Autoimmune host-microbiota interactions at barrier sites and beyond

Trends in Molecular Medicine

Volumn 21, Issue 4, 2015, Pages 233-244

  Ruff, William E ^a   Kriegel, Martin A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bystander activation; Commensal; Crossreactivity; Epitope spread; Microbiome; Molecular mimicry

Indexed keywords

IMMUNOGLOBULIN A; SHORT CHAIN FATTY ACID;

ADAPTIVE IMMUNITY; AUTOIMMUNE DISEASE; AUTOIMMUNITY; B LYMPHOCYTE; BACTEROIDES FRAGILIS; CLOSTRIDIUM; COMMENSAL; DYSBIOSIS; ENVIRONMENT; GENETICS; HOMEOSTASIS; HOST; HOST MICROBIOTA INTERACTION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY BOWEL DISEASE; INTESTINE; INTESTINE FLORA; MICROBIAL COMMUNITY; MICROBIOME; MICROFLORA; MOLECULAR MIMICRY; NONHUMAN; ORGANISMAL INTERACTION; REVIEW; T LYMPHOCYTE; ANIMAL; DISEASE MODEL; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MICROBIOLOGY;

ANIMALIA;

ADAPTIVE IMMUNITY; ANIMALS; AUTOIMMUNE DISEASES; AUTOIMMUNITY; DISEASE MODELS, ANIMAL; HOMEOSTASIS; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLAMMATORY BOWEL DISEASES; INTESTINES; MICROBIOTA;

EID: 84925708633     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2015.02.006     Document Type: Review

References (134)

1. Belkaid Y., Naik S. Compartmentalized and systemic control of tissue immunity by commensals. Nat. Immunol. 2013, 14:646-653.
2. Brestoff J.R., Artis D. Commensal bacteria at the interface of host metabolism and the immune system. Nat. Immunol. 2013, 14:676-684.
3. Sommer F., Backhed F. The gut microbiota - masters of host development and physiology. Nat. Rev. Microbiol. 2013, 11:227-238.
4. Maynard C.L., et al. Reciprocal interactions of the intestinal microbiota and immune system. Nature 2012, 489:231-241.
5. Belkaid Y., Hand T.W. Role of the microbiota in immunity and inflammation. Cell 2014, 157:121-141.
6. Cho I., Blaser M.J. The human microbiome: at the interface of health and disease. Nat. Rev. Genet. 2012, 13:260-270.
7. Ochoa-Reparaz J., et al. Role of gut commensal microflora in the development of experimental autoimmune encephalomyelitis. J. Immunol. 2009, 183:6041-6050.
8. Berer K., et al. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature 2011, 479:538-541.
9. Lee Y.K., et al. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. U.S.A. 2011, 108(Suppl 1):4615-4622.
10. Rath H.C., et al. Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats. J. Clin. Invest. 1996, 98:945-953.
11. Abdollahi-Roodsaz S., et al. Stimulation of TLR2 and TLR4 differentially skews the balance of T cells in a mouse model of arthritis. J. Clin. Invest. 2008, 118:205-216.
12. Wu H.J., et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 2010, 32:815-827.
13. Scher J.U., et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife 2013, 2:e01202.
14. Pozzilli P., et al. NOD mouse colonies around the world - recent facts and figures. Immunol. Today 1993, 14:193-196.
15. Wen L., et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 2008, 455:1109-1113.
16. Kriegel M.A., et al. Naturally transmitted segmented filamentous bacteria segregate with diabetes protection in nonobese diabetic mice. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:11548-11553.
17. Markle J.G., et al. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 2013, 339:1084-1088.
18. Yurkovetskiy L., et al. Gender bias in autoimmunity is influenced by microbiota. Immunity 2013, 39:400-412.
19. Sudo N., et al. The requirement of intestinal bacterial flora for the development of an IgE production system fully susceptible to oral tolerance induction. J. Immunol. 1997, 159:1739-1745.
20. von Mutius E., Vercelli D. Farm living: effects on childhood asthma and allergy. Nat. Rev. Immunol. 2010, 10:861-868.
21. Olszak T., et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 2012, 336:489-493.
22. Cahenzli J., et al. Intestinal microbial diversity during early-life colonization shapes long-term IgE levels. Cell Host Microbe 2013, 14:559-570.
23. Garrett W.S., et al. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe 2010, 8:292-300.
24. Palm N.W., et al. Immunoglobulin a coating identifies colitogenic bacteria in inflammatory bowel disease. Cell 2014, 158:1000-1010.
25. Kostic A.D., et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 2013, 14:207-215.
26. Rubinstein M.R., et al. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/beta-catenin signaling via its FadA adhesin. Cell Host Microbe 2013, 14:195-206.
27. Vieira S.M., et al. Diet, microbiota and autoimmune diseases. Lupus 2014, 23:518-526.
28. Cho J.H., Gregersen P.K. Genomics and the multifactorial nature of human autoimmune disease. N. Engl. J. Med. 2011, 365:1612-1623.
29. Cotsapas C., Hafler D.A. Immune-mediated disease genetics: the shared basis of pathogenesis. Trends Immunol. 2013, 34:22-26.
30. Selmi C., et al. Heritability versus the role of the environment in autoimmunity. J. Autoimmun. 2012, 39:249-252.
31. Tiniakou E., et al. Sex-specific environmental influences on the development of autoimmune diseases. Clin. Immunol. 2013, 149:182-191.
32. Turnbaugh P.J., et al. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med. 2009, 1:6ra14.
33. Cox L.M., et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell 2014, 158:705-721.
34. Atarashi K., et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011, 331:337-341.
35. Cha H.R., et al. Downregulation of Th17 cells in the small intestine by disruption of gut flora in the absence of retinoic acid. J. Immunol. 2010, 184:6799-6806.
36. Smith P.M., et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013, 341:569-573.
37. Maslowski K.M., et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 2009, 461:1282-1286.
38. Rakoff-Nahoum S., et al. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004, 118:229-241.
39. Sansonetti P.J., Medzhitov R. Learning tolerance while fighting ignorance. Cell 2009, 138:416-420.
40. Gevers D., et al. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe 2014, 15:382-392.
41. Manichanh C., et al. The gut microbiota in IBD. Nat. Rev. Gastroenterol. Hepatol. 2012, 9:599-608.
42. Huttenhower C., et al. Inflammatory bowel disease as a model for translating the microbiome. Immunity 2014, 40:843-854.
43. + T cells with a naive phenotype in the periphery. Dev. Immunol. 1992, 2:141-150.
44. Strachan D.P. Hay fever, hygiene, and household size. BMJ 1989, 299:1259-1260.
45. Mazmanian S.K., et al. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 2005, 122:107-118.
46. + regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:12204-12209.
47. Wang Y., et al. An intestinal commensal symbiosis factor controls neuroinflammation via TLR2-mediated CD39 signalling. Nat. Commun. 2014, 5:4432.
48. Dasgupta S., et al. Plasmacytoid dendritic cells mediate anti-inflammatory responses to a gut commensal molecule via both innate and adaptive mechanisms. Cell Host Microbe 2014, 15:413-423.
49. Antonioli L., et al. CD39 and CD73 in immunity and inflammation. Trends Mol. Med. 2013, 19:355-367.
50. Sears C.L., et al. Bacteroides fragilis subverts mucosal biology: from symbiont to colon carcinogenesis. J. Clin. Invest. 2014, 124:4166-4172.
51. Hsiao E.Y., et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 2013, 155:1451-1463.
52. Atarashi K., et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 2013, 500:232-236.
53. Narushima S., et al. Characterization of the 17 strains of regulatory T cell-inducing human-derived Clostridia. Gut Microbes 2014, 5:333-339.
54. Furusawa Y., et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 2013, 504:446-450.
55. Arpaia N., et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013, 504:451-455.
56. Chang P.V., et al. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:2247-2252.
57. Kim S.V., et al. GPR15-mediated homing controls immune homeostasis in the large intestine mucosa. Science 2013, 340:1456-1459.
58. Kim M.H., et al. Short-chain fatty acids activate GPR41 and GPR43 on intestinal epithelial cells to promote inflammatory responses in mice. Gastroenterology 2013, 145:396-406.
59. Singh N., et al. Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity 2014, 40:128-139.
60. Obata Y., et al. The epigenetic regulator Uhrf1 facilitates the proliferation and maturation of colonic regulatory T cells. Nat. Immunol. 2014, 15:571-579.
61. Lopetuso L.R., et al. Commensal Clostridium: leading players in the maintenance of gut homeostasis. Gut Pathog. 2013, 5:23.
62. Gomez A., et al. Loss of sex and age driven differences in the gut microbiome characterize arthritis-susceptible 0401 mice but not arthritis-resistant 0402 mice. PLoS ONE 2012, 7:e36095.
63. Loo V.G., et al. Host and pathogen factors for Clostridium difficile infection and colonization. N. Engl. J. Med. 2011, 365:1693-1703.
64. Ivanov I.I., et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009, 139:485-498.
65. Berer K., et al. Selective accumulation of pro-inflammatory T cells in the intestine contributes to the resistance to autoimmune demyelinating disease. PLoS ONE 2014, 9:e87876.
66. Chung H., et al. Gut immune maturation depends on colonization with a host-specific microbiota. Cell 2012, 149:1578-1593.
67. Yin Y., et al. Comparative analysis of the distribution of segmented filamentous bacteria in humans, mice and chickens. ISME J. 2013, 7:615-621.
68. Obata T., et al. Indigenous opportunistic bacteria inhabit mammalian gut-associated lymphoid tissues and share a mucosal antibody-mediated symbiosis. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:7419-7424.
69. Reading N.C., Kasper D.L. The starting lineup: key microbial players in intestinal immunity and homeostasis. Front. Microbiol. 2011, 2:148.
70. Kunisawa J., Kiyono H. Alcaligenes is commensal bacteria habituating in the gut-associated lymphoid tissue for the regulation of intestinal IgA responses. Front. Immunol. 2012, 3:65.
71. Suzuki K., et al. Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:1981-1986.
72. Fagarasan S., et al. Adaptive immune regulation in the gut: T cell-dependent and T cell-independent IgA synthesis. Annu. Rev. Immunol. 2010, 28:243-273.
73. Craft J.E. Follicular helper T cells in immunity and systemic autoimmunity. Nat. Rev. Rheumatol. 2012, 8:337-347.
74. Kato L.M., et al. The role of the adaptive immune system in regulation of gut microbiota. Immunol. Rev. 2014, 260:67-75.
75. Kawamoto S., et al. The inhibitory receptor PD-1 regulates IgA selection and bacterial composition in the gut. Science 2012, 336:485-489.
76. Wang N., et al. Selective IgA deficiency in autoimmune diseases. Mol. Med. 2011, 17:1383-1396.
77. + T cells regulate immunoglobulin a selection and facilitate diversification of bacterial species responsible for immune homeostasis. Immunity 2014, 41:152-165.
78. Hirota K., et al. Plasticity of Th17 cells in Peyer's patches is responsible for the induction of T cell-dependent IgA responses. Nat. Immunol. 2013, 14:372-379.
79. Trama A.M., et al. HIV-1 Envelope gp41 antibodies can originate from terminal ileum B cells that share cross-reactivity with commensal bacteria. Cell Host Microbe 2014, 16:215-226.
80. Hunger R.E., et al. Male gonadal environment paradoxically promotes dacryoadenitis in nonobese diabetic mice. J. Clin. Invest. 1998, 101:1300-1309.
81. Nicholson J.K., et al. Host-gut microbiota metabolic interactions. Science 2012, 336:1262-1267.
82. Haiser H.J., et al. Predicting and manipulating cardiac drug inactivation by the human gut bacterium Eggerthella lenta. Science 2013, 341:295-298.
83. Norman J.M., et al. Kingdom-agnostic metagenomics and the importance of complete characterization of enteric microbial communities. Gastroenterology 2014, 146:1459-1469.
84. Stetson D.B., et al. Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 2008, 134:587-598.
85. Weinstock J.V., Elliott D.E. Helminth infections decrease host susceptibility to immune-mediated diseases. J. Immunol. 2014, 193:3239-3247.
86. Hand T.W., et al. Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses. Science 2012, 337:1553-1556.
87. Yang Y., et al. Focused specificity of intestinal TH17 cells towards commensal bacterial antigens. Nature 2014, 510:152-156.
88. Goto Y., et al. Segmented filamentous bacteria antigens presented by intestinal dendritic cells drive mucosal Th17 cell differentiation. Immunity 2014, 40:594-607.
89. Kuhn K.A., Stappenbeck T.S. Peripheral education of the immune system by the colonic microbiota. Semin. Immunol. 2013, 25:364-369.
90. Cong Y., et al. A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:19256-19261.
91. Alexander K.L., et al. Microbiota activation and regulation of innate and adaptive immunity. Immunol. Rev. 2014, 260:206-220.
92. Lathrop S.K., et al. Peripheral education of the immune system by colonic commensal microbiota. Nature 2011, 478:250-254.
93. Cebula A., et al. Thymus-derived regulatory T cells contribute to tolerance to commensal microbiota. Nature 2013, 497:258-262.
94. Faith J.J., et al. Identifying gut microbe-host phenotype relationships using combinatorial communities in gnotobiotic mice. Sci. Transl. Med. 2014, 6:220ra211.
95. Ahern P.P., et al. Mining the human gut microbiota for effector strains that shape the immune system. Immunity 2014, 40:815-823.
96. Smith K., et al. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin. Immunol. 2007, 19:59-69.
97. Konrad A., et al. Tight mucosal compartmentation of the murine immune response to antigens of the enteric microbiota. Gastroenterology 2006, 130:2050-2059.
98. Munz C., et al. Antiviral immune responses: triggers of or triggered by autoimmunity?. Nat. Rev. Immunol. 2009, 9:246-258.
99. Horwitz M.S., et al. Diabetes induced by Coxsackie virus: initiation by bystander damage and not molecular mimicry. Nat. Med. 1998, 4:781-785.
100. Miller S.D., et al. Persistent infection with Theiler's virus leads to CNS autoimmunity via epitope spreading. Nat. Med. 1997, 3:1133-1136.
101. Oldstone M.B. Molecular mimicry, microbial infection, and autoimmune disease: evolution of the concept. Curr. Top. Microbiol. Immunol. 2005, 296:1-17.
102. Fae K.C., et al. Mimicry in recognition of cardiac myosin peptides by heart-intralesional T cell clones from rheumatic heart disease. J. Immunol. 2006, 176:5662-5670.
103. Ang C.W., et al. The Guillain-Barre syndrome: a true case of molecular mimicry. Trends Immunol. 2004, 25:61-66.
104. Ley R.E., et al. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 2006, 124:837-848.
105. Li J., Jia H. An integrated catalog of reference genes in the human gut microbiome. Nat. Biotechnol. 2014, 32:834-841.
106. + memory-phenotype T cells are abundant in unexposed adults. Immunity 2013, 38:373-383.
107. Nylander A., Hafler D.A. Multiple sclerosis. J. Clin. Invest. 2012, 122:1180-1188.
108. + plasmablasts in the human gut are antigen-specific. J. Clin. Invest. 2011, 121:1946-1955.
109. + memory B cells. Immunity 2007, 26:205-213.
110. Wardemann H., et al. Predominant autoantibody production by early human B cell precursors. Science 2003, 301:1374-1377.
111. Menard L., et al. The PTPN22 allele encoding an R620W variant interferes with the removal of developing autoreactive B cells in humans. J. Clin. Invest. 2011, 121:3635-3644.
112. Samuels J., et al. Impaired early B cell tolerance in patients with rheumatoid arthritis. J. Exp. Med. 2005, 201:1659-1667.
113. Kinnunen T., et al. Specific peripheral B cell tolerance defects in patients with multiple sclerosis. J. Clin. Invest. 2013, 123:2737-2741.
114. Wesemann D.R., et al. Microbial colonization influences early B-lineage development in the gut lamina propria. Nature 2013, 501:112-115.
115. Birnbaum M.E., et al. Deconstructing the peptide-MHC specificity of T cell recognition. Cell 2014, 157:1073-1087.
116. Alekseyenko A.V., et al. Community differentiation of the cutaneous microbiota in psoriasis. Microbiome 2013, 1:31.
117. Dickson R.P., et al. The role of the microbiome in exacerbations of chronic lung diseases. Lancet 2014, 384:691-702.
118. Sonnenburg J.L., Fischbach M.A. Community health care: therapeutic opportunities in the human microbiome. Sci. Transl. Med. 2011, 3:78ps12.
119. Husebye E.S., Anderson M.S. Autoimmune polyendocrine syndromes: clues to type 1 diabetes pathogenesis. Immunity 2010, 32:479-487.
120. Hafler D.A., et al. Risk alleles for multiple sclerosis identified by a genomewide study. N. Engl. J. Med. 2007, 357:851-862.
121. Sawcer S., et al. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 2011, 476:214-219.
122. Ubeda C., et al. Familial transmission rather than defective innate immunity shapes the distinct intestinal microbiota of TLR-deficient mice. J. Exp. Med. 2012, 209:1445-1456.
123. Adrianto I., et al. Association of a functional variant downstream of TNFAIP3 with systemic lupus erythematosus. Nat. Genet. 2011, 43:253-258.
124. Farh K.K., et al. Genetic and epigenetic fine mapping of causal autoimmune disease variants. Nature 2015, 518:337-343.
125. Topol E.J. Individualized medicine from prewomb to tomb. Cell 2014, 157:241-253.
126. Faith J.J., et al. The long-term stability of the human gut microbiota. Science 2013, 341:1237439.
127. Ding T., Schloss P.D. Dynamics and associations of microbial community types across the human body. Nature 2014, 509:357-360.
128. Qin J., et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010, 464:59-65.
129. Garrett W.S., et al. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell 2007, 131:33-45.
130. Rooks M.G., et al. Gut microbiome composition and function in experimental colitis during active disease and treatment-induced remission. ISME J. 2014, 8:1403-1417.
131. Winter S.E., et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 2010, 467:426-429.
132. Winter S.E., et al. The dynamics of gut-associated microbial communities during inflammation. EMBO Rep. 2013, 14:319-327.
133. H17 cell differentiation. Nature 2008, 455:808-812.
134. + innate lymphoid cells. Immunity 2012, 37:674-684.