Home LiteratureArticle Details
PMID: 25120539 Published · epublish English Journal Article Review

Blowing on embers: commensal microbiota and our immune system.

Frontiers in immunology ·Vol. 5 ·2014-00-00 ·Pages 318

Spasova DS, Surh CD

Abstract

Vertebrates have co-evolved with microorganisms resulting in a symbiotic relationship, which plays an important role in health and disease. Skin and mucosal surfaces are colonized with a diverse population of commensal microbiota, over 1000 species, outnumbering the host cells by 10-fold. In the past 40 years, studies have built on the idea that commensal microbiota is in constant contact with the host immune system and thus influence immune function. Recent studies, focusing on mutualism in the gut, have shown that commensal microbiota seems to play a critical role in the development and homeostasis of the host immune system. In particular, the gut microbiota appears to direct the organization and maturation of lymphoid tissues and acts both locally and systemically to regulate the recruitment, differentiation, and function of innate and adaptive immune cells. While the pace of research in the area of the mucosal-immune interface has certainly intensified over the last 10 years, we are still in the early days of this field. Illuminating the mechanisms of how gut microbes shape host immunity will enhance our understanding of the causes of immune-mediated pathologies and improve the design of next-generation vaccines. This review discusses the recent advances in this field, focusing on the close relationship between the adaptive immune system and commensal microbiota, a constant and abundant source of foreign antigens.

Keywords
T cells commensal immune system microbiota regulation
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Spasova Darina S
Kellog School of Science and Technology Doctoral Program in Chemical and Biological Sciences and the Department of Immunology and Microbial Science, The Scripps Research Institute , La Jolla, CA , USA ; Division of Developmental Immunology, La Jolla Institute for Allergy and Immunology , La Jolla, CA , USA.
Surh Charles D
Division of Developmental Immunology, La Jolla Institute for Allergy and Immunology , La Jolla, CA , USA ; Academy of Immunology and Microbiology, Institute of Basic Science , Pohang , South Korea ; Department of Integrative Biosciences and Biotechnology, Pohang University of Science and Technology , Pohang , South Korea.
References (151)
151 references, click to expand
  1. Inflammatory bowel disease.
    N Engl J Med. 2009 Nov 19;361(21):2066-78 PMID: 19923578
  2. Dendritic cells derived from murine colonic mucosa have unique functional and phenotypic characteristics.
    J Immunol. 2007 Jun 15;178(12):7984-93 PMID: 17548635
  3. Inflammatory bowel disease: epidemiology, pathogenesis, and therapeutic opportunities.
    Inflamm Bowel Dis. 2006 Jan;12 Suppl 1:S3-9 PMID: 16378007
  4. Bugs inside Bugs: what the fruit fly can teach us about immune and microbial balance in the gut.
    Cell Host Microbe. 2008 Mar 13;3(3):117-8 PMID: 18329607
  5. Mutualism and parasitism: the yin and yang of plant symbioses.
    Curr Opin Plant Biol. 2006 Aug;9(4):364-70 PMID: 16713732
  6. Host-microbial symbiosis in the mammalian intestine: exploring an internal ecosystem.
    Bioessays. 1998 Apr;20(4):336-43 PMID: 9619105
  7. Taming the beast within: regulation of innate lymphoid cell homeostasis and function.
    J Immunol. 2013 Nov 1;191(9):4489-96 PMID: 24141855
  8. Gut microbiota from twins discordant for obesity modulate metabolism in mice.
    Science. 2013 Sep 6;341(6150):1241214 PMID: 24009397
  9. Commensal host-bacterial relationships in the gut.
    Science. 2001 May 11;292(5519):1115-8 PMID: 11352068
  10. Regulatory T cells: mechanisms of differentiation and function.
    Annu Rev Immunol. 2012;30:531-64 PMID: 22224781
  11. Examining host-microbial interactions through the lens of NOD: From plants to mammals.
    Semin Immunol. 2012 Feb;24(1):9-16 PMID: 22296734
  12. 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
  13. Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues.
    Nat Immunol. 2013 Mar;14(3):221-9 PMID: 23334791
  14. 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
  15. IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis.
    J Exp Med. 2006 Oct 30;203(11):2485-94 PMID: 17030948
  16. Metagenomic analyses reveal antibiotic-induced temporal and spatial changes in intestinal microbiota with associated alterations in immune cell homeostasis.
    Mucosal Immunol. 2010 Mar;3(2):148-58 PMID: 19940845
  17. Recognition and signaling by toll-like receptors.
    Annu Rev Cell Dev Biol. 2006;22:409-37 PMID: 16822173
  18. Interleukin-12 and the regulation of innate resistance and adaptive immunity.
    Nat Rev Immunol. 2003 Feb;3(2):133-46 PMID: 12563297
  19. Interactions between commensal intestinal bacteria and the immune system.
    Nat Rev Immunol. 2004 Jun;4(6):478-85 PMID: 15173836
  20. The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus.
    Nature. 2011 Sep 14;477(7366):596-600 PMID: 21918512
  21. Intestinal bacterial colonization induces mutualistic regulatory T cell responses.
    Immunity. 2011 May 27;34(5):794-806 PMID: 21596591
  22. The expanding family of innate lymphoid cells: regulators and effectors of immunity and tissue remodeling.
    Nat Immunol. 2011 Jan;12(1):21-7 PMID: 21113163
  23. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells.
    Science. 2006 Nov 17;314(5802):1157-60 PMID: 17110582
  24. Nod-like proteins in inflammation and disease.
    J Pathol. 2008 Jan;214(2):136-48 PMID: 18161746
  25. The interface between innate and adaptive immunity.
    Nat Immunol. 2004 Oct;5(10):971-4 PMID: 15454919
  26. Natural Treg cells spontaneously differentiate into pathogenic helper cells in lymphopenic conditions.
    Eur J Immunol. 2009 Apr;39(4):948-55 PMID: 19291701
  27. Concurrent murine cytomegalovirus and Klebsiella pneumoniae infections in germfree mice.
    Tokai J Exp Clin Med. 1990 Mar;15(1):87-92 PMID: 1965065
  28. The role of the intestinal microbiota in the development of atopic disorders.
    Allergy. 2007 Nov;62(11):1223-36 PMID: 17711557
  29. Impaired regulatory T cell function in germ-free mice.
    Eur J Immunol. 2006 Sep;36(9):2336-46 PMID: 16897813
  30. Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion.
    J Exp Med. 2006 Apr 17;203(4):1105-16 PMID: 16606668
  31. Toll-like receptor 2 and nucleotide-binding oligomerization domain-2 play divergent roles in the recognition of gut-derived lactobacilli and bifidobacteria in dendritic cells.
    Immunology. 2008 Aug;124(4):489-502 PMID: 18217947
  32. Toll-like receptor-2 expression is upregulated in antigen-presenting cells from patients with psoriatic arthritis: a pathogenic role for innate immunity?
    J Rheumatol. 2007 Feb;34(2):374-9 PMID: 17183618
  33. Innate lymphoid cells--a proposal for uniform nomenclature.
    Nat Rev Immunol. 2013 Feb;13(2):145-9 PMID: 23348417
  34. Differential activity of IL-12 and IL-23 in mucosal and systemic innate immune pathology.
    Immunity. 2006 Aug;25(2):309-18 PMID: 16919486
  35. Compartmentalized control of skin immunity by resident commensals.
    Science. 2012 Aug 31;337(6098):1115-9 PMID: 22837383
  36. IL-23 stimulates epidermal hyperplasia via TNF and IL-20R2-dependent mechanisms with implications for psoriasis pathogenesis.
    J Exp Med. 2006 Nov 27;203(12):2577-87 PMID: 17074928
  37. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection.
    Cell. 2006 Oct 20;127(2):423-33 PMID: 17055441
  38. Peripheral education of the immune system by colonic commensal microbiota.
    Nature. 2011 Sep 21;478(7368):250-4 PMID: 21937990
  39. Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses.
    Science. 2012 Sep 21;337(6101):1553-6 PMID: 22923434
  40. Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria.
    Nature. 2013 Jun 6;498(7452):113-7 PMID: 23698371
  41. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis.
    Nature. 2008 Nov 27;456(7221):507-10 PMID: 18987631
  42. MyD88-dependent signaling for IL-15 production plays an important role in maintenance of CD8 alpha alpha TCR alpha beta and TCR gamma delta intestinal intraepithelial lymphocytes.
    J Immunol. 2006 May 15;176(10):6180-5 PMID: 16670327
  43. Anti-CD3 therapy permits regulatory T cells to surmount T cell receptor-specified peripheral niche constraints.
    J Exp Med. 2010 Aug 30;207(9):1879-89 PMID: 20679403
  44. IL-12, but not IFN-gamma, plays a major role in sustaining the chronic phase of colitis in IL-10-deficient mice.
    J Immunol. 1998 Sep 15;161(6):3143-9 PMID: 9743382
  45. Influence of intestinal bacteria on induction of regulatory T cells: lessons from a transfer model of colitis.
    Gut. 2005 Nov;54(11):1546-52 PMID: 15987795
  46. Innate lymphoid cells: balancing immunity, inflammation, and tissue repair in the intestine.
    Cell Host Microbe. 2012 Oct 18;12(4):445-57 PMID: 23084914
  47. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis.
    Science. 2013 Aug 2;341(6145):569-73 PMID: 23828891
  48. 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
  49. NOD-like receptors: role in innate immunity and inflammatory disease.
    Annu Rev Pathol. 2009;4:365-98 PMID: 18928408
  50. Microbial colonization induces oligoclonal expansions of intraepithelial CD8 T cells in the gut.
    Eur J Immunol. 2004 Dec;34(12):3389-400 PMID: 15517613
  51. Responses of single germinal-center B cells in T-cell-dependent microculture.
    Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):11-5 PMID: 1824722
  52. Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement.
    J Exp Med. 2006 Dec 25;203(13):2841-52 PMID: 17145958
  53. Reconstituted NALP1 inflammasome reveals two-step mechanism of caspase-1 activation.
    Mol Cell. 2007 Mar 9;25(5):713-24 PMID: 17349957
  54. 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
  55. Local and systemic immune responses in murine Helicobacter felis active chronic gastritis.
    Infect Immun. 1993 Jun;61(6):2309-15 PMID: 8500873
  56. Microbiota-stimulated immune mechanisms to maintain gut homeostasis.
    Curr Opin Immunol. 2010 Aug;22(4):455-60 PMID: 20656465
  57. Freshly isolated Peyer's patch, but not spleen, dendritic cells produce interleukin 10 and induce the differentiation of T helper type 2 cells.
    J Exp Med. 1999 Jul 19;190(2):229-39 PMID: 10432286
  58. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus.
    Nat Immunol. 2011 Nov;12(11):1045-54 PMID: 21946417
  59. 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
  60. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance.
    Science. 2005 Jan 14;307(5707):254-8 PMID: 15653504
  61. Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity.
    Nature. 2011 Aug 28;477(7366):592-5 PMID: 21874021
  62. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation.
    Nature. 2013 Dec 19;504(7480):451-5 PMID: 24226773
  63. Isolation of naturally associated bacteria of necromenic Pristionchus nematodes and fitness consequences.
    J Exp Biol. 2008 Jun;211(Pt 12):1927-36 PMID: 18515723
  64. Small intestinal CD103+ dendritic cells display unique functional properties that are conserved between mice and humans.
    J Exp Med. 2008 Sep 1;205(9):2139-49 PMID: 18710932
  65. Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria.
    Science. 2012 Jun 8;336(6086):1321-5 PMID: 22674331
  66. Innate immunity and intestinal microbiota in the development of Type 1 diabetes.
    Nature. 2008 Oct 23;455(7216):1109-13 PMID: 18806780
  67. Mucosal dendritic cells.
    Annu Rev Immunol. 2007;25:381-418 PMID: 17378762
  68. Toll-like receptor 4 is required for optimal development of Th2 immune responses: role of dendritic cells.
    J Immunol. 2002 May 1;168(9):4524-30 PMID: 11970998
  69. Influences of microbiota on intestinal immune system development.
    Am J Clin Nutr. 1999 May;69(5):1046S-1051S PMID: 10232647
  70. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis.
    Science. 2014 Mar 28;343(6178):1249288 PMID: 24625929
  71. Dendritic cells in intestinal immune regulation.
    Nat Rev Immunol. 2008 Jun;8(6):435-46 PMID: 18500229
  72. NALP1 in vitiligo-associated multiple autoimmune disease.
    N Engl J Med. 2007 Mar 22;356(12):1216-25 PMID: 17377159
  73. IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo.
    Immunity. 2001 Dec;15(6):985-95 PMID: 11754819
  74. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation.
    J Exp Med. 2003 Dec 15;198(12):1951-7 PMID: 14662908
  75. Interleukin-23 drives innate and T cell-mediated intestinal inflammation.
    J Exp Med. 2006 Oct 30;203(11):2473-83 PMID: 17030949
  76. Expression of Helios in peripherally induced Foxp3+ regulatory T cells.
    J Immunol. 2012 Feb 1;188(3):976-80 PMID: 22198953
  77. Hyporesponsiveness of intestinal dendritic cells to TLR stimulation is limited to TLR4.
    J Immunol. 2009 Feb 15;182(4):2405-15 PMID: 19201895
  78. Nucleotide binding oligomerization domain 2 deficiency leads to dysregulated TLR2 signaling and induction of antigen-specific colitis.
    Immunity. 2006 Sep;25(3):473-85 PMID: 16949315
  79. Host-bacterial mutualism in the human intestine.
    Science. 2005 Mar 25;307(5717):1915-20 PMID: 15790844
  80. Cell biology of antigen processing in vitro and in vivo.
    Annu Rev Immunol. 2005;23:975-1028 PMID: 15771591
  81. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach.
    Gut. 2006 Feb;55(2):205-11 PMID: 16188921
  82. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis.
    Cell. 2011 May 27;145(5):745-57 PMID: 21565393
  83. Commensal bacteria calibrate the activation threshold of innate antiviral immunity.
    Immunity. 2012 Jul 27;37(1):158-70 PMID: 22705104
  84. Commensal gut flora drives the expansion of proinflammatory CD4 T cells in the colonic lamina propria under normal and inflammatory conditions.
    J Immunol. 2008 Jan 1;180(1):559-68 PMID: 18097058
  85. Innate lymphoid cells: emerging insights in development, lineage relationships, and function.
    Annu Rev Immunol. 2012;30:647-75 PMID: 22224763
  86. 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
  87. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria.
    Nat Immunol. 2001 Apr;2(4):361-7 PMID: 11276208
  88. IL-23 production by cosecretion of endogenous p19 and transgenic p40 in keratin 14/p40 transgenic mice: evidence for enhanced cutaneous immunity.
    J Immunol. 2003 Jun 1;170(11):5438-44 PMID: 12759419
  89. Intestinal bacteria and the regulation of immune cell homeostasis.
    Annu Rev Immunol. 2010;28:623-67 PMID: 20192812
  90. Reciprocal interactions between commensal bacteria and gamma delta intraepithelial lymphocytes during mucosal injury.
    J Immunol. 2009 Mar 1;182(5):3047-54 PMID: 19234201
  91. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells.
    Nature. 2003 Jul 3;424(6944):88-93 PMID: 12840763
  92. Microbial pattern recognition receptors mediate M-cell uptake of a gram-negative bacterium.
    Infect Immun. 2006 Jan;74(1):625-31 PMID: 16369019
  93. Immune regulation in the intestine: a balancing act between effector and regulatory T cell responses.
    Ann N Y Acad Sci. 2004 Dec;1029:132-41 PMID: 15681752
  94. CARD15/NOD2 functions as an antibacterial factor in human intestinal epithelial cells.
    Gastroenterology. 2003 Apr;124(4):993-1000 PMID: 12671896
  95. 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
  96. Induction of colonic regulatory T cells by indigenous Clostridium species.
    Science. 2011 Jan 21;331(6015):337-41 PMID: 21205640
  97. Control of intestinal inflammation by regulatory T cells.
    Immunol Rev. 2001 Aug;182:190-200 PMID: 11722634
  98. Neuropilin 1 is expressed on thymus-derived natural regulatory T cells, but not mucosa-generated induced Foxp3+ T reg cells.
    J Exp Med. 2012 Sep 24;209(10):1723-42, S1 PMID: 22966001
  99. Nalp1b controls mouse macrophage susceptibility to anthrax lethal toxin.
    Nat Genet. 2006 Feb;38(2):240-4 PMID: 16429160
  100. Pathogenesis of Listeria monocytogenes for gnotobiotic rats.
    Infect Immun. 1981 Apr;32(1):323-31 PMID: 6783550
  101. A requisite role for induced regulatory T cells in tolerance based on expanding antigen receptor diversity.
    Immunity. 2011 Jul 22;35(1):109-22 PMID: 21723159
  102. Interleukin-23 restrains regulatory T cell activity to drive T cell-dependent colitis.
    Immunity. 2008 Apr;28(4):559-70 PMID: 18400195
  103. Dominant-negative TLR5 polymorphism reduces adaptive immune response to flagellin and negatively associates with Crohn's disease.
    Am J Physiol Gastrointest Liver Physiol. 2006 Jun;290(6):G1157-63 PMID: 16439468
  104. Innate lymphoid cells in immunity and disease.
    Adv Exp Med Biol. 2013;785:9-26 PMID: 23456833
  105. Responses of the Peyer's Patches in Germ-Free Mice to Antigenic Stimulation.
    Infect Immun. 1970 Jul;2(1):96-100 PMID: 16557807
  106. Gut microbiota composition and development of atopic manifestations in infancy: the KOALA Birth Cohort Study.
    Gut. 2007 May;56(5):661-7 PMID: 17047098
  107. Obesity alters gut microbial ecology.
    Proc Natl Acad Sci U S A. 2005 Aug 2;102(31):11070-5 PMID: 16033867
  108. Mucosal immunity and inflammation. I. Mucosal dendritic cells: their specialized role in initiating T cell responses.
    Am J Physiol. 1999 May;276(5):G1074-8 PMID: 10329996
  109. Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses.
    Immunity. 2008 Oct 17;29(4):637-49 PMID: 18835196
  110. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis.
    Cell. 2004 Jul 23;118(2):229-41 PMID: 15260992
  111. Adaptive immunity in the host-microbiota dialog.
    Mucosal Immunol. 2011 Jan;4(1):15-21 PMID: 20944557
  112. IL-17 and Th17 Cells.
    Annu Rev Immunol. 2009;27:485-517 PMID: 19132915
  113. Tissue remodeling induced by hypersecreted epidermal growth factor and amphiregulin in the airway after an acute asthma attack.
    J Allergy Clin Immunol. 2009 Nov;124(5):913-20.e1-7 PMID: 19895983
  114. NOD2 transgenic mice exhibit enhanced MDP-mediated down-regulation of TLR2 responses and resistance to colitis induction.
    Gastroenterology. 2007 Nov;133(5):1510-21 PMID: 17915219
  115. IL-10-dependent partial refractoriness to Toll-like receptor stimulation modulates gut mucosal dendritic cell function.
    Eur J Immunol. 2008 Jun;38(6):1533-47 PMID: 18461564
  116. Increased susceptibility to primary infection with Listeria monocytogenes in germfree mice may be due to lack of accumulation of L-selectin+ CD44+ T cells in sites of inflammation.
    Infect Immun. 1996 Aug;64(8):3280-7 PMID: 8757865
  117. Preferential induction of polyclonal IgA secretion by murine Peyer's patch dendritic cell-T cell mixtures.
    J Exp Med. 1984 Sep 1;160(3):941-6 PMID: 6332171
  118. Decreased cellular immune response of germ-free mice.
    Acta Microbiol Acad Sci Hung. 1976;23(3):231-4 PMID: 1020696
  119. Recognition of microorganisms and activation of the immune response.
    Nature. 2007 Oct 18;449(7164):819-26 PMID: 17943118
  120. Gut flora antigens are not important in the maintenance of regulatory T cell heterogeneity and homeostasis.
    Eur J Immunol. 2007 Jul;37(7):1916-23 PMID: 17549737
  121. Experimental models of inflammatory bowel disease reveal innate, adaptive, and regulatory mechanisms of host dialogue with the microbiota.
    Immunol Rev. 2005 Aug;206:260-76 PMID: 16048554
  122. Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12- and IL-15-responsive IFN-γ-producing cells.
    Immunity. 2013 Apr 18;38(4):769-81 PMID: 23453631
  123. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity.
    Nature. 1997 Jul 24;388(6640):394-7 PMID: 9237759
  124. Cytolytic activity of intestinal intraepithelial lymphocytes in germ-free mice is strain dependent and determined by T cells expressing gamma delta T-cell antigen receptors.
    Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8591-4 PMID: 8378333
  125. NOD2 is a negative regulator of Toll-like receptor 2-mediated T helper type 1 responses.
    Nat Immunol. 2004 Aug;5(8):800-8 PMID: 15220916
  126. Commensals, probiotics and pathogens in the Caenorhabditis elegans model.
    Cell Microbiol. 2014 Jan;16(1):27-38 PMID: 24168639
  127. 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
  128. Differentiation and function of Th17 T cells.
    Curr Opin Immunol. 2007 Jun;19(3):281-6 PMID: 17433650
  129. Nod-like proteins in immunity, inflammation and disease.
    Nat Immunol. 2006 Dec;7(12):1250-7 PMID: 17110941
  130. Genetics and pathogenesis of inflammatory bowel disease.
    Nature. 2011 Jun 15;474(7351):307-17 PMID: 21677747
  131. OX-22high CD4+ T cells induce wasting disease with multiple organ pathology: prevention by the OX-22low subset.
    J Exp Med. 1990 Dec 1;172(6):1701-8 PMID: 2258700
  132. Intestinal floras of populations that have a high risk of colon cancer.
    Appl Environ Microbiol. 1995 Sep;61(9):3202-7 PMID: 7574628
  133. Intestinal dendritic cells increase T cell expression of alpha4beta7 integrin.
    Eur J Immunol. 2002 May;32(5):1445-54 PMID: 11981833
  134. Human intestinal microbiota and type 1 diabetes.
    Curr Diab Rep. 2013 Oct;13(5):601-7 PMID: 23934614
  135. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells.
    Nature. 2013 Dec 19;504(7480):446-50 PMID: 24226770
  136. The interleukin-23 axis in intestinal inflammation.
    Immunol Rev. 2008 Dec;226:147-59 PMID: 19161422
  137. The toll-like receptor signaling molecule Myd88 contributes to pancreatic beta-cell homeostasis in response to injury.
    PLoS One. 2009;4(4):e5063 PMID: 19357791
  138. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system.
    Cell. 2005 Jul 15;122(1):107-18 PMID: 16009137
  139. Intestinal homeostasis and its breakdown in inflammatory bowel disease.
    Nature. 2011 Jun 15;474(7351):298-306 PMID: 21677746
  140. Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing Toll-like receptors.
    J Immunol. 2000 Jan 15;164(2):966-72 PMID: 10623846
  141. CARD15/NOD2 is required for Peyer's patches homeostasis in mice.
    PLoS One. 2007 Jun 13;2(6):e523 PMID: 17565376
  142. Induction of intestinal Th17 cells by segmented filamentous bacteria.
    Cell. 2009 Oct 30;139(3):485-98 PMID: 19836068
  143. CCR7 is critically important for migration of dendritic cells in intestinal lamina propria to mesenteric lymph nodes.
    J Immunol. 2006 Jan 15;176(2):803-10 PMID: 16393963
  144. Proliferative recruitment of intestinal intraepithelial lymphocytes after microbial colonization of germ-free mice.
    Eur J Immunol. 1996 Apr;26(4):945-8 PMID: 8625993
  145. Intestinal intraepithelial lymphocyte gamma delta-T cell-derived keratinocyte growth factor modulates epithelial growth in the mouse.
    J Immunol. 2004 Apr 1;172(7):4151-8 PMID: 15034027
  146. Metagenomic analysis of the human distal gut microbiome.
    Science. 2006 Jun 2;312(5778):1355-9 PMID: 16741115
  147. Functional specialization of gut CD103+ dendritic cells in the regulation of tissue-selective T cell homing.
    J Exp Med. 2005 Oct 17;202(8):1063-73 PMID: 16216890
  148. Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota.
    Cell Host Microbe. 2007 Dec 13;2(6):371-82 PMID: 18078689
  149. Antibodies to interleukin 12 abrogate established experimental colitis in mice.
    J Exp Med. 1995 Nov 1;182(5):1281-90 PMID: 7595199
  150. Prokaryotes: the unseen majority.
    Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):6578-83 PMID: 9618454
  151. Development and cytolytic function of intestinal intraepithelial T lymphocytes in antigen-minimized mice.
    Immunology. 1996 Oct;89(2):268-73 PMID: 8943725
Article Info
Journal
Frontiers in immunology
Abbr.
Front Immunol
ISSN
1664-3224
Published
2014-00-00
Epub
2014-00-28
Pages
318
Language
English
Region
Switzerland
NLM ID
101560960
PMCID
PMC4112811
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