Lymphoid-Tissue-Resident Commensal Bacteria Promote Members of the IL-10 Cytokine Family to Establish Mutualism

Immunity

Volumn 44, Issue 3, 2016, Pages 634-646

  Fung, Thomas C ^a,b   Bessman, Nicholas J ^b   Hepworth, Matthew R ^b   Kumar, Nitin ^c   Shibata, Naoko ^d,e   Kobuley, Dmytro ^a   Wang, Kelvin ^a   Ziegler, Carly G K ^f   Goc, Jeremy ^b   Shima, Tatsuichiro ^g   Umesaki, Yoshinori ^g   Sartor, R Balfour ^h   Sullivan, Kaede V ^a   Lawley, Trevor D ^c   Kunisawa, Jun ⁱ   Kiyono, Hiroshi ^d,e   Sonnenberg, Gregory F ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d THE UNIVERSITY OF TOKYO   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^f MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^g YAKULT CENTRAL INSTITUTE FOR MICROBIOLOGICAL RESEARCH   (Japan)

^h UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

ⁱ and Nutrition   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 22; CYTOKINE; INTERLEUKIN 10 RECEPTOR; INTERLEUKIN DERIVATIVE; INTERLEUKIN-22;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIUM; COMMENSAL; CYTOKINE PRODUCTION; DENDRITIC CELL; INTESTINE INJURY; LYMPHOID CELL; LYMPHOID TISSUE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SYMBIOSIS; 129 MOUSE; ANIMAL; BORDETELLA; BORDETELLOSIS; C57BL MOUSE; CELL CULTURE; GENETICS; IMMUNOLOGY; INTESTINE; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; MICROFLORA; TH17 CELL;

ANIMALS; BORDETELLA; BORDETELLA INFECTIONS; CELLS, CULTURED; CYTOKINES; DENDRITIC CELLS; INTERLEUKIN-10; INTERLEUKINS; INTESTINES; LYMPHOID TISSUE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROBIOTA; RECEPTORS, INTERLEUKIN-10; SYMBIOSIS; TH17 CELLS;

EID: 84960341158     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.02.019     Document Type: Article

References (38)

1. Arpaia N., Campbell C., Fan X., Dikiy S., van der Veeken J., deRoos P., Liu H., Cross J.R., Pfeffer K., Coffer P.J., Rudensky A.Y. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013, 504:451-455.
2. Atarashi K., Tanoue T., Shima T., Imaoka A., Kuwahara T., Momose Y., Cheng G., Yamasaki S., Saito T., Ohba Y., et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011, 331:337-341.
3. Ayres J.S., Trinidad N.J., Vance R.E. Lethal inflammasome activation by a multidrug-resistant pathobiont upon antibiotic disruption of the microbiota. Nat. Med. 2012, 18:799-806.
4. Belkaid Y., Hand T.W. Role of the microbiota in immunity and inflammation. Cell 2014, 157:121-141.
5. Brenchley J.M., Douek D.C. Microbial translocation across the GI tract. Annu. Rev. Immunol. 2012, 30:149-173.
6. Chiu C.C., Ching Y.H. Monocolonization of germ-free mice with Bacteroides fragilis protects against dextran sulfate sodium-induced acute colitis. BioMed Res. Int. 2014, 2014:675786.
7. Chow J., Lee S.M., Shen Y., Khosravi A., Mazmanian S.K. Host-bacterial symbiosis in health and disease. Adv. Immunol. 2010, 107:243-274.
8. Fung T.C., Artis D., Sonnenberg G.F. Anatomical localization of commensal bacteria in immune cell homeostasis and disease. Immunol. Rev. 2014, 260:35-49.
9. Furusawa Y., Obata Y., Fukuda S., Endo T.A., Nakato G., Takahashi D., Nakanishi Y., Uetake C., Kato K., Kato T., et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 2013, 504:446-450.
10. Gaboriau-Routhiau V., Rakotobe S., Lécuyer E., Mulder I., Lan A., Bridonneau C., Rochet V., Pisi A., De Paepe M., Brandi G., et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 2009, 31:677-689.
11. Geuking M.B., Cahenzli J., Lawson M.A., Ng D.C., Slack E., Hapfelmeier S., McCoy K.D., Macpherson A.J. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity 2011, 34:794-806.
12. Honda K., Littman D.R. The microbiome in infectious disease and inflammation. Annu. Rev. Immunol. 2012, 30:759-795.
13. Hooper L.V., Macpherson A.J. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat. Rev. Immunol. 2010, 10:159-169.
14. Hooper L.V., Littman D.R., Macpherson A.J. Interactions between the microbiota and the immune system. Science 2012, 336:1268-1273.
15. Ivanov I.I., Atarashi K., Manel N., Brodie E.L., Shima T., Karaoz U., Wei D., Goldfarb K.C., Santee C.A., Lynch S.V., et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009, 139:485-498.
16. Kitajima S., Morimoto M., Sagara E., Shimizu C., Ikeda Y. Dextran sodium sulfate-induced colitis in germ-free IQI/Jic mice. Exp. Anim. 2001, 50:387-395.
17. Klose C.S., Kiss E.A., Schwierzeck V., Ebert K., Hoyler T., d'Hargues Y., Göppert N., Croxford A.L., Waisman A., Tanriver Y., Diefenbach A. A T-bet gradient controls the fate and function of CCR6-RORγt+ innate lymphoid cells. Nature 2013, 494:261-265.
18. Kühn R., Löhler J., Rennick D., Rajewsky K., Müller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 1993, 75:263-274.
19. 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.
20. Lee S.M., Donaldson G.P., Mikulski Z., Boyajian S., Ley K., Mazmanian S.K. Bacterial colonization factors control specificity and stability of the gut microbiota. Nature 2013, 501:426-429.
21. Liu B., Tonkonogy S.L., Sartor R.B. Antigen-presenting cell production of IL-10 inhibits T-helper 1 and 17 cell responses and suppresses colitis in mice. Gastroenterology 2011, 141:653-662. 662.e1-662.e4.
22. Manichanh C., Borruel N., Casellas F., Guarner F. The gut microbiota in IBD. Nat. Rev. Gastroenterol. Hepatol. 2012, 9:599-608.
23. Maslowski K.M., Vieira A.T., Ng A., Kranich J., Sierro F., Yu D., Schilter H.C., Rolph M.S., Mackay F., Artis D., et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 2009, 461:1282-1286.
24. McGeachy M.J., Bak-Jensen K.S., Chen Y., Tato C.M., Blumenschein W., McClanahan T., Cua D.J. TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat. Immunol. 2007, 8:1390-1397.
25. Obata T., Goto Y., Kunisawa J., Sato S., Sakamoto M., Setoyama H., Matsuki T., Nonaka K., Shibata N., Gohda M., et al. Indigenous opportunistic bacteria inhabit mammalian gut-associated lymphoid tissues and share a mucosal antibody-mediated symbiosis. Proc. Natl. Acad. Sci. USA 2010, 107:7419-7424.
26. Ouyang W., Rutz S., Crellin N.K., Valdez P.A., Hymowitz S.G. Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu. Rev. Immunol. 2011, 29:71-109.
27. Qiu J., Guo X., Chen Z.M., He L., Sonnenberg G.F., Artis D., Fu Y.X., Zhou L. Group 3 innate lymphoid cells inhibit T-cell-mediated intestinal inflammation through aryl hydrocarbon receptor signaling and regulation of microflora. Immunity 2013, 39:386-399.
28. Rakoff-Nahoum S., Paglino J., Eslami-Varzaneh F., Edberg S., Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004, 118:229-241.
29. Round J.L., Mazmanian S.K. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc. Natl. Acad. Sci. USA 2010, 107:12204-12209.
30. Sander L.E., Davis M.J., Boekschoten M.V., Amsen D., Dascher C.C., Ryffel B., Swanson J.A., Müller M., Blander J.M. Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 2011, 474:385-389.
31. Satoh-Takayama N., Vosshenrich C.A., Lesjean-Pottier S., Sawa S., Lochner M., Rattis F., Mention J.J., Thiam K., Cerf-Bensussan N., Mandelboim O., et al. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 2008, 29:958-970.
32. Shih V.F., Cox J., Kljavin N.M., Dengler H.S., Reichelt M., Kumar P., Rangell L., Kolls J.K., Diehl L., Ouyang W., Ghilardi N. Homeostatic IL-23 receptor signaling limits Th17 response through IL-22-mediated containment of commensal microbiota. Proc. Natl. Acad. Sci. USA 2014, 111:13942-13947.
33. Smith P.M., Howitt M.R., Panikov N., Michaud M., Gallini C.A., Bohlooly-Y M., Glickman J.N., Garrett W.S. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013, 341:569-573.
34. Sonnenberg G.F., Artis D. Innate lymphoid cells in the initiation, regulation and resolution of inflammation. Nat. Med. 2015, 21:698-708.
35. Sonnenberg G.F., Fouser L.A., Artis D. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat. Immunol. 2011, 12:383-390.
36. Sonnenberg G.F., Monticelli L.A., Alenghat T., Fung T.C., Hutnick N.A., Kunisawa J., Shibata N., Grunberg S., Sinha R., Zahm A.M., et al. Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria. Science 2012, 336:1321-1325.
37. Ueda Y., Kayama H., Jeon S.G., Kusu T., Isaka Y., Rakugi H., Yamamoto M., Takeda K. Commensal microbiota induce LPS hyporesponsiveness in colonic macrophages via the production of IL-10. Int. Immunol. 2010, 22:953-962.
38. Upadhyay V., Poroyko V., Kim T.J., Devkota S., Fu S., Liu D., Tumanov A.V., Koroleva E.P., Deng L., Nagler C., et al. Lymphotoxin regulates commensal responses to enable diet-induced obesity. Nat. Immunol. 2012, 13:947-953.