Role of microbiota in postnatal maturation of intestinal T-cell responses

Current Opinion in Gastroenterology

Volumn 27, Issue 6, 2011, Pages 502-508

  Gaboriau Routhiau, Valérie ^a,b   Lécuyer, Emelyne ^a,b   Cerf Bensussan, Nadine ^a,b  

^a INSERM   (France)

^b UMR1319 MICALIS   (France)

Author keywords

gut immune system; intestinal T cells; microbiota

Indexed keywords

CYCLOOXYGENASE 2; GAMMA INTERFERON; IMMUNOGLOBULIN A; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR; INTERLEUKIN 17; INTERLEUKIN 22; INTERLEUKIN 3; INTERLEUKIN 4; MYELOID DIFFERENTIATION FACTOR 88; PROBIOTIC AGENT; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ATOPIC DERMATITIS; BIFIDOBACTERIUM BIFIDUM; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COLITIS; COLON MUCOSA; CYTOKINE RELEASE; HUMAN; INTESTINE FLORA; LACTOBACILLUS; LAMINA PROPRIA; NONHUMAN; PROTEIN EXPRESSION; REVIEW; STREPTOCOCCUS THERMOPHILUS; SYMBIONT; T LYMPHOCYTE;

HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, MUCOSAL; INTESTINAL MUCOSA; METAGENOME; T-LYMPHOCYTES;

EID: 80054680603     PISSN: 02671379     EISSN: 15317056     Source Type: Journal    
DOI: 10.1097/MOG.0b013e32834bb82b     Document Type: Review

References (58)

1. Hooper LV, Macpherson AJ. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol 2010;10:159-169.
2. Mora JR, von Andrian UH. Differentiation and homing of IgA-secreting cells. Mucosal Immunol 2008;1:96-109.
3. Sigmundsdottir H, Butcher EC. Environmental cues, dendritic cells and the programming of tissue-selective lymphocyte trafficking. Nat Immunol 2008;9:981-987.
4. Bouskra D, Brezillon C, Berard M, et al. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 2008;456:507-510. (Pubitemid 352759006)
5. Guy-Grand D, Griscelli C, Vassalli P. Gut-associated lymphoblasts and intestinal IgA plasma cells. Adv Exp Med Biol 1974;45:41-46.
6. Macpherson AJ, Harris NL. Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 2004;4:478-485. (Pubitemid 38745559)
7. Umesaki Y, Okada Y, Matsumoto S, et al. Segmented filamentous bacteria are indigenous intestinal bacteria that activate intraepithelial lymphocytes and induce MHC class II molecules and fucosyl asialo GM1 glycolipids on the small intestinal epithelial cells in the ex-germ-free mouse. Microbiol Immunol 1995;39:555-562.
8. Umesaki Y, Setoyama H, Matsumoto S, et al. Differential roles of segmented filamentous bacteria and clostridia in development of the intestinal immune system. Infect Immun 1999;67:3504-3511. (Pubitemid 29291522)
9. Gaboriau-Routhiau V, Rakotobe S, Lecuyer E, et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 2009;31:677-689.
10. Geuking MB, Cahenzli J, Lawson MA, et al. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity 2011;34:794-806. This elegant study shows that the induction of colonic lamina propria Tregs in mice colonized by ASF prevents inflammatory Th17 and Th1 responses. The latter responses are uncovered when mice are treated with a blocking anti-IL-10 antibody. These experimental data illustrate the critical role of IL-10 in the control of host immune responses to the microbiota.
11. Duan J, Chung H, Troy E, Kasper DL. Microbial colonization drives expansion of IL-1 receptor 1-expressing and IL-17-producing gamma/delta T cells. Cell Host Microbe 2010;7:140-150.
12. Lochner M, Berard M, Sawa S, et al. Restricted microbiota and absence of cognate TCR antigen leads to an unbalanced generation of Th17 cells. J Immunol 2011;186:1531-1537.
13. Spits H, Di Santo JP. The expanding family of innate lymphoid cells, regulators and effectors of immunity and tissue remodeling. Nat Immunol 2011;12:21-27.
14. Maloy KJ, Powrie F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 2011;474:298-306.
15. Cerf-Bensussan N, Gaboriau-Routhiau V. The immune system and the gut microbiota: friends or foes? Nat Rev Immunol 2010;10:735-744.
16. De Filippo C, Cavalieri D, Di Paola M, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 2010;107:14691-14696. Along with [17"], this work demonstrated the considerable impact of the diet in shaping gut microbial communities and how it can induce rapid shifts in its composition. Major differences were observed in microbiota composition between European children and children living in a rural part of Africa who eat a traditional fiber-rich diet.
17. Faith JJ, McNulty NP, et al. Predicting a human gut microbiota's response to diet in gnotobiotic mice. Science 2011;333:101-104. Using gnotobiotic mice harboring a 10-member community of sequenced human gut bacteria, the authors test a mathematical model and predict how different ingredients of the diet can influence the composition of the microbiota. These data illustrate the major impact of the diet on the structure of the intestinal microbiota and the possibility to influence this composition by changing the diet.
18. Dominguez-Bello MG, Costello EK, Contreras M, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA 2010;107:11971-11975.
19. Atarashi K, Tanoue T, Shima T, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011;331:337-341. The authors showed that colonization by a cocktail of 46 Clostridium strains induces the accumulation of Tregs producing IL-10 in the colonic lamina propria and can protect against colitis and allergic peripheral sensitization.
20. Hadis U, Wahl B, Schulz O, et al. Intestinal tolerance requires gut homing and expansion of FoxP3+ regulatory T cells in the lamina propria. Immunity 2011;34:237-246. This elegant study describes the induction of iTregs that mediate tolerance to dietary ovalbumin (OVA). It shows that CD103+ dendritic cells loaded with OVA migrate toward MLNsand induce iTregs that home into the intestinal lamina propria in which they expand and then disseminate to the periphery. Depletion experiments confirm the central role of Tregs in tolerance to OVA.
21. Zheng Y, Josefowicz S, Chaudhry A, et al. Role of conserved noncoding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature 2010;463:808-812.
22. Begue B, Verdier J, Rieux-Laucat F, et al. Defective IL10 signaling defining a subgroup of patients with inflammatory bowel disease. Am J Gastroenterol 2011;106:1544-1555.
23. Glocker EO, Kotlarz D, Boztug K, et al. Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N Engl J Med 2009;361:2033-2045.
24. Maynard CL, Weaver CT. Diversity in the contribution of interleukin-10 to T-cell-mediated immune regulation. Immunol Rev 2008;226:219-233.
25. + Tregs activated by IL-10 downmodulate Th17 cell responses.
26. Huber S, Gagliani N, Esplugues E, et al. Th17 cells express interleukin-10 receptor and are controlled by Foxp3 and Foxp3+ regulatory CD4+ T cells in an interleukin-10-dependent manner. Immunity 2011;34:554-565. This article provides complementary data, showing that Th17 cells express IL-1 0R and can be directly inhibited by IL-10.
27. Cong Y, Feng T, Fujihashi K, et al. A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota. Proc Natl Acad Sci USA 2009;106:19256-19261.
28. Tsuji M, Komatsu N, Kawamoto S, et al. Preferential generation of follicular B helper T cells from Foxp3+ T cells in gut Peyer's patches. Science 2009;323:1488-1492.
29. Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 2008;453:620-625. (Pubitemid 351769307)
30. Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci USA 2010;107:12204-12209.
31. Round JL, Lee SM, Li J, et al. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 2011;332:974-977. This article shows that B. fragilis PSA can bind TLR2 on Tregs and stimulate their regulatory properties.
32. Grangette C, Nutten S, Palumbo E, et al. Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. Proc Natl Acad Sci USA 2005;102:10321-10326. (Pubitemid 41023369)
33. Kwon HK, Lee CG, So JS, et al. Generation of regulatory dendritic cells and CD4+Foxp3+ T cells by probiotics administration suppresses immune disorders. Proc Natl Acad Sci USA 2010;107:2159-2164. This study provides evidence that in-vitro screening can help to select probiotic strains with potent immunoregulatory properties.
34. Maslowski KM, Vieira AT, Ng A, et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 2009;461:1282-1286.
35. Tannock GW, Miller JR, Savage DC. Host specificity of filamentous, segmented microorganisms adherent to the small bowel epithelium in mice and rats. Appl Environ Microbiol 1984;47:441-442. (Pubitemid 14185010)
36. Talham GL, Jiang HQ, Bos NA, Cebra JJ. Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the murine gut mucosal immune system. Infect Immun 1999;67:1992-2000. (Pubitemid 29144426)
37. Ivanov II, Atarashi K, Manel N, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009;139:485-498.
38. Davis CP, Savage DC. Habitat, succession, attachment, and morphology of segmented, filamentous microbes indigenous to the murine gastrointestinal tract. Infect Immun 1974;10:948-956.
39. Klaasen HL, Koopman JP, Van den Brink ME, et al. Intestinal, segmented, filamentous bacteria in a wide range of vertebrate species. Lab Anim (NY) 1993;27:141-150. (Pubitemid 23104423)
40. Snel J, Heinen PP, Blok HJ, et al. Comparison of 16S rRNA sequences of segmented filamentous bacteria isolated from mice, rats, and chickens and proposal of 'Candidatus Arthromitus'. Int J Syst Bacteriol 1995;45:780-782.
41. Atarashi K, Nishimura J, Shima T, et al. ATP drives lamina propria T (H) 17 cell differentiation. Nature 2008;455:808-812.
42. Iwase T, Shinji H, Tajima A, et al. Isolation and identification of ATP-secreting bacteria from mice and humans. J Clin Microbiol 2010;48:1949-1951. This study suggests that ATP-producing strains may be infrequent in the mouse and human microbiota and rather pathogenic bacteria.
43. Chow J, Mazmanian SK. A pathobiont of the microbiota balances host colonization and intestinal inflammation. Cell Host Microbe 2010;7:265-276.
44. Polk DB, Peek RM Jr. Helicobacter pylori: gastric cancer and beyond. Nat Rev Cancer 2010;10:403-414.
45. Tenaillon O, Skurnik D, Picard B, Denamur E. The population genetics of commensal Escherichia coli. Nat Rev Microbiol 2010;8:207-217.
46. Nenci A, Becker C, Wullaert A, et al. Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature 2007;446:557-561. (Pubitemid 46514732)
47. Dupaul-Chicoine J, Yeretssian G, Doiron K, et al. Control of intestinal homeostasis, colitis, and colitis-associated colorectal cancer by the inflammatory caspases. Immunity 2010;32:367-378.
48. Elinav E, Strowig T, Kau AL, et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 2011;145:745-757.
49. Carvalho FA, Barnich N, Sivignon A, et al. Crohn's disease adherentinvasive Escherichia coli colonize and induce strong gut inflammation in transgenic mice expressing human CEACAM. J Exp Med 2009;206:2179-2189.
50. Barnich N, Carvalho FA, Glasser AL, et al. CEACAM6 acts as a receptor for adherent-invasive E. coli, supporting ileal mucosa colonization in Crohn disease. J Clin Invest 2007;117:1566-1574. (Pubitemid 46871341)
51. Stecher B, Robbiani R, Walker AW, et al. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol 2007;5:2177-2189. (Pubitemid 350035420)
52. Garrett WS, Lord GM, Punit S, et al. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell 2007;131:33-45. (Pubitemid 47505255)
53. Garrett WS, Punit S, Gallini CA, et al. Colitis-associated colorectal cancer driven by T-bet deficiency in dendritic cells. Cancer Cell 2009;16:208-219.
54. Garrett WS, Gallini CA, Yatsunenko T, et al. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe 2010;8:292-300.
55. Sokol H, Pigneur B, Watterlot L, et al. Faecalibacterium prausnitzii is an antiinflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 2008;105:16731-16736.
56. Sokol H, Seksik P, Furet JP, et al. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis 2009;15:1183-1189.
57. Darfeuille-Michaud A, Boudeau J, Bulois P, et al. High prevalence of adherentinvasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology 2004;127:412-421. (Pubitemid 39091889)
58. Veiga P, Gallini CA, Beal C, et al. Bifidobacterium animalis subsp. lactis fermented milk product reduces inflammation by altering a niche for colitogenic microbes. Proc Natl Acad Sci USA 2010;107:18132-18137.