rev Immunol. 2008 Mar;8(3):205-17 PMID: 18301424
  229. Intestinal microbial diversity during early-life colonization shapes long-term IgE levels.
    Cell Host Microbe. 2013 Nov 13;14(5):559-70 PMID: 24237701
  230. Culture-independent analyses of temporal variation of the dominant fecal microbiota and targeted bacterial subgroups in Crohn's disease.
    J Clin Microbiol. 2006 Nov;44(11):3980-8 PMID: 16988018
Article Info
Journal
Immunological reviews
Abbr.
Immunol Rev
ISSN
1600-065X
DOI
10.1111/imr.12567
Published
2017-09-00
Pages
70-89
Language
English
Region
England
NLM ID
7702118
PMCID
PMC5657496
Subset
IM
Grants
NIDDK NIH HHS · R01 DK091191 · United States
NHLBI NIH HHS · T32 HL007517 · United States
NIDDK NIH HHS · R01 DK061707 · United States
NIDDK NIH HHS · P30 DK034933 · United States
NIDDK NIH HHS · R01 DK095782 · United States
NIDDK NIH HHS · T32 DK094775 · United States
External Links
PubMed source DOI: 10.1111/imr.12567 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2