Adherent-invasive Escherichia coli blocks interferon-γ-induced signal transducer and activator of transcription (STAT)-1 in human intestinal epithelial cells

Cellular Microbiology

Volumn 15, Issue 3, 2013, Pages 446-457

  Ossa, Juan C ^a,b   Ho, Nathan K ^a,b   Wine, Eytan ^c   Leung, Nelly ^a,b   Gray Owen, Scott D ^a,b   Sherman, Philip M ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERFERON REGULATORY FACTOR 1; MESSENGER RNA; STAT1 PROTEIN;

ADHERENT INVASIVE ESCHERICHIA COLI; ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATION; CELL STIMULATION; CELL VIABILITY; CROHN DISEASE; ESCHERICHIA COLI INFECTION; ESCHERICHIA COLI O157; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOBLOTTING; INTESTINE EPITHELIUM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

CELL LINE; EPITHELIAL CELLS; ESCHERICHIA COLI; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; INTERFERON-GAMMA; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; STAT1 TRANSCRIPTION FACTOR;

ESCHERICHIA COLI;

EID: 84873710707     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12048     Document Type: Article

References (53)

1. Abraham, C., and Cho, J.H. (2007) Bugging of the intestinal mucosa. N Engl J Med 357: 708-710.
2. Abubakar, I., Myhill, D., Aliyu, S.H., and Hunter, P.R. (2008) Detection of Mycobacterium avium subspecies paratuberculosis from patients with Crohn's disease using nucleic acid-based techniques: a systematic review and meta-analysis. Inflamm Bowel Dis 14: 401-410.
3. Adams, R.B., Planchon, S.M., and Roche, J.K. (1993) IFN-gamma modulation of epithelial barrier function. Time course, reversibility, and site of cytokine binding. J Immunol 150: 2356-2363.
4. Andersen, P., Pedersen, M.W., Woetmann, A., Villingshoj, M., Stockhausen, M.T., Odum, N., and Poulsen, H.S. (2008) EGFR induces expression of IRF-1 via STAT1 and STAT3 activation leading to growth arrest of human cancer cells. Int J Cancer 122: 342-349.
5. Barnich, N., Carvalho, F.A., Glasser, A.L., Darcha, C., Jantscheff, P., Allez, M., etal. (2007) CEACAM6 acts as a receptor for adherent-invasive E.coli, supporting ileal mucosa colonization in Crohn disease. J Clin Invest 117: 1566-1574.
6. Baumgart, M., Dogan, B., Rishniw, M., Weitzman, G., Bosworth, B., Yantiss, R., etal. (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.
7. Bogdan, C., Rollinghoff, M., and Diefenbach, A. (2000) The role of nitric oxide in innate immunity. Immunol Rev 173: 17-26.
8. Boudeau, J., Glasser, A.L., Masseret, E., Joly, B., and Darfeuille-Michaud, A. (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.
9. Carvalho, F.A., Barnich, N., Sivignon, A., Darcha, C., Chan, C.H., Stanners, C.P., and Darfeuille-Michaud, A. (2009) Crohn's disease adherent-invasive Escherichia coli colonize and induce strong gut inflammation in transgenic mice expressing human CEACAM. J Exp Med 206: 2179-2189.
10. Ceponis, P.J., McKay, D.M., Ching, J.C., Pereira, P., and Sherman, P.M. (2003) Enterohemorrhagic Escherichia coli O157:H7 disrupts Stat1-mediated gamma interferon signal transduction in epithelial cells. Infect Immun 71: 1396-1404.
11. Chapgier, A., Kong, X.F., Boisson-Dupuis, S., Jouanguy, E., Averbuch, D., Feinberg, J., etal. (2009) A partial form of recessive STAT1 deficiency in humans. J Clin Invest 119: 1502-1514.
12. Chassaing, B., Rolhion, N., de Vallee, A., Salim, S.Y., Prorok-Hamon, M., Neut, C., etal. (2011) Crohn disease-associated adherent-invasive E.coli bacteria target mouse and human Peyer's patches via long polar fimbriae. J Clin Invest 121: 966-975.
13. Cho, J.H. (2008) The genetics and immunopathogenesis of inflammatory bowel disease. Nat Rev Immunol 8: 458-466.
14. Darfeuille-Michaud, A., Neut, C., Barnich, N., Lederman, E., Di Martino, P., Desreumaux, P., etal. (1998) Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn's disease. Gastroenterology 115: 1405-1413.
15. Darfeuille-Michaud, A., Boudeau, J., Bulois, P., Neut, C., Glasser, A.L., Barnich, N., etal. (2004) High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology 127: 412-421.
16. Donato, K.A., Gareau, M.G., Wang, Y.J., and Sherman, P.M. (2010) Lactobacillus rhamnosus GG attenuates interferon-{gamma} and tumour necrosis factor-alpha-induced barrier dysfunction and pro-inflammatory signalling. Microbiology 156: 3288-3297.
17. Eaves-Pyles, T., Allen, C.A., Taormina, J., Swidsinski, A., Tutt, C.B., Jezek, G.E., etal. (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.
18. Finlay, B.B., and McFadden, G. (2006) Anti-immunology: evasion of the host immune system by bacterial and viral pathogens. Cell 124: 767-782.
19. Forget, G., Gregory, D.J., and Olivier, M. (2005) Proteasome-mediated degradation of STAT1 alpha following infection of macrophages with Leishmania donovani. J Biol Chem 280: 30542-30549.
20. Glasser, A.L., Boudeau, J., Barnich, N., Perruchot, M.H., Colombel, J.F., and Darfeuille-Michaud, A. (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.
21. Ho, N.K., Crandall, I., and Sherman, P.M. (2012a) Identifying mechanisms by which Escherichia coli O157:H7 subverts interferon-gamma mediated signal transducer and activator of transcription-1 activation. PLoS ONE 7: e30145.
22. Ho, N.K., Ossa, J.C., Silphaduang, U., Johnson, R., Johnson-Henry, K.C., and Sherman, P.M. (2012b) Enterohemorrhagic Escherichia coli O157:H7 Shiga toxins inhibit gamma interferon-mediated cellular activation. Infect Immun 80: 2307-2315.
23. Hu, X., and Ivashkiv, L.B. (2009) Cross-regulation of signaling pathways by interferon-gamma: implications for immune responses and autoimmune diseases. Immunity 31: 539-550.
24. Irvine, G.B. (2001) Determination of molecular size by size-exclusion chromatography (gel filtration). Curr Protoc Cell Biol. Chapter 5, Unit 5.5.1-5.5.16.
25. Ismaili, A., Meddings, J.B., Ratnam, S., and Sherman, P.M. (1999) Modulation of host cell membrane fluidity: a novel mechanism for preventing bacterial adhesion. Am J Physiol 277: G201-G208.
26. Kamijo, R., Harada, H., Matsuyama, T., Bosland, M., Gerecitano, J., Shapiro, D., etal. (1994) Requirement for transcription factor IRF-1 in NO synthase induction in macrophages. Science 263: 1612-1615.
27. Kaper, J.B., Nataro, J.P., and Mobley, H.L. (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2: 123-140.
28. Karst, S.M., Wobus, C.E., Lay, M., Davidson, J., and Virgin, H.W. (2003) STAT1-dependent innate immunity to a Norwalk-like virus. Science 299: 1575-1578.
29. Kaser, A., Zeissig, S., and Blumberg, R.S. (2010) Inflammatory bowel disease. Annu Rev Immunol 28: 573-621.
30. Kotlowski, R., Bernstein, C.N., Sepehri, S., and Krause, D.O. (2007) High prevalence of Escherichia coli belonging to the B2+D phylogenetic group in inflammatory bowel disease. Gut 56: 669-675.
31. Liu, L., Okada, S., Kong, X.F., Kreins, A.Y., Cypowyj, S., Abhyankar, A., etal. (2011) Gain-of-function human STAT1 mutations impair IL-17 immunity and underlie chronic mucocutaneous candidiasis. J Exp Med 208: 1635-1648.
32. Martinez-Medina, M., Aldeguer, X., Lopez-Siles, M., Gonzalez-Huix, F., Lopez-Oliu, C., Dahbi, G., etal. (2009) Molecular diversity of Escherichia coli in the human gut: new ecological evidence supporting the role of adherent-invasive E.coli (AIEC) in Crohn's disease. Inflamm Bowel Dis 15: 872-882.
33. Meraz, M.A., White, J.M., Sheehan, K.C., Bach, E.A., Rodig, S.J., Dighe, A.S., etal. (1996) Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 84: 431-442.
34. Miquel, S., Peyretaillade, E., Claret, L., de Vallee, A., Dossat, C., Vacherie, B., etal. (2010) Complete genome sequence of Crohn's disease-associated adherent-invasive E.coli strain LF82. PLoS ONE 5: e12714.
35. Naser, S.A., Ghobrial, G., Romero, C., and Valentine, J.F. (2004) Culture of Mycobacterium avium subspecies paratuberculosis from the blood of patients with Crohn's disease. Lancet 364: 1039-1044.
36. Negroni, A., Costanzo, M., Vitali, R., Superti, F., Bertuccini, L., Tinari, A., etal. (2012) Characterization of adherent-invasive Escherichia coli isolated from pediatric patients with inflammatory bowel disease. Inflamm Bowel Dis 18: 913-924.
37. Pedron, T., and Sansonetti, P. (2008) Commensals, bacterial pathogens and intestinal inflammation: an intriguing menage a trois. Cell Host Microbe 3: 344-347.
38. Philpott, D.J., McKay, D.M., Mak, W., Perdue, M.H., and Sherman, P.M. (1998) Signal transduction pathways involved in enterohemorrhagic Escherichia coli-induced alterations in T84 epithelial permeability. Infect Immun 66: 1680-1687.
39. Rosselin, M., Virlogeux-Payant, I., Roy, C., Bottreau, E., Sizaret, P.Y., Mijouin, L., etal. (2012) Rck of Salmonella enterica, subspecies enterica serovar enteritidis, mediates zipper-like internalization. Cell Res 20: 647-664.
40. Sartor, R.B. (2008) Microbial influences in inflammatory bowel diseases. Gastroenterology 134: 577-594.
41. Sasaki, M., Sitaraman, S.V., Babbin, B.A., Gerner-Smidt, P., Ribot, E.M., Garrett, N., etal. (2007) Invasive Escherichia coli are a feature of Crohn's disease. Lab Invest 87: 1042-1054.
42. Schroder, K., Hertzog, P.J., Ravasi, T., and Hume, D.A. (2004) Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 75: 163-189.
43. Sepehri, S., Khafipour, E., Bernstein, C.N., Coombes, B.K., Pilar, A.V., Karmali, M., etal. (2010) Characterization of Escherichia coli isolated from gut biopsies of newly diagnosed patients with inflammatory bowel disease. Inflamm Bowel Dis 17: 1451-1463.
44. Sologuren, I., Boisson-Dupuis, S., Pestano, J., Vincent, Q.B., Fernandez-Perez, L., Chapgier, A., etal. (2011) Partial recessive IFN-gammaR1 deficiency: genetic, immunological and clinical features of 14 patients from 11 kindreds. Hum Mol Genet 20: 1509-1523.
45. Stark, G.R. (2007) How cells respond to interferons revisited: from early history to current complexity. Cytokine Growth Factor Rev 18: 419-423.
46. Stark, G.R., Kerr, I.M., Williams, B.R., Silverman, R.H., and Schreiber, R.D. (1998) How cells respond to interferons. Annu Rev Biochem 67: 227-264.
47. Tamura, T., Yanai, H., Savitsky, D., and Taniguchi, T. (2008) The IRF family transcription factors in immunity and oncogenesis. Annu Rev Immunol 26: 535-584.
48. Ulane, C.M., and Horvath, C.M. (2002) Paramyxoviruses SV5 and HPIV2 assemble STAT protein ubiquitin ligase complexes from cellular components. Virology 304: 160-166.
49. van de Veerdonk, F.L., Plantinga, T.S., Hoischen, A., Smeekens, S.P., Joosten, L.A., Gilissen, C., etal. (2011) STAT1 mutations in autosomal dominant chronic mucocutaneous candidiasis. N Engl J Med 365: 54-61.
50. Wine, E., Ossa, J.C., Gray-Owen, S.D., and Sherman, P.M. (2009) Adherent-invasive Escherichia coli, strain LF82 disrupts apical junctional complexes in polarized epithelia. BMC Microbiol 9: 180.
51. Xavier, R.J., and Podolsky, D.K. (2007) Unravelling the pathogenesis of inflammatory bowel disease. Nature 448: 427-434.
52. Yokosawa, N., Yokota, S., Kubota, T., and Fujii, N. (2002) C-terminal region of STAT-1alpha is not necessary for its ubiquitination and degradation caused by mumps virus V protein. J Virol 76: 12683-12690.
53. Zhang, S.Y., Boisson-Dupuis, S., Chapgier, A., Yang, K., Bustamante, J., Puel, A., etal. (2008) Inborn errors of interferon (IFN)-mediated immunity in humans: insights into the respective roles of IFN-alpha/beta, IFN-gamma, and IFN-lambda in host defense. Immunol Rev 226: 29-40.