Subversion of human intestinal mucosa innate immunity by a Crohn's disease-associated E. coli

Mucosal Immunology

Volumn 8, Issue 3, 2015, Pages 572-581

  Jarry, A ^a   Cremet L ^b,c   Caroff, N ^b,c   Bou Hanna, C ^a   Mussini, J M ^d   Reynaud, A ^b,c   Servin, A L ^e   Mosnier, J F ^a,d   Lievin Le Moal V ^e   Laboisse, C L ^a,d  

^a UNIVERSITÉ DE NANTES   (France)

^b UNIVERSITÉ DE NANTES   (France)

^c NANTES UNIVERSITY HOSPITAL   (France)

^d SMUR Nantes   (France)

^e UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GENTAMICIN; I KAPPA B KINASE ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA CONVERTING ENZYME; TUMOR NECROSIS FACTOR ALPHA; I KAPPA B; INTERLEUKIN 18 PROTEIN, HUMAN; NF-KAPPAB INHIBITOR ALPHA; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR;

ADHERENT INVASIVE ESCHERICHIA COLI; ADULT; AGED; ARTICLE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; CLINICAL ARTICLE; CONTROLLED STUDY; CROHN DISEASE; CYTOARCHITECTURE; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ESCHERICHIA COLI; EX VIVO STUDY; FEMALE; HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN TISSUE; INNATE IMMUNITY; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA; MACROPHAGE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; SALMONELLA; SIGNAL TRANSDUCTION; VERY ELDERLY; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; IMMUNE EVASION; IMMUNOLOGY; MICROBIOLOGY; MUCOSAL IMMUNITY; PATHOLOGY; PHOSPHORYLATION; TISSUE CULTURE TECHNIQUE;

CASPASE 1; CROHN DISEASE; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; I-KAPPA B PROTEINS; IMMUNE EVASION; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; INFLAMMASOMES; INTERLEUKIN-18; INTESTINAL MUCOSA; MACROPHAGES; PHOSPHORYLATION; SALMONELLA; SIGNAL TRANSDUCTION; TISSUE CULTURE TECHNIQUES; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84928919829     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2014.89     Document Type: Article

References (38)

1. Martinon, F., Mayor, A. & Tschopp, J. The inflammasomes: guardians of the body. Annu. Rev. Immunol. 27, 229-265 (2009).
2. Jarry, A. et al. Interleukin 1 and interleukin 1beta converting enzyme (caspase 1) expression in the human colonic epithelial barrier. Caspase 1 downregulation in colon cancer. Gut 45, 246-251 (1999).
3. Pages, F. et al. Modulation of interleukin-18 expression in human colon carcinoma: consequences for tumor immune surveillance. Int. J. Cancer 84, 326-330 (1999).
4. McAlindon, M.E., Hawkey, C.J. & Mahida, Y.R. Expression of interleukin 1 beta and interleukin 1 beta converting enzyme by intestinal macrophages in health and inflammatory bowel disease. Gut 42, 214-219 (1998).
5. Jarry, A., Bossard, C., Sarrabayrouse, G., Mosnier, J.-F. & Laboisse, C.L. Loss of interleukin-10 or transforming growth factor beta signaling in the human colon initiates a T-helper 1 response via distinct pathways. Gastroenterology 141, 1887-1896. e1881-1882 (2011).
6. Fink, S.L. & Cookson, B.T. Pyroptosis and host cell death responses during Salmonella infection. Cell Microbiol. 9, 2562-2570 (2007).
7. Miao, E.A. et al. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat. Immunol. 11, 1136-1142 (2010).
8. Hayden, M.S. & Ghosh, S. Signaling to NF-kappaB. Gene. Dev. 18, 2195-2224 (2004).
9. Sadikot, R.T. et al. Targeted immunomodulation of the NF-kappaB pathway in airway epithelium impacts host defense against Pseudomonas aeruginosa. J. Immunol. 176, 4923-4930 (2006).
10. Jiang, D. et al. Airway epithelial NF-kappaB activation promotes Mycoplasma pneumoniae clearance in mice. PloS One 7, e52969 (2012).
11. Jobin, C. & Sartor, R.B. The I kappa B/NF-kappa B system: a key determinant of mucosal inflammation and protection. Am. J. Physiol. Cell Physiol. 278, C451-C462 (2000).
12. Karin, M. & Lin, A. NF-kappaB at the crossroads of life and death. Nat. Immunol. 3, 221-227 (2002).
13. Jarry, A. et al. Mucosal IL-10 and TGF-beta play crucial roles in preventing LPS-driven, IFN-gamma-mediated epithelial damage in human colon explants. J. Clin. Invest. 118, 1132-1142 (2008).
14. Di Sabatino, A. et al. Blockade of transforming growth factor beta upregulates T-box transcription factor T-bet, and increases T helper cell type 1 cytokine and matrix metalloproteinase-3 production in the human gut mucosa. Gut 57, 605-612 (2008).
15. Croxen, M.A. et al. Recent advances in understanding enteric pathogenic Escherichia coli. Clin. Microbiol. Rev. 26, 822-880 (2013).
16. Darfeuille-Michaud, A. et al. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology 127, 412-421 (2004).
17. Pineton de Chambrun, G., Colombel, J.-F., Poulain, D. & Darfeuille-Michaud, A. Pathogenic agents in inflammatory bowel diseases. Curr. Opin. Gastroenterol. 24, 440-447 (2008).
18. Darfeuille-Michaud, A. et al. Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn's disease. Gastroenterology 115, 1405-1413 (1998).
19. Jensen, S.R., Fink, L.N., Nielsen, O.H., Brynskov, J. & Brix, S. Ex vivo intestinal adhesion of Escherichia coli LF82 in Crohn's disease. Microb. Pathog. 51, 426-431 (2011).
20. Boudeau, J., Glasser, A.L., Masseret, E., Joly, B. & Darfeuille-Michaud, A. Invasive ability of an Escherichia coli strain isolated from the ileal mucosa of a patient with Crohn's disease. Infect. Immun. 67, 4499-4509 (1999).
21. Glasser, A.L. 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. 69, 5529-5537 (2001).
22. Eaves-Pyles, T. et al. 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 (2008).
23. Bringer, M.A., Billard, E., Glasser, A.L., Colombel, J.-F. & Darfeuille-Michaud, A. Replication of Crohn's disease-associated AIEC within macrophages is dependent on TNF-alpha secretion. Lab Invest 92, 411-419 (2012).
24. Dunne, K.A. et al. Increased S-nitrosylation and proteasomal degradation of caspase-3 during infection contribute to the persistence of adherent invasive Escherichia coli (AIEC) in immune cells. PloS One 8, e68386 (2013).
25. Albina, J.E. On the expression of nitric oxide synthase by human macrophages. Why no NO?. J. Leuk. Biol. 58, 643-649 (1995).
26. Barnich, N. et al.CEACAM6acts as a receptor for adherent-invasive E. coli, supporting ileal mucosa colonization in Crohn disease. J. Clin. Invest. 117, 1566-1574 (2007).
27. Grassl, G.A. & Finlay, B.B. Pathogenesis of enteric Salmonella infections. Curr. Opin. Gastroenterol. 24, 22-26 (2008).
28. Lievin-Le Moal, V. & Servin, A.L. Pathogenesis of human enterovirulent bacteria: lessons from cultured, fully differentiated human colon cancer cell lines. Microbiol. Mol. Biol. Rev. 77, 380-439 (2013).
29. Kumar, A., Takada, Y., Boriek, A.M. & Aggarwal, B.B. Nuclear factorkappaB: its role in health and disease. J. Mol. Med. (Berl) 82, 434-448 (2004).
30. Karin, M. NF-kappaB and cancer: mechanisms and targets. Mol. Carcinog. 45, 355-361 (2006).
31. Tsilingiri, K. et al. Probiotic and postbiotic activity in health and disease: comparison on a novel polarised ex-vivo organ culture model. Gut 61, 1007-1015 (2012).
32. Hammarström, S. The carcinoembryonic antigen (CEA) family: structures, suggested functions and expression in normal and malignant tissues. Semin. Cancer Biol. 9, 67-81 (1999).
33. Coburn, B., Grassl, G.A. & Finlay, B.B. Salmonella, the host and disease: a brief review. Immunol. Cell. Biol. 85, 112-118 (2007).
34. Barnich, N., Boudeau, J., Claret, L. & Darfeuille-Michaud, A. 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 (2003).
35. Cleynen, I. et al. Genetic and microbial factors modulating the ubiquitin proteasome system in inflammatory bowel disease. Gut 63, 1265-1274 (2014).
36. Caulin, C., Salvesen, G.S. & Oshima, R.G. Caspase cleavage of keratin 18 and reorganization of intermediate filaments during epithelial cell apoptosis. J. Cell Biol. 138, 379-1394 (1997).
37. Leers, M.P. et al. Immunocytochemical detection and mapping of a cytokeratin 18 neo-epitope exposed during early apoptosis. J. Pathol. 187, 567-572 (1999).
38. Souaze, F. et al. Differential roles of Hath1, MUC2 and P27Kip1 in relation with gamma-secretase inhibition in human colonic carcinomas: a translational study. PloS One 8, e55904 (2013).