Interaction between the gut microbiome and mucosal immune system

Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464:59–65. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science. 2005;308:1635–8. Lee YK, Mazmanian SK. Has the microbiota played a critical role in the evolution of the adaptive immune system? Science. 2010;330:1768–73. Harmsen H, de Goffau M. The human gut microbiota. Adv Exp Med Biol. 2016;902:95–108. Hasegawa M, Inohara N. Regulation of the gut microbiota by the mucosal immune system in mice. Int Immunol. 2014;26:481–7. Richards JL, Yap YA, Mcleod KH, Mackay CR, Marino E. Dietary metabolites and the gut microbiota: an alternative approach to control inflammatory and autoimmune diseases. Clin Transl Immunol. 2016;5:e82. Chan CW, Wong RS, Law PT, Wong CL, Tsui SK, Tang WP, et al. Environmental factors associated with altered gut microbiota in children with eczema: a systematic review. Int J Mol Sci. 2016;17:1147. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI. Human nutrition, the gut microbiome and the immune system. Nature. 2011;474:327–36. Mcdermott AJ, Huffnagle GB. The microbiome and regulation of mucosal immunity. Immunology. 2014;142:24–31. Topping DL, Clifton PM. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev. 2001;81:1031–64. Kuhn KA, Pedraza I, Demoruelle MK. Mucosal immune responses to microbiota in the development of autoimmune disease. Rheum Dis Clin N Am. 2014;40:711–25. Romanokeeler J, Moore DJ, Wang C, Brucker RM, Fonnesbeck C. Early life establishment of site-specific microbial communities in the gut. Gut Microbes. 2014;5:192–201. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–131. Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490:55–60. Yang T, Santisteban MM, Rodriguez V, Li E, Ahmari N, Carvajal JM, et al. Gut dysbiosis is linked to hypertensionnovelty and significance. Hypertension. 2015;65:1331–40. Mai V, Young CM, Ukhanova M, Wang X, Sun Y, Casella G, et al. Fecal microbiota in premature infants prior to necrotizing enterocolitis. PLoS ONE. 2011;6:e20647. Frank DN, St AA, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A. 2007;104:13780–5. Ayabe T, Ashida T, Kohgo Y, Kono T. The role of paneth cells and their antimicrobial peptides in innate host defense. Trends Microbiol. 2004;12:394–8. van Es JH, Jay P, Gregorieff A, Van Gijn ME, Jonkheer S, Hatzis P, et al. Wnt signalling induces maturation of paneth cells in intestinal crypts. Nat Cell Biol. 2005;7:381–6. Bals R, Weiner DJ, Moscioni AD, Meegalla RL, Wilson JM. Augmentation of innate host defense by expression of a cathelicidin antimicrobial peptide. Infect Immunol. 1999;67:6084–9. Scott MG, Davidson DJ, Gold MR, Bowdish D, Hancock RE. The human antimicrobial peptide IL-37 is a multifunctional modulator of innate immune responses. J Immunol. 2002;169:3883–91. Wilson CL, Ouellette AJ, Satchell DP, Ayabe T, Lopez-Boado YS, Stratman JL, et al. Regulation of intestinal alpha-defensin activation by the metalloproteinase matrilysin in innate host defense. Science. 1999;286:113–7. Cash HL, Whitham CV, Behrendt CL, Hooper LV. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science. 2006;313:1126–30. Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, Ouellette AJ. Secretion of microbicidal alpha-defensins by intestinal paneth cells in response to bacteria. Nat Immunol. 2000;1:113–8. Birchler T, Seibl R, Buchner K, Loeliger S, Seger R, Hossle JP, et al. Human Toll-like receptor 2 mediates induction of the antimicrobial peptide human beta-defensin 2 in response to bacterial lipoprotein. Eur J Immunol. 2001;31:3131–7. Stelter C, Kappeli R, Konig C, Krah A, Hardt WD, Stecher B, et al. Salmonella-induced mucosal lectin regiiibeta kills competing gut microbiota. PLoS ONE. 2011;6:E20749. Vaishnava S, Yamamoto M, Severson KM, Ruhn KA, Yu X, Koren O, et al. The Antibacterial lectin RegIII promotes the spatial segregation of microbiota and host in the intestine. Science. 2011;334:255–8. Zenewicz LA, Yancopoulos GD, Valenzuela DM, Murphy AJ, Stevens S, Flavell RA. Innate and adaptive interleukin-22 protects mice from inflammatory bowel disease. Immunity. 2008;29:947–57. Sonnenberg GF, Monticelli LA, Elloso MM, Fouser LA, Artis D. CD4(+) lymphoid tissue-inducer cells promote innate immunity in the gut. Immunity. 2011;34:122–34. Mukherjee S, Zheng H, Derebe MG, Callenberg KM, Partch CL, Rollins D, et al. Antibacterial membrane attack by a pore-forming intestinal c-type lectin. Nature. 2014;505:103–7. Wang HC, Zhou Q, Dragoo J, Klein JR. Most murine CD8+ intestinal intraepithelial lymphocytes are partially but not fully activated t cells. J Immunol. 2002;169:4717–22. Moretto M, Weiss LM, Khan IA. Induction of a rapid and strong antigen-specific intraepithelial lymphocyte response during oral Encephalitozoon cuniculi infection. J Immunol. 2004;172:4402–9. Boismenu R, Havran WL. Modulation of epithelial cell growth by intraepithelial gamma delta T cells. Science. 1994;266:1253–5. Simpson SJ, Hollander GA, Mizoguchi E, Allen D, Bhan AK, Wang B, et al. Expression of pro-inflammatory cytokines by TCR alpha beta + and TCR gamma delta + T cells in an experimental model of colitis. Eur J Immunol. 1997;27:17–25. Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R, et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol. 2001;2:361–7. Colombo BM, Scalvenzi T, Benlamara S, Pollet N. Microbiota and mucosal immunity in amphibians. Front Immunol. 2015;6:111. Chu H, Khosravi A, Kusumawardhani IP, Kwon AH, Vasconcelos AC, Cunha LD, et al. Gene-microbiota interactions contribute to the pathogenesis of inflammatory bowel disease. Science. 2016;352:1116–20. Sierro F, Dubois B, Coste A, Kaiserlian D, Kraehenbuhl JP, Sirard JC. Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells. Proc Natl Acad Sci U S A. 2001;98:13722–7. Gewirtz AT, Navas TA, Lyons S, Godowski PJ, Madara JL. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol. 2001;167:1882–5. Akira S, Takeda K, Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol. 2001;2:675–80. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, Goodlett DR, et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature. 2001;410:1099–103. Lui JB, Devarajan P, Teplicki SA, Chen Z. Cross-differentiation from the CD8 lineage to cd4 t cells in the gut-associated microenvironment with a nonessential role of microbiota. Cell Rep. 2015;10:574–85. Munoz M, Heimesaat MM, Danker K, Struck D, Lohmann U, Plickert R, et al. Interleukin (IL)-23 mediates toxoplasma gondii-induced immunopathology in the gut via matrixmetalloproteinase-2 and IL-22 but independent of IL-17. J Exp Med. 2009;206:3047–59. Awane M, Andres PG, Li DJ, Reinecker HE. NF-kappa B-inducing kinase is a common mediator of IL-17, TNF-alpha, and IL-1 beta-induced chemokine promoter activation in intestinal epithelial cells. J Immunol. 1999;162:5337–44. Reboldi A, Cyster JG. Peyer’s patches: organizing B-cell responses at the intestinal frontier. Immunol Rev. 2016;271:230–45. Bemark M, Boysen P, Lycke NY. Induction of gut IgA production through T cell-dependent and T cell-independent pathways. Ann N Y Acad Sci. 2012;1247:97–116. Bergqvist P, Stensson A, Lycke NY, Bemark M. T cell-independent IgA class switch recombination is restricted to the galt and occurs prior to manifest germinal center formation. J Immunol. 2010;184:3545–53. Carasi P, Racedo SM, Jacquot C, Romanin DE, Serradell MA, Urdaci MC. Impact of kefir derived lactobacillus kefiri on the mucosal immune response and gut microbiota. J Immunol Res. 2015;2015:1–12. Gicheva N, Macauley MS, Arlian BM, Paulson JC, Kawasaki N. Siglec-F is a novel intestinal M cell marker. Biochem Biophys Res Commun. 2016;479:1–4. Berg D, Clemente JC, Colombel JF. Can inflammatory bowel disease be permanently treated with short-term interventions on the microbiome? Expert Rev Gastroenterol Hepatol. 2015;9:781–95. Bandeira A, Mota-Santos T, Itohara S, Degermann S, Heusser C, Tonegawa S, et al. Localization of gamma/delta T cells to the intestinal epithelium is independent of normal microbial colonization. J Exp Med. 1990;172:239–44. Crabbe PA, Bazin H, Eyssen H, Heremans JF. The normal microbial flora as a major stimulus for proliferation of plasma cells synthesizing Iga in the gut. the germ-free intestinal tract. Int Arch Allergy Appl Immunol. 1968;34:362–75. Ostman S, Rask C, Wold AE, Hultkrantz S, Telemo E. Impaired regulatory T cell function in germ-free mice. Eur J Immunol. 2006;36:2336–46. Hooper LV, Stappenbeck TS, Hong CV, Gordon JI. Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat Immunol. 2003;4:269–73. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444:1022–3. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–63. Wright EK, Kamm MA, Teo SM, Inouye M, Wagner J, Kirkwood CD. Recent advances in characterizing the gastrointestinal microbiome in crohnʼs disease. Inflamm Bowel Dis. 2015;21:1219–28. Sk M, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 2008;453:620–5. Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci U S A. 2010;107:12204–9. Round JL, Lee SM, Li J, Tran G, Jabri B, Chatila TA, et al. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science. 2011;332:974–7. Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, et al. Induction of colonic regulatory T cells by indigenous clostridium species. Science. 2011;331:337–41. Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, et al. Treg induction by a rationally selected mixture of clostridia strains from the human microbiota. Nature. 2013;500:232–6. Norman JM, Handley SA, Baldridge MT, Droit L, Liu CY, Keller BC, et al. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell. 2015;160:447–60. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009;139:485–98. Stepankova R, Powrie F, Kofronova O, Kozakova H, Hudcovic T, Hrncir T, et al. Segmented filamentous bacteria in a defined bacterial cocktail induce intestinal inflammation in SCID mice reconstituted with CD45RB high CD4+ T cells. Inflamm Bowel Dis. 2007;13:1202–11. Ivanov II WHJ, Darce J, Hattori K, Shima T, Umesaki Y, et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity. 2010;32:815–27. Lee YK, Menezes JS, Umesaki Y, Mazmanian SK. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A. 2011;108:4615–22. Spehlmann ME, Begun AZ, Burghardt J, Lepage P, Raedler A, Schreiber S. Epidemiology of inflammatory bowel disease in a german twin cohort: results of a nationwide study. Inflamm Bowel Dis. 2008;14:968–76. Seksik P, Rigottier-Gois L, Gramet G, Sutren M, Pochart P, Marteau P, et al. Alterations of the dominant faecal bacterial groups in patients with crohn’s disease of the colon. Gut. 2003;52:237–42. Gophna U, Sommerfeld K, Gophna S, Doolittle WF, Veldhuyzen VZS. Differences between tissue-associated intestinal microfloras of patients with Crohn’s disease and ulcerative colitis. J Clin Microbiol. 2006;44:4136–41. Wang ZK, Yang YS, Chen Y, Yuan J, Sun G, Peng LH. Intestinal microbiota pathogenesis and fecal microbiota transplantation for inflammatory bowel disease. World J Gastroenterol. 2014;20:14805–20. Lamas B, Richard ML, Leducq V, Pham HP, Michel ML, Da CG, et al. CARD9 impacts colitis by altering gut microbiota metabolism of tryptophan into aryl hydrocarbon receptor ligands. Nat Med. 2016;22:598–605. Longman RS, Diehl GE, Victorio DA, Huh JR, Galan C, Miraldi ER, et al. CX(3)CR1(+) mononuclear phagocytes support colitis-associated innate lymphoid cell production of IL-22. J Exp Med. 2014;211:1571–83. Cheng X, Zhang X, Su J, Zhang Y, Zhou W, Zhou J, et al. Mir-19b downregulates intestinal SOCS3 to reduce intestinal inflammation in Crohn’s disease. Sci Rep. 2015;5:10397. Glocker EO, Kotlarz D, Boztug K, Gertz EM, Schaffer AA, Noyan F, et al. Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N Engl J Med. 2009;361:2033–45. Shah N, Kammermeier J, Elawad M, Glocker EO. Interleukin-10 and interleukin-10-receptor defects in inflammatory bowel disease. Curr Allergy Asthma Rep. 2012;12:373–9. Huda-Faujan N, Abdulamir AS, Fatimah AB, Anas OM, Shuhaimi M, Yazid AM, et al. The impact of the level of the intestinal short chain fatty acids in inflammatory bowel disease patients versus healthy subjects. Open Biochem J. 2010;4:53–8. Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, Yu D, et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature. 2009;461:1282–6. Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly YM, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013;341:569–73. Macfarlane GT, Blackett KL, Nakayama T, Steed H, Macfarlane S. The gut microbiota in inflammatory bowel disease. Curr Pharm Design. 2009;15:1528–36. Palm NW, de Zoete MR, Cullen TW, Barry NA, Stefanowski J, Hao L, et al. Immunoglobulin A coating identifies colitogenic bacteria in inflammatory bowel disease. Cell. 2014;158:1000–10. Rantapaa-Dahlqvist S, de Jong BA, Berglin E, Hallmans G, Wadell G, Stenlund H, et al. Antibodies against cyclic citrullinated peptide and IgA rheumatoid factor predict the development of rheumatoid arthritis. Arthritis Rheum. 2003;48:2741–9. Arbuckle MR, Mcclain MT, Rubertone MV, Scofield RH, Dennis GJ, James JA, et al. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N Engl J Med. 2003;349:1526–33. Mikuls TR, Thiele GM, Deane KD, Payne JB, O’dell JR, Yu F, et al. Porphyromonas gingivalis and disease-related autoantibodies in individuals at increased risk of rheumatoid arthritis. Arthritis Rheum. 2012;64:3522–30. Hevia A, Milani C, Lopez P, Cuervo A, Arboleya S, Duranti S, et al. Intestinal dysbiosis associated with systemic lupus erythematosus. MBio. 2014;5:E01548–14. Ramirez AS, Rosas A, Hernandez-Beriain JA, Orengo JC, Saavedra P, de la Fe C, et al. Relationship between rheumatoid arthritis and mycoplasma pneumoniae: a case–control study. Rheumatology (Oxford). 2005;44:912–4. Rashid T, Ebringer A. Rheumatoid arthritis is linked to proteus--the evidence. Clin Rheumatol. 2007;26:1036–43. Syrbe U, Scheer R, Wu P, Sieper J. Differential synovial Th1 cell reactivity towards escherichia coli antigens in patients with ankylosing spondylitis and rheumatoid arthritis. Ann Rheum Dis. 2012;71:1573–6. Zhang X, Zhang D, Jia H, Feng Q, Wang D, Liang D, et al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat Med. 2015;21:895–905. Liu X, Zou Q, Zeng B, Fang Y, Wei H. Analysis of fecal lactobacillus community structure in patients with early rheumatoid arthritis. Curr Microbiol. 2013;67:170–6. Scher JU, Sczesnak A, Longman RS, Segata N, Ubeda C, Bielski C, et al. Expansion of intestinal prevotella copri correlates with enhanced susceptibility to arthritis. Elife. 2013;2:E01202. Costello M, Ciccia F, Willner D, Warrington N, Robinson PC, Gardiner B, et al. Intestinal dysbiosis in ankylosing spondylitis. Arthritis Rheumatol. 2015;67:686–91.