Human gut symbiont Roseburia hominis promotes and regulates innate immunity

Frontiers in Immunology

Volumn 8, Issue SEP, 2017, Pages

  Patterson, Angela M ^a,h,i   Mulder, Imke E ^a   Travis, Anthony J ^a   Lan, Annaig ^a   Cerf Bensussan, Nadine ^b,c   Gaboriau Routhiau, Valerie ^b,c,d   Garden, Karen ^a   Logan, Elizabeth ^a   Delday, Margaret I ^a   Coutts, Alistair G P ^a   Monnais, Edouard ^a   Ferraria, Vanessa C ^a   Inoue, Ryo ^e   Grant, George ^a,f   Aminov, Rustam I ^a,g  

^a ROWETT RESEARCH INSTITUTE   (United Kingdom)

^b INSERM   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d UNIVERSITÉ PARIS SACLAY   (France)

^e KYOTO PREFECTURAL UNIVERSITY   (Japan)

^f UNIVERSITY OF ABERDEEN   (United Kingdom)

^g KAZAN FEDERAL UNIVERSITY   (Russian Federation)

^h INSTITUTE OF FOOD RESEARCH   (United Kingdom)

ⁱ UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

Flagellin; Immune tolerance; Inflammatory bowel disease; Roseburia; T lymphocytes; TLR5

Indexed keywords

FLAGELLIN; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTOME;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL METABOLISM; BACTERIUM CONJUGATION; BODY COMPOSITION; CD4+ CD25+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL MOTILITY; CHEMOTAXIS; CONTROLLED STUDY; DEXTRAN SULFATE SODIUM-INDUCED COLITIS; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; GRAM POSITIVE BACTERIUM; HISTOLOGY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IMMUNOMODULATION; INNATE IMMUNITY; INTESTINE FLORA; INTESTINE FUNCTION; MALE; MOLECULAR INTERACTION; MOUSE; NONHUMAN; ORGANISMAL INTERACTION; POLYMERASE CHAIN REACTION; ROSEBURIA HOMINIS; SATIETY; SYMBIONT; TRANSCRIPTOMICS; UPREGULATION;

EID: 85030162883     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.01166     Document Type: Article

References (44)

1. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science (2005) 308(5728):1635-8. doi:10.1126/science.1110591
2. Macpherson AJ, Hunziker L, McCoy K, Lamarre A. IgA responses in the intestinal mucosa against pathogenic and non-pathogenic microorganisms. Microbes Infect (2001) 3(12):1021-35. doi:10.1016/S1286-4579(01)01460-5
3. Macpherson AJ, Martinic MM, Harris N. The functions of mucosal T cells in containing the indigenous commensal flora of the intestine. Cell Mol Life Sci (2002) 59(12):2088-96. doi:10.1007/s000180200009
4. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell (2005) 122(1):107-18. doi:10.1016/j.cell.2005.05.007
5. Macpherson AJ. IgA adaptation to the presence of commensal bacteria in the intestine. Curr Top Microbiol Immunol (2006) 308:117-36. doi:10.1007/3-540-30657-9_5
6. Chung H, Kasper DL. Microbiota-stimulated immune mechanisms to maintain gut homeostasis. Curr Opin Immunol (2010) 22(4):455-60. doi:10.1016/j.coi.2010.06.008
7. Gaboriau-Routhiau V, Rakotobe S, Lecuyer E, Mulder I, Lan A, Bridonneau C, et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity (2009) 31(4):677-89. doi:10.1016/j.immuni.2009.08.020
8. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell (2009) 139(3):485-98. doi:10.1016/j.cell.2009.09.033
9. Geuking MB, Cahenzli J, Lawson MA, Ng DC, Slack E, Hapfelmeier S, et al. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity (2011) 34(5):794-806. doi:10.1016/j.immuni.2011.03.021
10. 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. doi:10.1126/science.1198469
11. Nutsch KM, Hsieh CS. T cell tolerance and immunity to commensal bacteria. Curr Opin Immunol (2012) 24(4):385-91. doi:10.1016/j.coi.2012.04.009
12. 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. doi:10.1126/science.1206095
13. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A (2007) 104(34):13780-5. doi:10.1073/pnas.0706625104
14. Scanlan PD, Shanahan F, Marchesi JR. Culture-independent analysis of desulfovibrios in the human distal colon of healthy, colorectal cancer and polypectomized individuals. FEMS Microbiol Ecol (2009) 69(2):213-21. doi:10.1111/j.1574-6941.2009.00709.x
15. Kang S, Denman SE, Morrison M, Yu Z, Dore J, Leclerc M, et al. Dysbiosis of fecal microbiota in Crohn's disease patients as revealed by a custom phylogenetic microarray. Inflamm Bowel Dis (2010) 16(12):2034-42. doi:10.1002/ibd.21319
16. 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 (2014) 63(8):1275-83. doi:10.1136/gutjnl-2013-304833
17. Gevers D, Kugathasan S, Denson LA, Vazquez-Baeza Y, Van Treuren W, Ren B, et al. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe (2014) 15(3):382-92. doi:10.1016/j.chom.2014.02.005
18. Hedin CR, McCarthy NE, Louis P, Farquharson FM, McCartney S, Taylor K, et al. Altered intestinal microbiota and blood T cell phenotype are shared by patients with Crohn's disease and their unaffected siblings. Gut (2014) 63(10):1578-86. doi:10.1136/gutjnl-2013-306226
19. Tilg H, Danese S. Roseburia hominis: a novel guilty player in ulcerative colitis pathogenesis? Gut (2014) 63(8):1204-5. doi:10.1136/gutjnl-2013-305799
20. 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's disease patients. Proc Natl Acad Sci U S A (2008) 105(43):16731-6. doi:10.1073/pnas.0804812105
21. Travis AJ, Kelly D, Flint HJ, Aminov RI. Complete genome sequence of the human gut symbiont Roseburia hominis. Genome Announc (2015) 3(6):e1286-1215. doi:10.1128/genomeA.01286-15
22. Duncan SH, Aminov RI, Scott KP, Louis P, Stanton TB, Flint HJ. Proposal of Roseburia faecis sp. nov., Roseburia hominis sp. nov. and Roseburia inulinivorans sp. nov., based on isolates from human faeces. Int J Syst Evol Microbiol (2006) 56(Pt 10):2437-41. doi:10.1099/ijs.0.64098-0
23. Flores-Langarica A, Marshall JL, Hitchcock J, Cook C, Jobanputra J, Bobat S, et al. Systemic flagellin immunization stimulates mucosal CD103+ dendritic cells and drives Foxp3+ regulatory T cell and IgA responses in the mesenteric lymph node. J Immunol (2012) 189(12):5745-54. doi:10.4049/jimmunol.1202283
24. Zhan T, Cao C, Li L, Gu N, Civin CI, Zhan X. MIM regulates the trafficking of bone marrow cells via modulating surface expression of CXCR4. Leukemia (2016) 30(6):1327-34. doi:10.1038/leu.2016.39
25. Berg DJ, Davidson N, Kuhn R, Muller W, Menon S, Holland G, et al. Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4(+) TH1-like responses. J Clin Invest (1996) 98(4):1010-20. doi:10.1172/JCI118861
26. Monteleone I, Platt AM, Jaensson E, Agace WW, Mowat AM. IL-10-dependent partial refractoriness to toll-like receptor stimulation modulates gut mucosal dendritic cell function. Eur J Immunol (2008) 38(6):1533-47. doi:10.1002/eji.200737909
27. Neville BA, Sheridan PO, Harris HM, Coughlan S, Flint HJ, Duncan SH, et al. Pro-inflammatory flagellin proteins of prevalent motile commensal bacteria are variably abundant in the intestinal microbiome of elderly humans. PLoS One (2013) 8(7):e68919. doi:10.1371/journal.pone.0068919
28. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature (2010) 464(7285):59-65. doi:10.1038/nature08821
29. Scott KP, Martin JC, Chassard C, Clerget M, Potrykus J, Campbell G, et al. Substrate-driven gene expression in Roseburia inulinivorans: importance of inducible enzymes in the utilization of inulin and starch. Proc Natl Acad Sci U S A (2011) 108(Suppl 1):4672-9. doi:10.1073/pnas.1000091107
30. Ukena SN, Singh A, Dringenberg U, Engelhardt R, Seidler U, Hansen W, et al. Probiotic Escherichia coli Nissle 1917 inhibits leaky gut by enhancing mucosal integrity. PLoS One (2007) 2(12):e1308. doi:10.1371/journal.pone.0001308
31. Ulluwishewa D, Anderson RC, McNabb WC, Moughan PJ, Wells JM, Roy NC. Regulation of tight junction permeability by intestinal bacteria and dietary components. J Nutr (2011) 141(5):769-76. doi:10.3945/jn.110.135657
32. Narushima S, Sugiura Y, Oshima K, Atarashi K, Hattori M, Suematsu M, et al. Characterization of the 17 strains of regulatory T cell-inducing human-derived Clostridia. Gut Microbes (2014) 5(3):333-9. doi:10.4161/gmic.28572
33. Aminov RI, Walker AW, Duncan SH, Harmsen HJ, Welling GW, Flint HJ. Molecular diversity, cultivation, and improved detection by fluorescent in situ hybridization of a dominant group of human gut bacteria related to Roseburia spp. or Eubacterium rectale. Appl Environ Microbiol (2006) 72(9):6371-6. doi:10.1128/AEM.00701-06
34. Van den Abbeele P, Belzer C, Goossens M, Kleerebezem M, De Vos WM, Thas O, et al. Butyrate-producing Clostridium cluster XIVa species specifically colonize mucins in an in vitro gut model. ISME J (2013) 7(5):949-61. doi:10.1038/ismej.2012.158
35. Juge N. Microbial adhesins to gastrointestinal mucus. Trends Microbiol (2012) 20:30-9. doi:10.1016/j.tim.2011.10.001
36. Choi YJ, Im E, Chung HK, Pothoulakis C, Rhee SH. TRIF mediates toll-like receptor 5-induced signaling in intestinal epithelial cells. J Biol Chem (2010) 285(48):37570-8. doi:10.1074/jbc. M110.158394
37. Singh V, Yeoh BS, Carvalho F, Gewirtz AT, Vijay-Kumar M. Proneness of TLR5-deficient mice to develop colitis is microbiota dependent. Gut Microbes (2015) 6(4):279-83. doi:10.1080/19490976.2015.1060390
38. Prakash T, Oshima K, Morita H, Fukuda S, Imaoka A, Kumar N, et al. Complete genome sequences of rat and mouse segmented filamentous bacteria, a potent inducer of Th17 cell differentiation. Cell Host Microbe (2011) 10(3):273-84. doi:10.1016/j.chom.2011.08.007
39. Sczesnak A, Segata N, Qin X, Gevers D, Petrosino JF, Huttenhower C, et al. The genome of Th17 cell-inducing segmented filamentous bacteria reveals extensive auxotrophy and adaptations to the intestinal environment. Cell Host Microbe (2011) 10(3):260-72. doi:10.1016/j.chom.2011.08.005
40. Yoon SI, Kurnasov O, Natarajan V, Hong M, Gudkov AV, Osterman AL, et al. Structural basis of TLR5-flagellin recognition and signaling. Science (2012) 335(6070):859-64. doi:10.1126/science.1215584
41. Crellin NK, Garcia RV, Hadisfar O, Allan SE, Steiner TS, Levings MK. Human CD4+ T cells express TLR5 and its ligand flagellin enhances the suppressive capacity and expression of FOXP3 in CD4+CD25+ T regulatory cells. J Immunol (2005) 175(12):8051-9. doi:10.4049/jimmunol.175.12.8051
42. Kinnebrew MA, Buffie CG, Diehl GE, Zenewicz LA, Leiner I, Hohl TM, et al. Interleukin 23 production by intestinal CD103(+)CD11b(+) dendritic cells in response to bacterial flagellin enhances mucosal innate immune defense. Immunity (2012) 36(2):276-87. doi:10.1016/j.immuni.2011.12.011
43. 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. doi:10.1126/science.1241165
44. 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. doi:10.1038/nature12721