Microbiota-specific CD4CD8αα Tregs: Role in intestinal immune homeostasis and implications for IBD

Frontiers in Immunology

Volumn 6, Issue OCT, 2015, Pages

  Sarrabayrouse, Guillaume ^a   Alameddine, Joudy ^b,c,d   Altare, Frédéric ^b,c,d   Jotereau, Francine ^b,c,d  

^a HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^b INSERM   (France)

^c UNIVERSITÉ DE NANTES   (France)

^d CNRS   (France)

Author keywords

Faecalibacterium prausnitzii; IBD; Inflammation; Microbiota; Tregs

Indexed keywords

CD8ALPHA ANTIGEN; CHEMOKINE RECEPTOR CCR9; DIPEPTIDYL PEPTIDASE; INTERLEUKIN 10; INTERLEUKIN 12; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; CD4 CD8 RATIO; CD4+ T LYMPHOCYTE; CLOSTRIDIUM; FAECALIBACTERIUM PRAUSNITZII; HOMEOSTASIS; HUMAN; IMMUNITY; INFLAMMATORY BOWEL DISEASE; INTESTINAL IMMUNITY; MICROFLORA; POLYENDOCRINOPATHY; REGULATORY T LYMPHOCYTE; ULCERATIVE COLITIS;

EID: 84949558129     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00522     Document Type: Article

References (50)

1. Josefowicz SZ, Lu LF, Rudensky AY. Regulatory T cells: mechanisms of differentiation and function. Annu Rev Immunol (2007) 30:531-64. doi:10.1146/annurev.immunol.25.022106.141623
2. Abbas AK, Benoist C, Bluestone JA, Campbell DJ, Ghosh S, Hori S, et al. Regulatory T cells: recommendations to simplify the nomenclature. Nat Immunol (2013) 14:307-8. doi:10.1038/ni.2554
3. Shevach EM, Thornton AM. tTregs, pTregs, and iTregs: similarities and differences. Immunol Rev (2014) 259:88-102. doi:10.1111/imr.12160
4. Weissler KA, Caton AJ. The role of T-cell receptor recognition of peptide:MHC complexes in the formation and activity of Foxp3(+) regulatory T cells. Immunol Rev (2014) 259:11-22. doi:10.1111/imr.12177
5. Wieczorek G, Asemissen A, Model F, Turbachova I, Gloess S, Liebenberg V, et al. Quantitative DNA methylation analysis of FOXP3 as a new method for counting regulatory cells in peripheral blood and solid tissue. Cancer Res (2009) 15:599-608. doi:10.1158/0008-5472.CAN-08-2361
6. Yadav M, Stephan S, Bluestone JA. Peripherally induced tregs - role in immune homeostasis and autoimmunity. Front Immunol (2013) 4:232. doi:10.3389/fimmu.2013.00232
7. Maynard CL, Harrington LE, Janowski KM, Oliver JR, Zindl CL, Rudensky AY, et al. Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3- precursor cells in the absence of interleukin 10. Nat Immunol (2007) 8:931-41. doi:10.1038/ni1504
8. + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature (1997) 389:737-42. doi:10.1038/39614
9. Gregori S, Goudy KS, Roncarolo MG. The cellular and molecular mechanisms of immuno-suppression by human type 1 regulatory T cells. Front Immunol (2012) 3:30. doi:10.3389/fimmu.2012.00030
10. Roncarolo MG, Gregori S, Bacchetta R, Battaglia M. Tr1 cells and the counter-regulation of immunity: natural mechanisms and therapeutic applications. Curr Top Microbiol Immunol (2014) 380:39-68. doi:10.1007/978-3-662-43492-5_3
11. Chen Y, Kuchroo VK, Inobe J, Hafler DA, Weiner HL. Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science (1994) 265:1237-40. doi:10.1126/science.7520605
12. Ochi H, Abraham M, Ishikawa H, Frenkel D, Yang K, Basso AS, et al. Oral CD3-specific antibody suppresses autoimmune encephalomyelitis by inducing CD4+ CD25- LAP+ T cells. Nat Med (2006) 12:627-35. doi:10.1038/nm1408
13. Awasthi A, Carrier Y, Peron JP, Bettelli E, Kamanaka M, Flavell RA, et al. A dominant function for interleukin 27 in generating interleukin 10-producing anti-inflammatory T cells. Nat Immunol (2007) 8:1380-9. doi:10.1038/ni1541
14. Hawrylowicz CM, O'Garra A. Potential role of interleukin-10-secreting regulatory T cells in allergy and asthma. Nat Rev Immunol (2005) 5:271-83. doi:10.1038/nri1589
15. Magnani CF, Alberigo G, Bacchetta R, Serafini G, Andreani M, Roncarolo MG, et al. Killing of myeloid APCs via HLA class I, CD2 and CD226 defines a novel mechanism of suppression by human Tr1 cells. Eur J Immunol (2011) 6:1652-62. doi:10.1002/eji.201041120
16. Gandhi R, Farez MF, Wang Y, Kozoriz D, Quintana FJ, Weiner HL. Cutting edge: human latency-associated peptide+ T cells: a novel regulatory T cell subset. J Immunol (2010) 184:4620-4. doi:10.4049/jimmunol.0903329
17. 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. doi:10.1126/science.1198469
18. Kugelberg E. Mucosal immunology: bacteria get T(Reg) cells into shape. Nat Rev Immunol (2014) 14:2-3. doi:10.1038/nri3794
19. Maul J, Loddenkemper C, Mundt P, Berg E, Giese T, Stallmach A, et al. Peripheral and intestinal regulatory CD4+ CD25(high) T cells in inflammatory bowel disease. Gastroenterology (2005) 128:1868-78. doi:10.1053/j.gastro.2005.03.043
20. Buckner JH. Mechanisms of impaired regulation by CD4(+)CD25(+)FOXP3(+) regulatory T cells in human autoimmune diseases. Nat Rev Immunol (2010) 10:849-59. doi:10.1038/nri2889
21. Tanoue T, Honda K. Induction of Treg cells in the mouse colonic mucosa: a central mechanism to maintain host-microbiota homeostasis. Semin Immunol (2012) 24:50-7. doi:10.1016/j.smim.2011.11.009
22. MacDonald TT, Monteleone I, Fantini MC, Monteleone G. Regulation of homeostasis and inflammation in the intestine. Gastroenterology (2011) 140:1768-75. doi:10.1053/j.gastro.2011.02.047
23. Sarrabayrouse G, Bossard C, Chauvin JM, Jarry A, Meurette G, Quevrain E, et al. CD4CD8alphaalpha lymphocytes, a novel human regulatory T cell subset induced by colonic bacteria and deficient in patients with inflammatory bowel disease. PLoS Biol (2014) 12:e1001833. doi:10.1371/journal.pbio.1001833
24. 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. doi:10.1038/nature12331
25. Goto Y, Panea C, Nakato G, Cebula A, Lee C, Diez MG, et al. Segmented filamentous bacteria antigens presented by intestinal dendritic cells drive mucosal Th17 cell differentiation. Immunity (2014) 40:594-607. doi:10.1016/j.immuni.2014.03.005
26. Hold GL, Schwiertz A, Aminov RI, Blaut M, Flint HL. Oligonucleotide probes that detect quantitatively significant groups of butyrate-producing bacteria in human feces. Appl Environ Microbiol (2003) 7:4320-4. doi:10.1128/AEM.69.7.4320-4324.2003
27. Miquel S, Martin R, Rossi O, Bermudez-Humaran LG, Chatel JM, Sokol H, et al. Faecalibacterium prausnitzii and human intestinal health. Curr Opin Microbiol (2013) 16:255-61. doi:10.1016/j.mib.2013.06.003
28. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A (2008) 105:16731-6. doi:10.1073/pnas.0804812105
29. Willing B, Halfvarson J, Dicksved J, Rosenquist M, Jarnerot G, Engstrand L, et al. Twin studies reveal specific imbalances in the mucosa-associated microbiota of patients with ileal Crohn's disease. Inflamm Bowel Dis (2009) 15:653-60. doi:10.1002/ibd.20783
30. Manichanh C, Borruel N, Casellas F, Guarner F. The gut microbiota in IBD. Nat Rev Gastroenterol Hepatol (2012) 9:599-608. doi:10.1038/nrgastro.2012.152
31. Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, Beaugerie L, et al. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis (2009) 15:1183-9. doi:10.1002/ibd.20903
32. Machiels K, Joossens M, Sabino J, De Preter V, Arijs I, Eeckhaut V, et al. A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut (2013) 63:1275-83. doi:10.1136/gutjnl-2013-304833
33. Martin R, Chain F, Miquel S, Lu J, Gratadoux JJ, Sokol H, et al. The commensal bacterium Faecalibacterium prausnitzii is protective in DNBS-induced chronic moderate and severe colitis model. Inflamm Bowel Dis (2014) 20:417-30. doi:10.1097/01.MIB.0000440815.76627.64
34. Quévrain E, Maubert MA, Michon C, Chain F, Marquant R, Tailhades J, et al. Identification of an anti-inflammatory protein from Faecalibacterium prausnitzii, a commensal bacterium deficient in Crohn's disease. Gut (2015). doi:10.1136/gutjnl-2014-307649
35. Gagliani N, Magnani CF, Huber S, Gianolini ME, Pala M, Licona-Limon P, et al. Coexpression of CD49b and LAG-3 identifies human and mouse T regulatory type 1 cells. Nat Med (2013) 19:739-46. doi:10.1038/nm.3179
36. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol (2003) 4:330-6. doi:10.1038/ni904
37. Arvey A, van der Veeken J, Samstein RM, Feng Y, Stamatoyannopoulos JA, Rudensky AY. Inflammation-induced repression of chromatin bound by the transcription factor Foxp3 in regulatory T cells. Nat Immunol (2007) 15:580-7. doi:10.1038/ni.2868
38. +CD8 alpha alpha T cells in the intestinal epithelial layer in the prevention of inflammatory bowel disease. Proc Natl Acad Sci U S A (2003) 100:5324-9. doi:10.1073/pnas.0831037100
39. Mowat AM, Agace WW. Regional specialization within the intestinal immune system. Nat Rev Immunol (2014) 14:667-85. doi:10.1038/nri3738
40. Chung H, Pamp SJ, Hill JA, Surana NK, Edelman SM, Troy EB, et al. Gut immune maturation depends on colonization with a host-specific microbiota. Cell (2012) 149:1578-93. doi:10.1016/j.cell.2012.04.037
41. Patey-Mariaud de Serre N, Canioni D, Ganousse S, Rieux-Laucat F, Goulet O, Ruemmele F, et al. Digestive histopathological presentation of IPEX syndrome. Mod Pathol (2009) 22:95-102. doi:10.1038/modpathol.2008.161
42. + T-cell clones. Nature (1988) 335:642-4. doi:10.1038/335642a0
43. Rybakin V, Clamme JP, Ampudia J, Yachi PP, Gascoigne NR. CD8alphaalpha and -alphabeta isotypes are equally recruited to the immunological synapse through their ability to bind to MHC class I. EMBO Rep (2011) 12:1251-6. doi:10.1038/embor.2011.209
44. Leishman AJ, Naidenko OV, Attinger A, Koning F, Lena CJ, Xiong Y, et al. T cell responses modulated through interaction between CD8alphaalpha and the nonclassical MHC class I molecule, TL. Science (2001) 294:1936-9. doi:10.1126/science.1063564
45. Campbell NA, Park MS, Toy LS, Yio XY, Devine L, Kavathas P, et al. A non-class I MHC intestinal epithelial surface glycoprotein, gp180, binds to CD8. Clin Immunol (2002) 102:267-74. doi:10.1006/clim.2001.5170
46. Roda G, Jianyu X, Park MS, DeMarte L, Hovhannisyan Z, Couri R, et al. Characterizing CEACAM5 interaction with CD8alpha and CD1d in intestinal homeostasis. Mucosal Immunol (2014) 7:615-24. doi:10.1038/mi.2013.80
47. Allez M, Brimnes J, Shao L, Dotan I, Nakazawa A, Mayer L. Activation of a unique population of CD8(+) T cells by intestinal epithelial cells. Ann N Y Acad Sci (2004) 1029:22-35. doi:10.1196/annals.1309.004
48. Huang Y, Park Y, Wang-Zhu Y, Larange A, Arens R, Bernardo I, et al. Mucosal memory CD8(+) T cells are selected in the periphery by an MHC class I molecule. Nat Immunol (2011) 12:1086-95. doi:10.1038/ni.2106
49. Levine AG, Arvey A, Jin W, Rudensky AY. Continuous requirement for the TCR in regulatory T cell function. Nat Immunol (2010) 15:1070-8. doi:10.1038/ni.3004
50. Kawamoto S, Maruya M, Kato LM, Suda W, Atarashi K, Doi Y, et al. Foxp3(+) T cells regulate immunoglobulinA selection and facilitate diversification of bacterial species responsible for immune homeostasis. Immunity (2014) 41:152-65. doi:10.1016/j.immuni.2014.05.016