Dysbiotic gut microbiota causes transmissible Crohn's disease-like ileitis independent of failure in antimicrobial defence

Gut

Volumn 65, Issue 2, 2016, Pages 225-237

  Schaubeck, Monika ^a   Clavel, Thomas ^a   Calasan, Jelena ^a   Lagkouvardos, Ilias ^a   Haange, Sven Bastiaan ^b   Jehmlich, Nico ^b   Basic, Marijana ^d   Dupont, Aline ^e   Hornef, Mathias ^e   Von Bergen, Martin ^b,c   Bleich, André ^e   Haller, Dirk ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^c AALBORG UNIVERSITY   (Denmark)

^d RWTH AACHEN UNIVERSITY   (Germany)

^e HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; LYSOZYME; METAPROTEOME; PROTEOME; RNA 16S; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL INFILTRATION; CONTROLLED STUDY; CROHN DISEASE; DISEASE ASSOCIATION; DISEASE SEVERITY; DYSBIOSIS; ESCHERICHIA COLI; GENE EXPRESSION; GENETIC ANALYSIS; GRANULOCYTE; HIGH THROUGHPUT SEQUENCING; ILEITIS; IMMUNOFLUORESCENCE; INTESTINE FLORA; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MICROBIAL COMMUNITY; MOUSE; NONHUMAN; PANETH CELL; PRIORITY JOURNAL; PROTEOMICS; RNA ANALYSIS; RNA SEQUENCE; ANIMAL; COLITIS; COMPLICATION; FLUOROIMMUNOASSAY; GERMFREE ANIMAL; INFLAMMATION; INTESTINE; MICROBIOLOGY; MICROFLORA; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; ANTI-BACTERIAL AGENTS; COLITIS; CROHN DISEASE; DYSBIOSIS; FLUOROIMMUNOASSAY; GERM-FREE LIFE; ILEITIS; INFLAMMATION; INTESTINES; MICE; MICROBIOTA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84958831500     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2015-309333     Document Type: Article

References (69)

1. Baumgart DC, Sandborn WJ. Crohn's disease. Lancet 2012;380:1590-605.
2. Ordas I, Eckmann L, Talamini M, et al. Ulcerative colitis. Lancet 2012;380:1606-19.
3. Huttenhower C, Kostic AD, Xavier RJ. Inflammatory bowel disease as a model for translating the microbiome. Immunity 2014;40:843-54.
4. Kaser A, Zeissig S, Blumberg RS. Inflammatory bowel disease. Annu Rev Immunol 2010;28:573-621.
5. Jostins L, Ripke S, Weersma RK, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 2012;491:119-24.
6. Mondot S, Barreau F, Al Nabhani Z, et al. Altered gut microbiota composition in immune-impaired Nod2(-/-) mice. Gut 2012;61:634-5.
7. Elinav E, Strowig T, Kau AL, et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 2011;145:745-57.
8. Lupp C, Robertson ML, Wickham ME, et al. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2007;2:204.
9. Frank DN, St Amand AL, Feldman RA, et al. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 2007;104:13780-5.
10. Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010;464:59-65.
11. Gevers D, Kugathasan S, Denson LA, et al. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe 2014;15:382-92.
12. Salzman NH, Hung K, Haribhai D, et al. Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 2010;11:76-83.
13. Clevers HC, Bevins CL. Paneth cells: maestros of the small intestinal crypts. Annu Rev Physiol 2013;75:289-311.
14. Wehkamp J, Salzman NH, Porter E, et al. Reduced Paneth cell alpha-defensins in ileal Crohn's disease. Proc Natl Acad Sci USA 2005;102:18129-34.
15. Sartor RB. Microbial influences in inflammatory bowel diseases. Gastroenterology 2008;134:577-94.
16. van Nood E, Vrieze A, Nieuwdorp M, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med 2013;368:407-15.
17. Angelberger S, Reinisch W, Makristathis A, et al. Temporal bacterial community dynamics vary among ulcerative colitis patients after fecal microbiota transplantation. Am J Gastroenterol 2013;108:1620-30.
18. Kump PK, Grochenig HP, Lackner S, et al. Alteration of intestinal dysbiosis by fecal microbiota transplantation does not induce remission in patients with chronic active ulcerative colitis. Inflamm Bowel Dis 2013;19:2155-65.
19. Cui B, Feng Q, Wang H, et al. Fecal microbiota transplantation through mid-gut for refractory Crohn's disease: Safety, feasibility and efficacy trial results. J Gastroenterol Hepatol 2015;30:51-8.
20. Madsen KL, Doyle JS, Tavernini MM, et al. Antibiotic therapy attenuates colitis in interleukin 10 gene-deficient mice. Gastroenterology 2000;118:1094-105.
21. Kim SC, Tonkonogy SL, Albright CA, et al. Variable phenotypes of enterocolitis in interleukin 10-deficient mice monoassociated with two different commensal bacteria. Gastroenterology 2005;128:891-906.
22. Steck N, Hoffmann M, Sava IG, et al. Enterococcus faecalis metalloprotease compromises epithelial barrier and contributes to intestinal inflammation. Gastroenterology 2011;141:959-71.
23. Rath HC, Herfarth HH, Ikeda JS, et al. Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats. J Clin Invest 1996;98:945-53.
24. Kontoyiannis D, Pasparakis M, Pizarro TT, et al. Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies. Immunity 1999;10:387-98.
25. Werner T, Wagner SJ, Martinez I, et al. Depletion of luminal iron alters the gut microbiota and prevents Crohn's disease-like ileitis. Gut 2011;60:325-33.
26. Erben U, Loddenkemper C, Doerfel K, et al. A guide to histomorphological evaluation of intestinal inflammation in mouse models. Int J Clin Exp Pathol 2014;7:4557-76.
27. Katakura K, Lee J, Rachmilewitz D, et al. Toll-like receptor 9-induced type I IFN protects mice from experimental colitis. J Clin Invest 2005;115:695-702.
28. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25:402-8.
29. Baur P, Martin FP, Gruber L, et al. Metabolic phenotyping of the Crohn's disease-like IBD etiopathology in the TNF(DeltaARE/WT) mouse model. J Proteome Res 2011;10:5523-35.
30. Mahler Convenor M, Berard M, Feinstein R, et al. FELASA recommendations for the health monitoring of mouse, rat, hamster, guinea pig and rabbit colonies in breeding and experimental units. Lab Anim 2014;48:178-92.
31. Moghadamrad S, McCoy KD, Geuking MB, et al. Attenuated portal hypertension in germ-free mice: Function of bacterial flora on the development of mesenteric lymphatic and blood vessels. Hepatology 2015. doi:10.1002/hep.27698
32. Inoue R, Tsuruta T, Nojima I, et al. Postnatal changes in the expression of genes for cryptdins 1-6 and the role of luminal bacteria in cryptdin gene expression in mouse small intestine. FEMS Immunol Med Microbiol 2008;52:407-16.
33. Boudeau J, Glasser AL, Masseret E, et al. Invasive ability of an Escherichia coli strain isolated from the ileal mucosa of a patient with Crohn's disease. Infect Immun 1999;67:4499-509.
34. Conte MP, Longhi C, Marazzato M, et al. Adherent-invasive Escherichia coli (AIEC) in pediatric Crohn's disease patients: phenotypic and genetic pathogenic features. BMC Res Notes 2014;7:748.
35. Sellon RK, Tonkonogy S, Schultz M, et al. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun 1998;66:5224-31.
36. 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.
37. Bamias G, Okazawa A, Rivera-Nieves J, et al. Commensal bacteria exacerbate intestinal inflammation but are not essential for the development of murine ileitis. J Immunol 2007;178:1809-18.
38. Matsumoto S, Okabe Y, Setoyama H, et al. Inflammatory bowel disease-like enteritis and caecitis in a senescence accelerated mouse P1/Yit strain. Gut 1998;43:71-8.
39. Bamias G, Dahman MI, Arseneau KO, et al. Intestinal-specific TNFalpha overexpression induces Crohn's-like ileitis in mice. PLoS One 2013;8:e72594.
40. Couturier-Maillard A, Secher T, Rehman A, et al. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J Clin Invest 2013;123:700-11.
41. Bloom SM, Bijanki VN, Nava GM, et al. Commensal Bacteroides species induce colitis in host-genotype-specific fashion in a mouse model of inflammatory bowel disease. Cell Host Microbe 2011;9:390-403.
42. Flavell RA. Commensal Bacteroides species induce colitis in host-genotype-specific fashion in a mouse model of inflammatory bowel disease. Cell 2011;9:390-403.
43. Scribano ML, Prantera C. Antibiotics and inflammatory bowel diseases. Dig Dis 2013;31:379-84.
44. Khan KJ, Ullman TA, Ford AC, et al. Antibiotic therapy in inflammatory bowel disease: a systematic review and meta-analysis. Am J Gastroenterol 2011;106:661-73.
45. Ghouri YA, Richards DM, Rahimi EF, et al. Systematic review of randomized controlled trials of probiotics, prebiotics, and synbiotics in inflammatory bowel disease. Clin Exp Gastroenterol 2014;7:473-87.
46. Cadwell K, Liu JY, Brown SL, et al. A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 2008;456:259-63.
47. Wehkamp J, Koslowski M, Wang G, et al. Barrier dysfunction due to distinct defensin deficiencies in small intestinal and colonic Crohn's disease. Mucosal Immunol 2008;1(Suppl 1):S67-74.
48. Bevins CL, Salzman NH. Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat Rev Microbiol 2011;9:356-68.
49. Cunliffe RN, Rose FR, Keyte J, et al. Human defensin 5 is stored in precursor form in normal Paneth cells and is expressed by some villous epithelial cells and by metaplastic Paneth cells in the colon in inflammatory bowel disease. Gut 2001;48:176-85.
50. Adolph TE, Tomczak MF, Niederreiter L, et al. Paneth cells as a site of origin for intestinal inflammation. Nature 2013;503:272-6.
51. Kaser A, Lee AH, Franke A, et al. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 2008;134:743-56.
52. Gunther C, Martini E, Wittkopf N, et al. Caspase-8 regulates TNF-alpha-induced epithelial necroptosis and terminal ileitis. Nature 2011;477:335-9.
53. Garabedian EM, Roberts LJ, McNevin MS, et al. Examining the role of Paneth cells in the small intestine by lineage ablation in transgenic mice. J Biol Chem 1997;272:23729-40.
54. Farin HF, Karthaus WR, Kujala P, et al. Paneth cell extrusion and release of antimicrobial products is directly controlled by immune cell-derived IFN-gamma. J Exp Med 2014;211:1393-405.
55. Manichanh C, Rigottier-Gois L, Bonnaud E, et al. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut 2006;55:205-11.
56. Perez-Munoz ME, Bergstrom K, Peng V, et al. Discordance between changes in the gut microbiota and pathogenicity in a mouse model of spontaneous colitis. Gut Microbes 2014;5:286-95.
57. Morgan XC, Tickle TL, Sokol H, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 2012;13:R79.
58. Pickard JM, Maurice CF, Kinnebrew MA, et al. Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature 2014;514:638-41.
59. Rausch P, Rehman A, Kunzel S, et al. Colonic mucosa-associated microbiota is influenced by an interaction of Crohn disease and FUT2 (Secretor) genotype. Proc Natl Acad Sci USA 2011;108:19030-5.
60. McGovern DP, Jones MR, Taylor KD, et al. Fucosyltransferase 2 (FUT2) non-secretor status is associated with Crohn's disease. Hum Mol Genet 2010;19:3468-76.
61. 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.
62. Powell N, Walker AW, Stolarczyk E, et al. The transcription factor T-bet regulates intestinal inflammation mediated by interleukin-7 receptor+ innate lymphoid cells. Immunity 2012;37:674-84.
63. Kaur S, Yawar M, Kumar PA, et al. Hungatella effluvii gen. nov., sp. nov., an obligately anaerobic bacterium isolated from an effluent treatment plant, and reclassification of Clostridium hathewayi as Hungatella hathewayi gen. nov., comb. nov. Int J Syst Evol Microbiol 2014;64(Pt 3):710-18.
64. Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 2008;453:620-5.
65. von Schillde MA, Hormannsperger G, Weiher M, et al. Lactocepin secreted by Lactobacillus exerts anti-inflammatory effects by selectively degrading proinflammatory chemokines. Cell Host Microbe 2012;11:387-96.
66. Devkota S, Wang Y, Musch MW, et al. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/-mice. Nature 2012;487:104-8.
67. Carvalho FA, Barnich N, Sivignon A, et al. Crohn's disease adherent-invasive Escherichia coli colonize and induce strong gut inflammation in transgenic mice expressing human CEACAM. J Exp Med 2009;206:2179-89.
68. Darfeuille-Michaud A, Boudeau J, Bulois P, et al. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology 2004;127:412-21.
69. Hemmerling J, Heller K, Hormannsperger G, et al. Fetal exposure to maternal inflammation does not affect postnatal development of genetically-driven ileitis and colitis. PLoS One 2014;9:e98237.