Regional Control of Regulatory Immune Cells in the Intestine

Current Pathobiology Reports

Volumn 6, Issue 1, 2018, Pages 29-34

  Morhardt, Tina L ^a   Hayashi, Atsushi ^b,c   Kao, John Y ^b   Kamada, Nobuhiko ^b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c Miyarisan Pharmaceutical Co   (Japan)

Author keywords

Dietary antigen; Gut immune system; Gut microbiota; Interleukin 10; Macrophages; Regulatory T cells

Indexed keywords

EID: 85055268807     PISSN: None     EISSN: 2167485X     Source Type: Journal    
DOI: 10.1007/s40139-018-0156-z     Document Type: Review

References (42)

1. Sakaguchi S, Miyara M, Costantino CM, Hafler DA. FOXP3+ regulatory T cells in the human immune system. Nat Rev Immunol. 2010;10(7):490–500. 10.1038/nri2785.
2. Chen W, Jin W, Hardegen N, et al. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med. 2003;198(12):1875–86. 10.1084/jem.20030152.
3. 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(6015):337–41. 10.1126/science.1198469.
4. Geuking MB, Cahenzli J, Lawson MA, et al. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity. 2011;34(5):794–806. 10.1016/j.immuni.2011.03.021.
5. Tanoue T, Atarashi K, Honda K. Development and maintenance of intestinal regulatory T cells. Nat Rev Immunol. 2016;16(5):295–309. 10.1038/nri.2016.36.
6. Ohnmacht C, Park JH, Cording S, Wing JB, Atarashi K, Obata Y, et al. MUCOSAL IMMUNOLOGY. The microbiota regulates type 2 immunity through RORgammat(+) T cells. Science. 2015;349(6251):989–93. 10.1126/science.aac4263.
7. Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, et al. T induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature. 2013;500(7461):232–6. 10.1038/nature12331.
8. Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly-Y M, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013;341(6145):569–73. 10.1126/science.1241165.
9. Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504(7480):446–50. 10.1038/nature12721.
10. Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504(7480):451–5. 10.1038/nature12726.
11. Park J, Kim M, Kang SG, Jannasch AH, Cooper B, Patterson J, et al. Short-chain fatty acids induce both effector and regulatory T cells by suppression of histone deacetylases and regulation of the mTOR-S6K pathway. Mucosal Immunol. 2015;8(1):80–93. 10.1038/mi.2014.44.
12. 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(27):12204–9. 10.1073/pnas.0909122107.
13. 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(6032):974–7. 10.1126/science.1206095.
14. Di Giacinto C, Marinaro M, Sanchez M, Strober W, Boirivant M. Probiotics ameliorate recurrent Th1-mediated murine colitis by inducing IL-10 and IL-10-dependent TGF-beta-bearing regulatory cells. J Immunol. 2005;174(6):3237–46. 10.4049/jimmunol.174.6.3237.
15. Tang C, Kamiya T, Liu Y, Kadoki M, Kakuta S, Oshima K, et al. Inhibition of dectin-1 signaling ameliorates colitis by inducing lactobacillus-mediated regulatory T cell expansion in the intestine. Cell Host Microbe. 2015;18(2):183–97. 10.1016/j.chom.2015.07.003.
16. • Mortha A, Chudnovskiy A, Hashimoto D, Bogunovic M, Spencer SP, Belkaid Y, et al. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science. 2014;343(6178):1249288. This study describes microbiota-dependent regulatory control of colonic Tregs by macrophages and dendritic cells by way of cytokine granulocyte-macrophage colony-stimulating factor (GM-CSF) produced by RORɣt+ type 3 innate lymphoid cells. 10.1126/science.1249288.
17. Mowat AM, Agace WW. Regional specialization within the intestinal immune system. Nat Rev Immunol. 2014;14(10):667–85. 10.1038/nri3738.
18. Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut. 1987;28(10):1221–7. 10.1136/gut.28.10.1221.
19. •• Kim KS, Hong SW, Han D, Yi J, Jung J, Yang BG, et al. Dietary antigens limit mucosal immunity by inducing regulatory T cells in the small intestine. Science. 2016;351(6275):858–863. This study demonstrated microbiota-independent dietary antigens that are required for the induction of peripheral Tregs in the small intestine. 10.1126/science.aac5560.
20. Coombes JL, Siddiqui KR, Arancibia-Carcamo CV, et al. 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(8):1757–64. 10.1084/jem.20070590.
21. Iwata M, Hirakiyama A, Eshima Y, Kagechika H, Kato C, Song SY. Retinoic acid imprints gut-homing specificity on T cells. Immunity. 2004;21(4):527–38. 10.1016/j.immuni.2004.08.011.
22. Sun CM, Hall JA, Blank RB, Bouladoux N, Oukka M, Mora JR, et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J Exp Med. 2007;204(8):1775–85. 10.1084/jem.20070602.
23. Hill JA, Hall JA, Sun CM, Cai Q, Ghyselinck N, Chambon P, et al. Retinoic acid enhances Foxp3 induction indirectly by relieving inhibition from CD4+CD44hi cells. Immunity. 2008;29(5):758–70. 10.1016/j.immuni.2008.09.018.
24. Kang SW, Kim SH, Lee N, Lee WW, Hwang KA, Shin MS, et al. 1,25-Dihyroxyvitamin D3 promotes FOXP3 expression via binding to vitamin D response elements in its conserved noncoding sequence region. J Immunol. 2012;188(11):5276–82. 10.4049/jimmunol.1101211.
25. Kinoshita M, Kayama H, Kusu T, Yamaguchi T, Kunisawa J, Kiyono H, et al. Dietary folic acid promotes survival of Foxp3+ regulatory T cells in the colon. J Immunol. 2012;189(6):2869–78. 10.4049/jimmunol.1200420.
26. Kuhn R, Lohler J, Rennick D, et al. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993;75(2):263–74. 10.1016/0092-8674(93)80068-P.
27. Sellon RK, Tonkonogy S, Schultz M, Dieleman LA, Grenther W, Balish E, et al. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun. 1998;66(11):5224–31.
28. Kim SC, Tonkonogy SL, Albright CA, Tsang J, Balish EJ, Braun J, et al. Variable phenotypes of enterocolitis in interleukin 10-deficient mice monoassociated with two different commensal bacteria. Gastroenterology. 2005;128(4):891–906. 10.1053/j.gastro.2005.02.009.
29. Cerovic V, Bain CC, Mowat AM, Milling SWF. Intestinal macrophages and dendritic cells: what's the difference? Trends Immunol. 2014;35(6):270–7. 10.1016/j.it.2014.04.003.
30. Denning TL, Wang YC, Patel SR, et al. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol. 2007;8(10):1086–94. 10.1038/ni1511.
31. Denning TL, Norris BA, Medina-Contreras O, Manicassamy S, Geem D, Madan R, et al. Functional specializations of intestinal dendritic cell and macrophage subsets that control Th17 and regulatory T cell responses are dependent on the T cell/APC ratio, source of mouse strain, and regional localization. J Immunol. 2011;187(2):733–47. 10.4049/jimmunol.1002701.
32. Rivollier A, He J, Kole A, Valatas V, Kelsall BL. Inflammation switches the differentiation program of Ly6Chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon. J Exp Med. 2012;209(1):139–55. 10.1084/jem.20101387.
33. Smythies LE, Sellers M, Clements RH, Mosteller-Barnum M, Meng G, Benjamin WH, et al. Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J Clin Invest. 2005;115(1):66–75. 10.1172/JCI200519229.
34. Kamada N, Hisamatsu T, Okamoto S, Sato T, Matsuoka K, Arai K, et al. Abnormally differentiated subsets of intestinal macrophage play a key role in Th1-dominant chronic colitis through excess production of IL-12 and IL-23 in response to bacteria. J Immunol. 2005;175(10):6900–8. 10.4049/jimmunol.175.10.6900.
35. Franchi L, Kamada N, Nakamura Y, Burberry A, Kuffa P, Suzuki S, et al. NLRC4-driven production of IL-1beta discriminates between pathogenic and commensal bacteria and promotes host intestinal defense. Nat Immunol. 2012;13(5):449–56. 10.1038/ni.2263.
36. Murai M, Turovskaya O, Kim G, Madan R, Karp CL, Cheroutre H, et al. Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat Immunol. 2009;10(11):1178–84. 10.1038/ni.1791.
37. Hadis U, Wahl B, Schulz O, Hardtke-Wolenski M, Schippers A, Wagner N, et al. Intestinal tolerance requires gut homing and expansion of FoxP3+ regulatory T cells in the lamina propria. Immunity. 2011;34(2):237–46. 10.1016/j.immuni.2011.01.016.
38. •• Bain CC, Bravo-Blas A, Scott CL, Gomez Perdiguero E, Geissmann F, Henri S, et al. Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat Immunol. 2014;15(10):929–937. This study describes the constant replenishment of macrophages in the colon to be reliant on circulating monocytes and microbiota. 10.1038/ni.2967.
39. • Ochi T, Feng Y, Kitamoto S, Nagao-Kitamoto H, Kuffa P, Atarashi K, et al. Diet-dependent, microbiota-independent regulation of IL-10-producing lamina propria macrophages in the small intestine. Sci Rep. 2016;6(1):27634. This study shows that microbiota is not necessary to induce small intestine IL-10 macrophages. 10.1038/srep27634.
40. Ueda Y, Kayama H, Jeon SG, Kusu T, Isaka Y, Rakugi H, et al. Commensal microbiota induce LPS hyporesponsiveness in colonic macrophages via the production of IL-10. Int Immunol. 2010;22(12):953–62. 10.1093/intimm/dxq449.
41. Hayashi A, Sato T, Kamada N, Mikami Y, Matsuoka K, Hisamatsu T, et al. A single strain of Clostridium butyricum induces intestinal IL-10-producing macrophages to suppress acute experimental colitis in mice. Cell Host Microbe. 2013;13(6):711–22. 10.1016/j.chom.2013.05.013.
42. •• Singh N, Gurav A, Sivaprakasam S, Brady E, Padia R, Shi H, et al. Activation of gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity. 2014;40(1):128–139. This study showed the relationship between microbial metabolite butyrate and niacin and their receptor GPR109A on colonic macrophages and dendritic cells to promote differentiation of Treg cells and IL-10-producing cells. 10.1016/j.immuni.2013.12.007.