Intestinal Bacterial Colonization Induces Mutualistic Regulatory T Cell Responses

Immunity

Volumn 34, Issue 5, 2011, Pages 794-806

  Geuking, Markus B ^a,b   Cahenzli, Julia ^a,b   Lawson, Melissa A E ^a,b   Ng, Derek C K ^b   Slack, Emma ^a,b   Hapfelmeier, Siegfried ^a,b   McCoy, Kathy D ^a,b   Macpherson, Andrew J ^a,b  

^a UNIVERSITY OF BERN   (Switzerland)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; CD4+ T LYMPHOCYTE; COLON INJURY; CONTROLLED STUDY; INTESTINE FLORA; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH17 CELL;

ADAPTIVE IMMUNITY; ANIMALS; CELL PROLIFERATION; COLON; HOMEOSTASIS; IMMUNITY, MUCOSAL; INTERLEUKIN-10; LYMPHOCYTE ACTIVATION; MICE; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; T-LYMPHOCYTES, REGULATORY;

EID: 79956315886     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2011.03.021     Document Type: Article

References (47)

1. 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.
2. Barnes M.J., Powrie F. Regulatory T cells reinforce intestinal homeostasis. Immunity 2009, 31:401-411.
3. Benson M.J., Pino-Lagos K., Rosemblatt M., Noelle R.J. All-trans retinoic acid mediates enhanced T reg cell growth, differentiation, and gut homing in the face of high levels of co-stimulation. J. Exp. Med. 2007, 204:1765-1774.
4. Chinen T., Volchkov P.Y., Chervonsky A.V., Rudensky A.Y. A critical role for regulatory T cell-mediated control of inflammation in the absence of commensal microbiota. J. Exp. Med. 2010, 207:2323-2330.
5. Coombes J.L., Siddiqui K.R., Arancibia-Cárcamo C.V., Hall J., Sun C.M., Belkaid Y., Powrie F. 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, 204:1757-1764.
6. Coyne M.J., Tzianabos A.O., Mallory B.C., Carey V.J., Kasper D.L., Comstock L.E. Polysaccharide biosynthesis locus required for virulence of Bacteroides fragilis. Infect. Immun. 2001, 69:4342-4350.
7. Curotto de Lafaille M.A., Lafaille J.J. Natural and adaptive foxp3+ regulatory T cells: more of the same or a division of labor?. Immunity 2009, 30:626-635.
8. Dewhirst F.E., Chien C.C., Paster B.J., Ericson R.L., Orcutt R.P., Schauer D.B., Fox J.G. Phylogeny of the defined murine microbiota: Altered Schaedler flora. Appl. Environ. Microbiol. 1999, 65:3287-3292.
9. Fontenot J.D., Rasmussen J.P., Williams L.M., Dooley J.L., Farr A.G., Rudensky A.Y. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 2005, 22:329-341.
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. Hapfelmeier S., Lawson M.A., Slack E., Kirundi J.K., Stoel M., Heikenwalder M., Cahenzli J., Velykoredko Y., Balmer M.L., Endt K., et al. Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses. Science 2010, 328:1705-1709.
12. Hoebe K., Du X., Georgel P., Janssen E., Tabeta K., Kim S.O., Goode J., Lin P., Mann N., Mudd S., et al. Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 2003, 424:743-748.
13. Hrncir T., Stepankova R., Kozakova H., Hudcovic T., Tlaskalova-Hogenova H. Gut microbiota and lipopolysaccharide content of the diet influence development of regulatory T cells: Studies in germ-free mice. BMC Immunol. 2008, 9:65.
14. Huehn J., Siegmund K., Lehmann J.C., Siewert C., Haubold U., Feuerer M., Debes G.F., Lauber J., Frey O., Przybylski G.K., et al. Developmental stage, phenotype, and migration distinguish naive- and effector/memory-like CD4+ regulatory T cells. J. Exp. Med. 2004, 199:303-313.
15. Ivanov I.I., McKenzie B.S., Zhou L., Tadokoro C.E., Lepelley A., Lafaille J.J., Cua D.J., Littman D.R. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006, 126:1121-1133.
16. Ivanov I.I., Frutos Rde.L., Manel N., Yoshinaga K., Rifkin D.B., Sartor R.B., Finlay B.B., Littman D.R. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 2008, 4:337-349.
17. 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.
18. Iwata M. Retinoic acid production by intestinal dendritic cells and its role in T-cell trafficking. Semin. Immunol. 2009, 21:8-13.
19. Izcue A., Coombes J.L., Powrie F. Regulatory lymphocytes and intestinal inflammation. Annu. Rev. Immunol. 2009, 27:313-338.
20. Jaensson E., Uronen-Hansson H., Pabst O., Eksteen B., Tian J., Coombes J.L., Berg P.L., Davidsson T., Powrie F., Johansson-Lindbom B., Agace W.W. Small intestinal CD103+ dendritic cells display unique functional properties that are conserved between mice and humans. J. Exp. Med. 2008, 205:2139-2149.
21. Konno R., Oowada T., Ozaki A., Iida T., Niwa A., Yasumura Y., Mizutani T. Origin of D-alanine present in urine of mutant mice lacking D-amino-acid oxidase activity. Am. J. Physiol. 1993, 265:G699-G703.
22. Lehmann J., Huehn J., de la Rosa M., Maszyna F., Kretschmer U., Krenn V., Brunner M., Scheffold A., Hamann A. Expression of the integrin alpha Ebeta 7 identifies unique subsets of CD25+ as well as CD25- regulatory T cells. Proc. Natl. Acad. Sci. USA 2002, 99:13031-13036.
23. Macpherson A.J., Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 2004, 303:1662-1665.
24. Macpherson A.J., Geuking M.B., McCoy K.D. Immune responses that adapt the intestinal mucosa to commensal intestinal bacteria. Immunology 2005, 115:153-162.
25. Mangan P.R., Harrington L.E., O'Quinn D.B., Helms W.S., Bullard D.C., Elson C.O., Hatton R.D., Wahl S.M., Schoeb T.R., Weaver C.T. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006, 441:231-234.
26. Manicassamy S., Reizis B., Ravindran R., Nakaya H., Salazar-Gonzalez R.M., Wang Y.C., Pulendran B. Activation of beta-catenin in dendritic cells regulates immunity versus tolerance in the intestine. Science 2010, 329:849-853.
27. Maynard C.L., Harrington L.E., Janowski K.M., Oliver J.R., Zindl C.L., Rudensky A.Y., Weaver C.T. Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3- precursor cells in the absence of interleukin 10. Nat. Immunol. 2007, 8:931-941.
28. Mazmanian S.K., Round J.L., Kasper D.L. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 2008, 453:620-625.
29. Min B., Thornton A., Caucheteux S.M., Younes S.A., Oh K., Hu-Li J., Paul W.E. Gut flora antigens are not important in the maintenance of regulatory T cell heterogeneity and homeostasis. Eur. J. Immunol. 2007, 37:1916-1923.
30. Oxenius A., Bachmann M.F., Zinkernagel R.M., Hengartner H. Virus-specific MHC-class II-restricted TCR-transgenic mice: effects on humoral and cellular immune responses after viral infection. Eur. J. Immunol. 1998, 28:390-400.
31. Polk B.F., Kasper D.L. Bacteroides fragilis subspecies in clinical isolates. Ann. Intern. Med. 1977, 86:569-571.
32. 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.
33. Ramsey C., Rubinstein M.P., Kim D.M., Cho J.H., Sprent J., Surh C.D. The lymphopenic environment of CD132 (common gamma-chain)-deficient hosts elicits rapid homeostatic proliferation of naive T cells via IL-15. J. Immunol. 2008, 180:5320-5326.
34. 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.
35. Sartor R.B. Pathogenesis and immune mechanisms of chronic inflammatory bowel diseases. Am. J. Gastroenterol. 1997, 92(12, Suppl):5S-11S.
36. Siewert C., Lauer U., Cording S., Bopp T., Schmitt E., Hamann A., Huehn J. Experience-driven development: Effector/memory-like alphaE+Foxp3+ regulatory T cells originate from both naive T cells and naturally occurring naive-like regulatory T cells. J. Immunol. 2008, 180:146-155.
37. Slack E., Hapfelmeier S., Stecher B., Velykoredko Y., Stoel M., Lawson M.A., Geuking M.B., Beutler B., Tedder T.F., Hardt W.D., et al. Innate and adaptive immunity cooperate flexibly to maintain host-microbiota mutualism. Science 2009, 325:617-620.
38. Smith K., McCoy K.D., Macpherson A.J. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin. Immunol. 2007, 19:59-69.
39. Stephens G.L., Andersson J., Shevach E.M. Distinct subsets of FoxP3+ regulatory T cells participate in the control of immune responses. J. Immunol. 2007, 178:6901-6911.
40. Sun C.M., Hall J.A., Blank R.B., Bouladoux N., Oukka M., Mora J.R., Belkaid Y. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 2007, 204:1775-1785.
41. Suzuki K., Meek B., Doi Y., Muramatsu M., Chiba T., Honjo T., Fagarasan S. Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proc. Natl. Acad. Sci. USA 2004, 101:1981-1986.
42. Tannock G.W. What immunologists should know about bacterial communities of the human bowel. Semin. Immunol. 2007, 19:94-105.
43. Thornton A.M., Korty P.E., Tran D.Q., Wohlfert E.A., Murray P.E., Belkaid Y., Shevach E.M. Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells. J. Immunol. 2010, 184:3433-3441.
44. Weisburg W.G., Barns S.M., Pelletier D.A., Lane D.J. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 1991, 173:697-703.
45. Wexler H.M. Bacteroides: The good, the bad, and the nitty-gritty. Clin. Microbiol. Rev. 2007, 20:593-621.
46. Whitman W.B., Coleman D.C., Wiebe W.J. Prokaryotes: The unseen majority. Proc. Natl. Acad. Sci. USA 1998, 95:6578-6583.
47. Zhao D., Zhang C., Yi T., Lin C.L., Todorov I., Kandeel F., Forman S., Zeng D. In vivo-activated CD103+CD4+ regulatory T cells ameliorate ongoing chronic graft-versus-host disease. Blood 2008, 112:2129-2138.