Regulation of inflammation by microbiota interactions with the host

Nature Immunology

Volumn 18, Issue 8, 2017, Pages 851-860

  Blander, J Magarian ^a   Longman, Randy S ^a   Iliev, Iliyan D ^a   Sonnenberg, Gregory F ^a   Artis, David ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN PRESENTING CELL; AUTOIMMUNE DISEASE; DEGENERATIVE DISEASE; DISEASE PREDISPOSITION; FUNGUS; HOST PATHOGEN INTERACTION; INFECTION; INFLAMMATION; INTESTINE FLORA; LYMPHOID CELL; MALIGNANT NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTOZOON; REGULATORY T LYMPHOCYTE; REVIEW; SYMBIOSIS; VACCINATION; VIRUS; WORM; ADAPTIVE IMMUNITY; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; LYMPHOCYTE; MUCOSAL IMMUNITY; NEOPLASM;

ADAPTIVE IMMUNITY; ANTIGEN-PRESENTING CELLS; AUTOIMMUNE DISEASES; GASTROINTESTINAL MICROBIOME; HUMANS; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; INFECTION; INFLAMMATION; LYMPHOCYTES; NEOPLASMS; NEURODEGENERATIVE DISEASES; SYMBIOSIS; T-LYMPHOCYTES, REGULATORY; VACCINATION;

EID: 85025806668     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3780     Document Type: Review

References (133)

1. Sender, R., Fuchs, S. &Milo, R. Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. Cell 164, 337-340 (2016).
2. Gilbert, J.A. et al. Microbiome-wide association studies link dynamic microbial consortia to disease. Nature 535, 94-103 (2016).
3. Honda, K. &Littman, D.R. The microbiota in adaptive immune homeostasis and disease. Nature 535, 75-84 (2016).
4. Sonnenburg, J.L. &Bäckhed, F. Diet-microbiota interactions as moderators of human metabolism. Nature 535, 56-64 (2016).
5. Bittinger, K. et al. Improved characterization of medically relevant fungi in the human respiratory tract using next-generation sequencing. Genome Biol. 15, 487 (2014).
6. Iliev, I.D. et al. Interactions between commensal fungi and the C-type lectin receptor dectin-1 influence colitis. Science 336, 1314-1317 (2012).
7. Iliev, I.D. &Leonardi, I. Fungal dysbiosis: immunity and interactions at mucosal barriers. Nat. Rev. Immunol. http://dx.doi.org/10.1038/nri.2017.55 (2017).
8. Qin, J. et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59-65 (2010).
9. Human Microbiome Project Consortium. A framework for human microbiome research. Nature 486, 215-221 (2012).
10. Browne, H.P. et al. Culturing of 'unculturable' human microbiota reveals novel taxa and extensive sporulation. Nature 533, 543-546 (2016).
11. Schloss, P.D., Iverson, K.D., Petrosino, J.F. &Schloss, S.J. The dynamics of a family's gut microbiota reveal variations on a theme. Microbiome 2, 25 (2014).
12. Yissachar, N. et al. An intestinal organ culture system uncovers a role for the nervous system in microbe-immune crosstalk. Cell 168, 1135-1148.e12 (2017).
13. Longman, R.S. &Littman, D.R. The functional impact of the intestinal microbiome on mucosal immunity and systemic autoimmunity. Curr. Opin. Rheumatol. 27, 381-387 (2015).
14. Roy, S. &Trinchieri, G. Microbiota: a key orchestrator of cancer therapy. Nat. Rev. Cancer 17, 271-285 (2017).
15. Smith, P.A. The tantalizing links between gut microbes and the brain. Nature 526, 312-314 (2015).
16. Hooper, L.V., Littman, D.R. &Macpherson, A.J. Interactions between the microbiota and the immune system. Science 336, 1268-1273 (2012).
17. Peterson, L.W. &Artis, D. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat. Rev. Immunol. 14, 141-153 (2014).
18. Blander, J.M. Death in the intestinal epithelium-basic biology and implications for inflammatory bowel disease. FEBS J. 283, 2720-2730 (2016).
19. Cummings, R.J. et al. Different tissue phagocytes sample apoptotic cells to direct distinct homeostasis programs. Nature 539, 565-569 (2016).
20. Donaldson, G.P., Lee, S.M. &Mazmanian, S.K. Gut biogeography of the bacterial microbiota. Nat. Rev. Microbiol. 14, 20-32 (2016).
21. Chu, H. et al. Gene-microbiota interactions contribute to the pathogenesis of inflammatory bowel disease. Science 352, 1116-1120 (2016).
22. Bunker, J.J. et al. Innate and adaptive humoral responses coat distinct commensal bacteria with immunoglobulin A. Immunity 43, 541-553 (2015).
23. Leone, V. et al. Effects of diurnal variation of gut microbes and high-fat feeding on host circadian clock function and metabolism. Cell Host Microbe 17, 681-689 (2015).
24. Thaiss, C.A. et al. Microbiota diurnal rhythmicity programs host transcriptome oscillations. Cell 167, 1495-1510.e12 (2016).
25. Thaiss, C.A., Zeevi, D., Levy, M., Segal, E. &Elinav, E. A day in the life of the meta-organism: diurnal rhythms of the intestinal microbiome and its host. Gut Microbes 6, 137-142 (2015).
26. Kau, A.L. et al. Functional characterization of IgA-targeted bacterial taxa from undernourished Malawian children that produce diet-dependent enteropathy. Sci. Transl. Med. 7, 276ra24 (2015)
27. Palm, N.W. et al. Immunoglobulin A coating identifies colitogenic bacteria in inflammatory bowel disease. Cell 158, 1000-1010 (2014).
28. Planer, J.D. et al. Development of the gut microbiota and mucosal IgA responses in twins and gnotobiotic mice. Nature 534, 263-266 (2016).
29. Moor, K. et al. High-avidity IgA protects the intestine by enchaining growing bacteria. Nature 544, 498-502 (2017).
30. Geva-Zatorsky, N. et al. Mining the human gut microbiota for immunomodulatory organisms. Cell 168, 928-943.e911 (2017).
31. Viladomiu, M. et al. IgA-coated E. coli enriched in Crohn's disease spondyloarthritis promote TH17-dependent inflammation. Sci. Transl. Med. 9, eaaf9655 (2017).
32. Tan, T.G. et al. Identifying species of symbiont bacteria from the human gut that, alone, can induce intestinal Th17 cells in mice. Proc. Natl. Acad. Sci. USA 113, E8141-E8150 (2016).
33. Atarashi, K. et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500, 232-236 (2013).
34. Fung, T.C. et al. Lymphoid-tissue-resident commensal bacteria promote members of the IL-10 cytokine family to establish mutualism. Immunity 44, 634-646 (2016).
35. Kunisawa, J. &Kiyono, H. Alcaligenes is commensal bacteria habituating in the gut-associated lymphoid tissue for the regulation of intestinal IgA responses. Front. Immunol. 3, 65 (2012).
36. Obata, T. et al. Indigenous opportunistic bacteria inhabit mammalian gut-associated lymphoid tissues and share a mucosal antibody-mediated symbiosis. Proc. Natl. Acad. Sci. USA 107, 7419-7424 (2010).
37. Sonnenberg, G.F. &Artis, D. Innate lymphoid cells in the initiation, regulation and resolution of inflammation. Nat. Med. 21, 698-708 (2015).
38. Sato, S. et al. Transcription factor Spi-B-dependent and-independent pathways for the development of Peyer's patch M cells. Mucosal Immunol. 6, 838-846 (2013).
39. Satoh-Takayama, N. et al. The chemokine receptor CXCR6 controls the functional topography of interleukin-22 producing intestinal innate lymphoid cells. Immunity 41, 776-788 (2014).
40. Stockinger, B., Di Meglio, P., Gialitakis, M. &Duarte, J.H. The aryl hydrocarbon receptor: multitasking in the immune system. Annu. Rev. Immunol. 32, 403-432 (2014).
41. Lindemans, C.A. et al. Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature 528, 560-564 (2015).
42. Hallen-Adams, H.E. &Suhr, M.J. Fungi in the healthy human gastrointestinal tract. Virulence 8, 352-358 (2016).
43. Liguori, G. et al. Fungal dysbiosis in mucosa-associated microbiota of Crohn's disease patients. J. Crohns Colitis 10, 296-305 (2016).
44. Suhr, M.J., Banjara, N. &Hallen-Adams, H.E. Sequence-based methods for detecting and evaluating the human gut mycobiome. Lett. Appl. Microbiol. 62, 209-215 (2016).
45. Hoarau, G. et al. Bacteriome and mycobiome interactions underscore microbial dysbiosis in familial Crohn's disease. MBio 7, e01250-16 (2016).
46. Li, Q. et al. Dysbiosis of gut fungal microbiota is associated with mucosal inflammation in Crohn's disease. J. Clin. Gastroenterol. 48, 513-523 (2014).
47. Sokol, H. et al. Fungal microbiota dysbiosis in IBD. Gut 66, 1039-1048 (2016).
48. Lamas, B. et al. CARD9 impacts colitis by altering gut microbiota metabolism of tryptophan into aryl hydrocarbon receptor ligands. Nat. Med. 22, 598-605 (2016).
49. Tang, C. et al. Inhibition of Dectin-1 signaling ameliorates colitis by inducing Lactobacillus-mediated regulatory T cell expansion in the intestine. Cell Host Microbe 18, 183-197 (2015).
50. Lewis, J.D. et al. Inflammation, antibiotics, and diet as environmental stressors of the gut microbiome in pediatric Crohn's disease. Cell Host Microbe 18, 489-500 (2015).
51. Wheeler, M.L. et al. Immunological consequences of intestinal fungal dysbiosis. Cell Host Microbe 19, 865-873 (2016).
52. Fan, D. et al. Activation of HIF-1α and LL-37 by commensal bacteria inhibits Candida albicans colonization. Nat. Med. 21, 808-814 (2015).
53. Chudnovskiy, A. et al. Host-protozoan interactions protect from mucosal infections through activation of the inflammasome. Cell 167, 444-456.e14 (2016).
54. Escalante, N.K. et al. The common mouse protozoa Tritrichomonas muris alters mucosal T cell homeostasis and colitis susceptibility. J. Exp. Med. 213, 2841-2850 (2016).
55. Kernbauer, E., Ding, Y. &Cadwell, K. An enteric virus can replace the beneficial function of commensal bacteria. Nature 516, 94-98 (2014).
56. Kuss, S.K. et al. Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science 334, 249-252 (2011).
57. Kane, M. et al. Successful transmission of a retrovirus depends on the commensal microbiota. Science 334, 245-249 (2011).
58. Monaco, C.L. et al. Altered virome and bacterial microbiome in human immunodeficiency virus-associated acquired immunodeficiency syndrome. Cell Host Microbe 19, 311-322 (2016).
59. Norman, J.M. et al. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 160, 447-460 (2015).
60. Handley, S.A. et al. Pathogenic simian immunodeficiency virus infection is associated with expansion of the enteric virome. Cell 151, 253-266 (2012).
61. Ramanan, D. et al. Helminth infection promotes colonization resistance via type 2 immunity. Science 352, 608-612 (2016).
62. Osborne, L.C. et al. Coinfection. Virus-helminth coinfection reveals a microbiota-independent mechanism of immunomodulation. Science 345, 578-582 (2014).
63. Reese, T.A. et al. Helminth infection reactivates latent γ-herpesvirus via cytokine competition at a viral promoter. Science 345, 573-577 (2014).
64. Wu, G.D. et al. Comparative metabolomics in vegans and omnivores reveal constraints on diet-dependent gut microbiota metabolite production. Gut 65, 63-72 (2016).
65. Desai, M.S. et al. A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell 167, 1339-1353.e21 (2016).
66. Corrêa-Oliveira, R., Fachi, J.L., Vieira, A., Sato, F.T. &Vinolo, M.A. Regulation of immune cell function by short-chain fatty acids. Clin. Transl. Immunology 5, e73 (2016).
67. Kaiko, G.E. et al. The colonic crypt protects stem cells from microbiota-derived metabolites. Cell 165, 1708-1720 (2016).
68. Kelly, C.J. et al. Crosstalk between microbiota-derived short-chain fatty acids and intestinal epithelial HIF augments tissue barrier function. Cell Host Microbe 17, 662-671 (2015).
69. Kibe, R. et al. Upregulation of colonic luminal polyamines produced by intestinal microbiota delays senescence in mice. Sci. Rep. 4, 4548 (2014).
70. Levy, M. et al. Microbiota-modulated metabolites shape the intestinal microenvironment by regulating NLRP6 inflammasome signaling. Cell 163, 1428-1443 (2015).
71. Zelante, T. et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 39, 372-385 (2013).
72. Schiering, C. et al. Feedback control of AHR signalling regulates intestinal immunity. Nature 542, 242-245 (2017).
73. Zhu, W. et al. Gut microbial metabolite TMAO enhances platelet hyperreactivity and thrombosis risk. Cell 165, 111-124 (2016).
74. Wang, Z. et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472, 57-63 (2011).
75. Koeth, R.A. et al. Intestinal microbiota metabolism of l-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat. Med. 19, 576-585 (2013).
76. Dumas, M.E. et al. Metabolic profiling reveals a contribution of gut microbiota to fatty liver phenotype in insulin-resistant mice. Proc. Natl. Acad. Sci. USA 103, 12511-12516 (2006).
77. Levin, B.J. et al. A prominent glycyl radical enzyme in human gut microbiomes metabolizes trans-4-hydroxy-l-proline. Science 355, eaai8386 (2017).
78. Donia, M.S. et al. A systematic analysis of biosynthetic gene clusters in the human microbiome reveals a common family of antibiotics. Cell 158, 1402-1414 (2014).
79. Guo, C.J. et al. Discovery of reactive microbiota-derived metabolites that inhibit host proteases. Cell 168, 517-526.e18 (2017).
80. Manoury, B. Proteases: essential actors in processing antigens and intracellular toll-like receptors. Front. Immunol. 4, 299 (2013).
81. Kim, Y.G. et al. Gut dysbiosis promotes M2 macrophage polarization and allergic airway inflammation via fungi-induced PGE2. Cell Host Microbe 15, 95-102 (2014).
82. Vatanen, T. et al. Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans. Cell 165, 842-853 (2016)
83. Bach, J.F. &Chatenoud, L. The hygiene hypothesis: an explanation for the increased frequency of insulin-dependent diabetes. Cold Spring Harb. Perspect. Med. 2, a007799 (2012).
84. von Mutius, E. &Vercelli, D. Farm living: effects on childhood asthma and allergy. Nat. Rev. Immunol. 10, 861-868 (2010).
85. Calderon-Gomez, E. et al. Commensal-specific CD4+ cells from patients with Crohn′s disease have a T-helper 17 inflammatory profile. Gastroenterology 151, 489-500 e3 (2016).
86. Campisi, L. et al. Apoptosis in response to microbial infection induces autoreactive TH17 cells. Nat. Immunol. 17, 1084-1092 (2016).
87. Hand, T.W. et al. Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses. Science 337, 1553-1556 (2012).
88. Blander, J.M., Torchinsky, M.B. &Campisi, L. Revisiting the old link between infection and autoimmune disease with commensals and T helper 17 cells. Immunol. Res. 54, 50-68 (2012).
89. Yang, Y. et al. Focused specificity of intestinal TH17 cells towards commensal bacterial antigens. Nature 510, 152-156 (2014).
90. Wu, H.J. et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 32, 815-827 (2010).
91. Lee, Y.K., Menezes, J.S., Umesaki, Y. &Mazmanian, S.K. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA 108 (Suppl. 1), 4615-4622 (2011).
92. Asquith, M.J. et al. Perturbed mucosal immunity and dysbiosis accompany clinical disease in a rat model of spondyloarthritis. Arthritis Rheumatol. 68, 2151-2162 (2016).
93. Ciccia, F. et al. Dysbiosis and zonulin upregulation alter gut epithelial and vascular barriers in patients with ankylosing spondylitis. Ann. Rheum. Dis. 76, 1123-1132 (2017).
94. Teng, F. et al. Gut microbiota drive autoimmune arthritis by promoting differentiation and migration of Peyer's patch T follicular helper cells. Immunity 44, 875-888 (2016).
95. Cryan, J.F. &Dinan, T.G. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 13, 701-712 (2012).
96. Sharon, G., Sampson, T.R., Geschwind, D.H. &Mazmanian, S.K. The central nervous system and the gut microbiome. Cell 167, 915-932 (2016).
97. Gabanyi, I. et al. Neuro-immune interactions drive tissue programming in intestinal macrophages. Cell 164, 378-391 (2016).
98. Rieder, R., Wisniewski, P.J., Alderman, B.L. &Campbell, S.C. Microbes and mental health: a review. Brain Behav. Immun. http://dx.doi.org/10.1016/j.bbi.2017.01.016 (2017).
99. Yano, J.M. et al. Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 161, 264-276 (2015)
100. Reigstad, C.S. et al. Gut microbes promote colonic serotonin production through an effect of short-chain fatty acids on enterochromaffin cells. FASEB J. 29, 1395-1403 (2015).
101. O'Mahony, S.M., Clarke, G., Borre, Y.E., Dinan, T.G. &Cryan, J.F. Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behav. Brain Res. 277, 32-48 (2015).
102. Erny, D. et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat. Neurosci. 18, 965-977 (2015).
103. Matcovitch-Natan, O. et al. Microglia development follows a stepwise program to regulate brain homeostasis. Science 353, aad8670 (2016).
104. Sampson, T.R. et al. Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson′s disease. Cell 167, 1469-1480.e12 (2016).
105. Rothhammer, V. et al. Type I interferons and microbial metabolites of tryptophan modulate astrocyte activity and central nervous system inflammation via the aryl hydrocarbon receptor. Nat. Med. 22, 586-597 (2016).
106. Schirmer, M. et al. Linking the human gut microbiome to inflammatory cytokine production capacity. Cell 167, 1125-1136.e8 (2016)
107. Buffie, C.G. et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature 517, 205-208 (2015).
108. Rangan, K.J. et al. A secreted bacterial peptidoglycan hydrolase enhances tolerance to enteric pathogens. Science 353, 1434-1437 (2016).
109. Sansone, C.L. et al. Microbiota-dependent priming of antiviral intestinal immunity in Drosophila. Cell Host Microbe 18, 571-581 (2015).
110. Khosravi, A. et al. Gut microbiota promote hematopoiesis to control bacterial infection. Cell Host Microbe 15, 374-381 (2014).
111. Ichinohe, T. et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc. Natl. Acad. Sci. USA 108, 5354-5359 (2011).
112. Clarke, T.B. et al. Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat. Med. 16, 228-231 (2010).
113. Pamer, E.G. Resurrecting the intestinal microbiota to combat antibiotic-resistant pathogens. Science 352, 535-538 (2016).
114. Soares, M.P., Teixeira, L. &Moita, L.F. Disease tolerance and immunity in host protection against infection. Nat. Rev. Immunol. 17, 83-96 (2017).
115. Schieber, A.M. et al. Disease tolerance mediated by microbiome E. coli involves inflammasome and IGF-1 signaling. Science 350, 558-563 (2015).
116. Pickard, J.M. et al. Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature 514, 638-641 (2014).
117. Reichardt, N. et al. Phylogenetic distribution of three pathways for propionate production within the human gut microbiota. ISME J. 8, 1323-1335 (2014).
118. Fonseca, D.M. et al. Microbiota-dependent sequelae of acute infection compromise tissue-specific immunity. Cell 163, 354-366 (2015).
119. Kim, D. et al. Nod2-mediated recognition of the microbiota is critical for mucosal adjuvant activity of cholera toxin. Nat. Med. 22, 524-530 (2016).
120. Ruane, D. et al. Microbiota regulate the ability of lung dendritic cells to induce IgA class-switch recombination and generate protective gastrointestinal immune responses. J. Exp. Med. 213, 53-73 (2016).
121. Oh, J.Z. et al. TLR5-mediated sensing of gut microbiota is necessary for antibody responses to seasonal influenza vaccination. Immunity 41, 478-492 (2014).
122. Nakaya, H.I. et al. Systems biology of vaccination for seasonal influenza in humans. Nat. Immunol. 12, 786-795 (2011).
123. Kollmann, T.R., Kampmann, B., Mazmanian, S.K., Marchant, A. &Levy, O. Protecting the newborn and young infant from infectious diseases: lessons from immune ontogeny. Immunity 46, 350-363 (2017).
124. Valdez, Y., Brown, E.M. &Finlay, B.B. Influence of the microbiota on vaccine effectiveness. Trends Immunol. 35, 526-537 (2014).
125. Grivennikov, S.I. et al. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature 491, 254-258 (2012).
126. Huber, S. et al. IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine. Nature 491, 259-263 (2012).
127. Ekbom, A., Helmick, C., Zack, M. &Adami, H.O. Ulcerative colitis and colorectal cancer: apopulation-based study. N. Engl. J. Med. 323, 1228-1233 (1990).
128. Arthur, J.C. et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338, 120-123 (2012).
129. Kostic, A.D. et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 14, 207-215 (2013).
130. Wu, S. et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat. Med. 15, 1016-1022 (2009).
131. Pitt, J.M. et al. Fine-tuning cancer immunotherapy: optimizing the gut microbiome. Cancer Res. 76, 4602-4607 (2016).
132. Vétizou, M. et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 350, 1079-1084 (2015).
133. Sivan, A. et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 350, 1084-1089 (2015).