Crohn's disease adherent-invasive Escherichia coli colonize and induce strong gut inflammation in transgenic mice expressing human CEACAM

Journal of Experimental Medicine

Volumn 206, Issue 10, 2009, Pages 2179-2189

  Carvalho, Frédéric A ^a   Barnich, Nicolas ^a,b   Sivignon, Adeline ^a,b   Darcha, Claude ^c   Chan, Carlos H F ^d   Stanners, Clifford P ^e   Darfeuille Michaud, Arlette ^a,b  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

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

^c UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

^d MCGILL UNIVERSITY   (Canada)

^e MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 6; ADHESIN; CEACAM6 PROTEIN, HUMAN; CELL ADHESION MOLECULE; FIMBRIA PROTEIN; FIMH PROTEIN, E COLI; LEUKOCYTE ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; COLITIS; CROHN DISEASE; ESCHERICHIA COLI; INTESTINE MUCOSA; MALE; MOUSE; MOUSE MUTANT; MUCOSA INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; RECTUM HEMORRHAGE; SURVIVAL RATE; TRANSGENIC MOUSE; WEIGHT REDUCTION; ANIMAL; BACTERIUM ADHERENCE; GASTROINTESTINAL TRACT; HUMAN; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY;

ADHESINS, ESCHERICHIA COLI; ANIMALS; ANTIGENS, CD; BACTERIAL ADHESION; CELL ADHESION MOLECULES; COLITIS; CROHN DISEASE; ESCHERICHIA COLI; FIMBRIAE PROTEINS; GASTROINTESTINAL TRACT; HUMANS; MICE; MICE, TRANSGENIC;

EID: 70350468598     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20090741     Document Type: Article

References (48)

1. Barnich, N., J. Boudeau, L. Claret, and A. Darfeuille-Michaud. 2003. Regulatory and functional co-operation 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. 48:781-794. doi:10.1046/j.1365-2958.2003.03468.x
2. Barnich, N., F.A. Carvalho, A.L. Glasser, C. Darcha, P. Jantscheff, M. Allez, H. Peeters, G. Bommelaer, P. Desreumaux, J.F. Colombel, and A. Darfeuille-Michaud. 2007. CEACAM6 acts as a receptor for adherent-invasive E. coli, supporting ileal mucosa colonization in Crohn disease. J. Clin. Invest. 117:1566-1574. doi:10.1172/JCI30504
3. Baumgart, M., B. Dogan, M. Rishniw, G. Weitzman, B. Bosworth, R. Yantiss, R.H. Orsi, M. Wiedmann, P. McDonough, S.G. Kim, et al. 2007. Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn's disease involving the ileum. ISME J. 1:403-418. doi:10.1038/ismej.2007.52
4. Boudeau, J., A.L. Glasser, E. Masseret, B. Joly, and A. Darfeuille-Michaud. 1999. Invasive ability of an Escherichia coli strain isolated from the ileal mucosa of a patient with Crohn's disease. Infect. Immun. 67:4499-4509.
5. Boudeau, J., A.L. Glasser, S. Julien, J.F. Colombel, and A. Darfeuille-Michaud. 2003. Inhibitory effect of probiotic Escherichia coli strain Nissle 1917 on adhesion to and invasion of intestinal epithelial cells by adherent-invasive E. coli strains isolated from patients with Crohn's disease. Aliment. Pharmacol. Ther. 18:45-56. doi:10.1046/j.1365-2036. 2003.01638.x
6. Carvalho, F.A., N. Barnich, P. Sauvanet, C. Darcha, A. Gelot, and A. Darfeuille-Michaud. 2008. Crohn's disease-associated Escherichia coli LF82 aggravates colitis in injured mouse colon via signaling by flagellin. Inflamm. Bowel Dis. 14:1051-1060. doi:10.1002/ibd.20423
7. Cegelski, L., G.R. Marshall, G.R. Eldridge, and S.J. Hultgren. 2008. The biology and future prospects of antivirulence therapies. Nat. Rev. Microbiol. 6:17-27. doi:10.1038/nrmicro1818
8. Chan, C.H., and C.P. Stanners. 2004. Novel mouse model for carcinoembryonic antigen-based therapy. Mol. Ther. 9:775-785. doi:10.1016/j.ymthe.2004.03.009
9. Claret, L., S. Miquel, N. Vieille, D.A. Ryjenkov, M. Gomelsky, and A. Darfeuille-Michaud. 2007. 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. 282:33275-33283. doi:10.1074/jbc.M702800200
10. Conte, M.P., S. Schippa, I. Zamboni, M. Penta, F. Chiarini, L. Seganti, J. Osborn, P. Falconieri, O. Borrelli, and S. Cucchiara. 2006. Gut-associated bacterial microbiota in paediatric patients with inflammatory bowel disease. Gut. 55:1760-1767. doi:10.1136/gut.2005.078824
11. Darfeuille-Michaud, A., C. Neut, N. Barnich, E. Lederman, P. Di Martino, P. Desreumaux, L. Gambiez, B. Joly, A. Cortot, and J.F. Colombel. 1998. Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn's disease. Gastroenterology. 115:1405-1413. doi:10.1016/S0016- 5085(98)70019-8
12. Darfeuille-Michaud, A., J. Boudeau, P. Bulois, C. Neut, A.L. Glasser, N. Barnich, M.A. Bringer, A. Swidsinski, L. Beaugerie, and J.F. Colombel. 2004. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology. 127:412-421. doi:10.1053/j.gastro.2004.04.061
13. Eaves-Pyles, T., C.A. Allen, J. Taormina, A. Swidsinski, C.B. Tutt, G.E. Jezek, M. Islas-Islas, and A.G. Torres. 2008. Escherichia coli isolated from a Crohn's disease patient adheres, invades, and induces inflammatory responses in polarized intestinal epithelial cells. Int. J. Med. Microbiol. 298:397-409. doi:10.1016/j.ijmm.2007.05.011
14. Fahlgren, A., V. Baranov, L. Frängsmyr, F. Zoubir, M.L. Hammarström, and S. Hammarström. 2003. Interferon-gamma tempers the expression of carcinoembryonic antigen family molecules in human colon cells: a possible role in innate mucosal defence. Scand. J. Immunol. 58:628-641. doi:10.1111/j.1365-3083.2003.01342.x
15. Glasser, A.L., J. Boudeau, N. Barnich, M.H. Perruchot, J.F. Colombel, and A. Darfeuille-Michaud. 2001. Adherent invasive Escherichia coli strains from patients with Crohn's disease survive and replicate within macrophages without inducing host cell death. Infect. Immun. 69:5529-5537. doi:10.1128/IAI.69.9.5529-5537.2001
16. Kotlowski, R., C.N. Bernstein, S. Sepehri, and D.O. Krause. 2007. High prevalence of Escherichia coli belonging to the B2+D phylogenetic group in inflammatory bowel disease. Gut. 56:669-675. doi:10.1136/gut.2006. 099796
17. Langermann, S., S. Palaszynski, M. Barnhart, G. Auguste, J.S. Pinkner, J. Burlein, P. Barren, S. Koenig, S. Leath, C.H. Jones, and S.J. Hultgren. 1997. Prevention of mucosal Escherichia coli infection by FimH-adhesin-based systemic vaccination. Science. 276:607-611. doi:10.1126/science.276.5312. 607
18. Langermann, S., R. Möllby, J.E. Burlein, S.R. Palaszynski, C.G. Auguste, A. DeFusco, R. Strouse, M.A. Schenerman, S.J. Hultgren, J.S. Pinkner, et al. 2000. Vaccination with FimH adhesin protects cynomolgus monkeys from colonization and infection by uropathogenic Escherichia coli. J. Infect. Dis. 181:774-778. doi:10.1086/315258
19. Larsson, A., S.M. Johansson, J.S. Pinkner, S.J. Hultgren, F. Almqvist, J. Kihlberg, and A. Linusson. 2005. Multivariate design, synthesis, and biological evaluation of peptide inhibitors of FimC/FimH protein-protein interactions in uropathogenic Escherichia coli. J. Med. Chem. 48:935-945. doi:10.1021/jm040818l
20. Loftus, E.V. Jr. 2004. Clinical epidemiology of inflammatory bowel disease: Incidence, prevalence, and environmental influences. Gastroenterology. 126:1504-1517. doi:10.1053/j.gastro.2004.01.063
21. Lupp, C., M.L. Robertson, M.E. Wickham, I. Sekirov, O.L. Champion, E.C. Gaynor, and B.B. Finlay. 2007. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe. 2:204. doi:10.1016/j.chom.2007.08.002
22. Malchow, H.A. 1997. Crohn's disease and Escherichia coli. A new approach in therapy to maintain remission of colonic Crohn's disease? J. Clin. Gastroenterol. 25:653-658. doi:10.1097/00004836-199712000-00021
23. Mansfield, L.S., J.A. Bell, D.L. Wilson, A.J. Murphy, H.M. Elsheikha, V.A. Rathinam, B.R. Fierro, J.E. Linz, and V.B. Young. 2007. C57BL/6 and congenic interleukin-10-deficient mice can serve as models of Campylobacter jejuni colonization and enteritis. Infect. Immun. 75:1099-1115. doi:10.1128/IAI.00833-06
24. Martin, H.M., B.J. Campbell, C.A. Hart, C. Mpofu, M. Nayar, R. Singh, H. Englyst, H.F. Williams, and J.M. Rhodes. 2004. Enhanced Escherichia coli adherence and invasion in Crohn's disease and colon cancer. Gastroenterology. 127:80-93. doi:10.1053/j.gastro.2004.03.054
25. Mossman, K.L., M.F. Mian, N.M. Lauzon, C.L. Gyles, B. Lichty, R. Mackenzie, N. Gill, and A.A. Ashkar. 2008. Cutting edge: FimH adhesin of type 1 fimbriae is a novel TLR4 ligand. J. Immunol. 181:6702-6706.
26. Mylonaki, M., N.B. Rayment, D.S. Rampton, B.N. Hudspith, and J. Brostoff. 2005. Molecular characterization of rectal mucosa-associated bacterial flora in inflammatory bowel disease. Inflamm. Bowel Dis. 11:481-487. doi:10.1097/01.MIB.0000159663.62651.4f
27. Neut, C., P. Bulois, P. Desreumaux, J.M. Membré, E. Lederman, L. Gambiez, A. Cortot, P. Quandalle, H. van Kruiningen, and J.F. Colombel. 2002. Changes in the bacterial flora of the neoterminal ileum after ileocolonic resection for Crohn's disease. Am. J. Gastroenterol. 97:939-946. doi:10.1111/j.1572-0241.2002.05613.x
28. Ofek, I., D.L. Hasty, S.N. Abraham, and N. Sharon. 2000. Role of bacterial lectins in urinary tract infections. Molecular mechanisms for diversification of bacterial surface lectins. Adv. Exp. Med. Biol. 485:183-192. doi:10.1007/0-306-46840-9-25
29. Podolsky, D.K. 2002. Inflammatory bowel disease. N. Engl. J. Med. 347:417-429. doi:10.1056/NEJMra020831
30. Poggio, T.V., J.L. La Torre, and E.A. Scodeller. 2006. Intranasal immunization with a recombinant truncated FimH adhesin adjuvanted with CpG oligodeoxynucleotides protects mice against uropathogenic Escherichia coli challenge. Can. J. Microbiol. 52:1093-1102. doi:10.1139/W06-065
31. Prantera, C., M.L. Scribano, G. Falasco, A. Andreoli, and C. Luzi. 2002. Ineffectiveness of probiotics in preventing recurrence after curative resection for Crohn's disease: a randomised controlled trial with Lactobacillus GG. Gut. 51:405-409. doi:10.1136/gut.51.3.405
32. Rinella, E.S., C.D. Eversley, I.M. Carroll, J.M. Andrus, D.W. Threadgill, and D.S. Threadgill. 2006. Human epithelial-specific response to pathogenic Campylobacter jejuni. FEMS Microbiol. Lett. 262:236-243.
33. Rolhion, N., F.A. Carvalho, and A. Darfeuille-Michaud. 2007. 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. 63:1684-1700. doi:10.1111/j.1365-2958.2007.05638.x
34. Rutgeerts, P., K. Goboes, M. Peeters, M. Hiele, F. Penninckx, R. Aerts, R. Kerremans, and G. Vantrappen. 1991. Effect of faecal stream diversion on recurrence of Crohn's disease in the neoterminal ileum. Lancet. 338:771-774. doi:10.1016/0140-6736(91)90663-A
35. Sands, B.E. 2007. Inflammatory bowel disease: past, present, and future. J. Gastroenterol. 42:16-25. doi:10.1007/s00535-006-1995-7
36. Sartor, R.B. 2004. Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology. 126:1620-1633. doi:10.1053/j.gastro.2004.03.024
37. Sartor, R.B. 2008. Microbial influences in inflammatory bowel diseases. Gastroenterology. 134:577-594. doi:10.1053/j.gastro.2007.11.059
38. Sasaki, M., S.V. Sitaraman, B.A. Babbin, P. Gerner-Smidt, E.M. Ribot, N. Garrett, J.A. Alpern, A. Akyildiz, A.L. Theiss, A. Nusrat, and J.M. Klapproth. 2007. Invasive Escherichia coli are a feature of Crohn's disease. Lab. Invest. 87:1042-1054. doi:10.1038/labinvest.3700661
39. Shanahan, F. 2002. Crohn's disease. Lancet. 359:62-69. doi:10.1016/S0140-6736(02)07284-7
40. Sokol, H., B. Pigneur, L. Watterlot, O. Lakhdari, L.G. Bermúdez-Humarán, J.J. Gratadoux, S. Blugeon, C. Bridonneau, J.P. Furet, G. Corthier, et al. 2008. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. USA. 105:16731-16736. doi:10.1073/pnas.0804812105
41. Stecher, B., R. Robbiani, A.W. Walker, A.M. Westendorf, M. Barthel, M. Kremer, S. Chaffron, A.J. Macpherson, J. Buer, J. Parkhill, et al. 2007. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol. 5:2177-2189. doi:10.1371/journal.pbio.0050244
42. Strober, W., I. Fuss, and P. Mannon. 2007. The fundamental basis of inflammatory bowel disease. J. Clin. Invest. 117:514-521. doi:10.1172/JCI30587
43. Svensson, A., A. Larsson, H. Emtenäs, M. Hedenström, T. Fex, S.J. Hultgren, J.S. Pinkner, F. Almqvist, and J. Kihlberg. 2001. Design and evaluation of pilicides: potential novel antibacterial agents directed against uropathogenic Escherichia coli. ChemBioChem. 2:915-918. doi:10.1002/1439-7633(20011203)2:12〈915::AID-CBIC915〉3.0.CO;2-M
44. Swidsinski, A., A. Ladhoff, A. Pernthaler, S. Swidsinski, V. Loening-Baucke, M. Ortner, J. Weber, U. Hoffmann, S. Schreiber, M. Dietel, and H. Lochs. 2002. Mucosal flora in inflammatory bowel disease. Gastroenterology. 122:44-54. doi:10.1053/gast.2002.30294
45. Tamboli, C.P., C. Neut, P. Desreumaux, and J.F. Colombel. 2004. Dysbiosis in inflammatory bowel disease. Gut. 53:1-4. doi:10.1136/gut.53.1.1
46. Thankavel, K., B. Madison, T. Ikeda, R. Malaviya, A.H. Shah, P.M. Arumugam, and S.N. Abraham. 1997. Localization of a domain in the FimH adhesin of Escherichia coli type 1 fimbriae capable of receptor recognition and use of a domain-specific antibody to confer protection against experimental urinary tract infection. J. Clin. Invest. 100:1123-1136. doi:10.1172/JCI119623
47. Wadolkowski, E.A., D.C. Laux, and P.S. Cohen. 1988. Colonization of the streptomycin-treated mouse large intestine by a human fecal Escherichia coli strain: role of growth in mucus. Infect. Immun. 56:1030-1035.
48. Wellens, A., C. Garofalo, H. Nguyen, N. Van Gerven, R. Slättegård, J.P. Hernalsteens, L. Wyns, S. Oscarson, H. De Greve, S. Hultgren, and J. Bouckaert. 2008. Intervening with urinary tract infections using anti-adhesives based on the crystal structure of the FimH-oligomannose-3 complex. PLoS One. 3:e2040. doi:10.1371/journal.pone.0002040