Crohn's disease-associated Escherichia coli LF82 aggravates colitis in injured mouse colon via signaling by flagellin

Inflammatory Bowel Diseases

Volumn 14, Issue 8, 2008, Pages 1051-1060

  Carvalho, Frédéric A ^a   Barnich, Nicolas ^a,b   Sauvanet, Pierre ^a   Darcha, Claude ^c   Gelot, Agathe ^b,d   Darfeuille Michaud, Arlette ^a,b  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b Institut Universitaire de Technologie en Genie Biologique   (France)

^c HÔTEL DIEU   (France)

^d INSERM   (France)

Author keywords

Adherent invasive E. coli; Crohn's disease; Flagellin receptor; Mouse model

Indexed keywords

CYTOKINE; CYTOSOL RECEPTOR; DEXTRAN SULFATE; FLAGELLIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; MEMBRANE RECEPTOR; MYELOPEROXIDASE; TOLL LIKE RECEPTOR 5;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM MUTANT; BAGG ALBINO MOUSE; COLITIS; COLON; COLON INJURY; CONTROLLED STUDY; CROHN DISEASE; DISEASE ACTIVITY; DISEASE EXACERBATION; DISEASE SEVERITY; ENZYME ACTIVITY; ESCHERICHIA COLI; HISTOPATHOLOGY; MALE; MOUSE; MUCOSA INFLAMMATION; MUCOSAL IMMUNITY; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RECTUM HEMORRHAGE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCORING SYSTEM; SIGNAL TRANSDUCTION; SURVIVAL RATE; WEIGHT REDUCTION;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; CALCIUM-BINDING PROTEINS; COLITIS; CROHN DISEASE; DISEASE MODELS, ANIMAL; ESCHERICHIA COLI; FLAGELLIN; GENE EXPRESSION; GENE EXPRESSION REGULATION, BACTERIAL; INTESTINAL MUCOSA; MICE; MICE, INBRED BALB C; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEVERITY OF ILLNESS INDEX; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 5;

EID: 49749149169     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1002/ibd.20423     Document Type: Article

References (42)

1. Bouma G, Strober W. The immunological and genetic basis of inflammatory bowel disease. Nat Rev Immunol. 2003;3:521-533.
2. Podolsky DK. Inflammatory bowel disease. N Engl J Med. 2002;347: 417-429.
3. Sartor RB. Pathogenesis and immune mechanisms of chronic inflammatory bowel diseases. Am J Gastroenterol. 1997;92:5S-11S.
4. Sartor RB. Intestinal microflora in human and experimental inflammatory bowel disease. Curr Opin Gastroenterol. 2001;17:324-330.
5. Shanahan F. Host-flora interactions in inflammatory bowel disease. Inflamm Bowel Dis. 2004;10(Suppl 1):S16-24.
6. Farrell RJ, LaMont JT. Microbial factors in inflammatory bowel disease. Gastroenterol Clin North Am. 2002;31:41-62.
7. 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;67:4499-4509.
8. Abraham C, Cho JH. Bugging of the intestinal mucosa. N Engl J Med. 2007;357:708-710.
9. 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;17:1566-1574.
10. Boudeau J, Barnich N, Darfeuille-Michaud A. Type 1 pili-mediated adherence of Escherichia coli strain LF82 isolated from Crohn's disease is involved in bacterial invasion of intestinal epithelial cells. Mol Microbiol. 2001;39:1272-1284.
11. Lodes MJ, Cong Y, Elson CO, et al. Bacterial flagellin is a dominant antigen in Crohn disease. J Clin Invest. 2004;113:1296-1306.
12. Arnott ID, Landers CJ, Nimmo EJ, et al. Sero-reactivity to microbial components in Crohn's disease is associated with disease severity and progression, but not NOD2/CARD15 genotype. Am J Gastroenterol. 2004;99:2376-2384.
13. Beaven SW, Abreu MT. Biomarkers in inflammatory bowel disease. Curr Opin Gastroenterol. 2004;20:318-327.
14. Mow WS, Vasiliauskas EA, Lin YC, et al. Association of antibody responses to microbial antigens and complications of small bowel Crohn's disease. Gastroenterology. 2004;126:414-424.
15. Barnich N, Boudeau J, Claret L, et al. Regulatory and functional cooperation of flagella and type 1 pili in adhesive and invasive abilities of AIEC strain LF82 isolated from a patient with Crohn's disease. Mol Microbiol. 2003;48:781-794.
16. Rolhion N, Carvalho FA, Darfeuille-Michaud A. OmpC and the sigma(E) regulatory pathway are involved in adhesion and invasion of the Crohn's disease-associated Escherichia coli strain LF82. Mol Microbiol. 2007;63:1684-1700.
17. Maaser C, Kannengiesser K, Specht C, et al. Crucial role of the melanocortin receptor MC1R in experimental colitis. Gut. 2006;55:1415-1422.
18. Rhee SH, Im E, Riegler M, et al. Pathophysiological role of Toll-like receptor 5 engagement by bacterial flagellin in colonic inflammation. Proc Natl Acad Sci USA. 2005;102:13610-13615.
19. Hayashi F, Smith KD, Ozinsky A, et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature. 2001;410: 1099-1103.
20. Miao EA, Alpuche-Aranda CM, Dors M, et al. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol. 2006;7:569-575.
21. Franchi L, Amer A, Body-Malapel M, et al. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat Immunol. 2006; 7:576-582.
22. Strober W, Fuss I, Mannon P. The fundamental basis of inflammatory bowel disease. J Clin Invest. 2007;117:514-521.
23. Swidsinski A, Ladhoff A, Pernthaler A, et al. Mucosal flora in inflammatory bowel disease. Gastroenterology. 2002;122:44-54.
24. Neut C, Bulois P, Desreumaux P, et al. Changes in the bacterial flora of the neoterminal ileum after ileocolonic resection for Crohn's disease. Am J Gastroenterol. 2002;97:939-946.
25. 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;127:412-421.
26. Martin HM, Campbell BJ, Hart CA, et al. Enhanced Escherichia coli adherence and invasion in Crohn's disease and colon cancer. Gastroenterology. 2004;127:80-93.
27. Kotlowski R, Bernstein CN, Sepehri S, et al. High prevalence of Escherichia coli belonging to the B2+D phylogenetic group in inflammatory bowel disease. Gut. 2007;56:669-675.
28. Conte MP, Schippa S, Zamboni I, et al. Gut-associated bacterial microbiota in paediatric patients with inflammatory bowel disease. Gut. 2006; 55:1760-1767.
29. Mylonaki M, Rayment NB, Rampton DS, et al. Molecular characterization of rectal mucosa-associated bacterial flora in inflammatory bowel disease. Inflamm Bowel Dis. 2005; 11:481-487.
30. Kamada N, Inoue N, Hisamatsu T, et al. Nonpathogenic Escherichia coli strain Nissle 1917 prevents murine acute and chronic colitis. Inflamm Bowel Dis. 2005; 11:455-463.
31. Grabig A, Paclik D, Guzy C, et al. Escherichia coli strain Nissle 1917 ameliorates experimental colitis via toll-like receptor 2- and toll-like receptor 4-dependent pathways. Infect Immun. 2006;74:4075-4082.
32. Kokesova A, Frolova L, Kverka M, et al. Oral administration of probiotic bacteria (E. coli Nissle, E. coli 083, Lactobacillus casei) influences the severity of dextran sodium sulfate-induced colitis in BALB/c mice. Folia Microbiol (Praha). 2006;51:478-484.
33. Rabizadeh S, Rhee KJ, Wu S, et al. Enterotoxigenic Bacteroidesfragilis: a potential instigator of colitis. Inflamm Bowel Dis. 2007;13:1475-1483.
34. Darfeuille-Michaud A, Neut C, Barnich N, et al. Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn's disease. Gastroenterology. 1998;115:1405-1413.
35. Glasser AL, Boudeau J, Barnich N, et al. Adherent invasive Escherichia coli strains from patients with Crohn's disease survive and replicate within macrophages without inducing host cell death, Infect Immun. 2001;69:5529-5537.
36. Claret L, Miquel S, Vieille N, et al. The flagellar sigma factor FliA regulates adhesion and invasion of Crohn disease-associated Escherichia coli via a cyclic dimeric GMP-dependent pathway. J Biol Chem. 2007; 282:33275-33283.
37. Saha S, Takeshita F, Matsuda T, et al. Blocking of the TLR5 activation domain hampers protective potential of flagellin DNA vaccine. J Immunol. 2007;179:1147-1154.
38. Miao EA, Andersen-Nissen E, Warren SE, et al. TLR5 and Ipaf: dual sensors of bacterial flagellin in the innate immune system. Semin Immunopathol. 2007;29:275-288.
39. Madrazo DR, Tranguch SL, Marriott I. Signaling via Toll-like receptor 5 can initiate inflammatory mediator production by murine osteoblasts. Infect Immun. 2003;71:5418-5421.
40. van Aubel RA, Keestra AM, Krooshoop DJ, et al. Ligand-induced differential cross-regulation of Toll-like receptors 2, 4 and 5 in intestinal epithelial cells. Mol Immunol. 2007;44:3702-3714.
41. Gewirtz AT, Navas TA, Lyons S, et al. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol. 2001; 167:1882-1885.
42. Uematsu S, Jang MH, Chevrier N, et al. Detection of pathogenic intestinal bacteria by Toll-like receptor 5 on intestinal CD11c+ lamina propria cells. Nat Immunol. 2006;7:868-874.