Conditioned medium from enterohemorrhagic Escherichia coli-infected T84 cells inhibits signal transducer and activator of transcription 1 activation by gamma interferon

Infection and Immunity

Volumn 74, Issue 3, 2006, Pages 1809-1818

  Jandu, Narveen ^a,b   Ceponis, Peter J M ^a,b   Kato, Seiichi ^a,b   Riff, Jason D ^a,b   McKay, Derek M ^c   Sherman, Philip M ^a,b,d  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

^d HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; CYTOKINE; FLAGELLIN; GAMMA INTERFERON; GAMMA INTERFERON RECEPTOR; GAMMA INTERFERON RECEPTOR DOMAIN 1 PROTEIN; PROTEASOME; PROTEIN TYROSINE PHOSPHATASE; PROTEINASE K; SODIUM; STAT1 PROTEIN; TRYPSIN; UNCLASSIFIED DRUG; VANADIC ACID;

ARTICLE; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM CULTURE; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CULTURE MEDIUM; ENTEROHEMORRHAGIC ESCHERICHIA COLI; EPITHELIUM CELL; ESCHERICHIA COLI O157; HEAT TREATMENT; HOST PATHOGEN INTERACTION; HOST RESISTANCE; HUMAN; HUMAN CELL; IMMUNE SYSTEM; IMMUNOBLOTTING; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; SEROTYPE; SIGNAL TRANSDUCTION; SUPERNATANT; TIME;

CULTURE MEDIA, CONDITIONED; DRUG INTERACTIONS; EPITHELIAL CELLS; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI O157; INTERFERON TYPE II; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; TRANS-ACTIVATORS;

EID: 33644749140     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.74.3.1809-1818.2006     Document Type: Article

References (60)

1. Bach, E. A., M. Aguet, and R. D. Schreiber. 1997. The IFN gamma receptor: a paradigm for cytokine receptor signaling. Annu. Rev. Immunol. 15:563-591.
2. Berin, M. C., A. Darfeuille-Michaud, L. J. Egan, Y. Miyamoto, and M. F. Kagnoff. 2002. Role of EHEC O157:H7 virulence factors in the activation of intestinal epithelial cell NF-kappaB and MAP kinase pathways and the upregulated expression of interleukin 8. Cell Microbiol. 4:635-648.
3. Bourdeau, A., N. Dube, and M. L. Tremblay. 2005. Cytoplasmic protein tyrosine phosphatases, regulation and function: the roles of PTP1B and TC-PTP. Curr. Opin. Cell Biol. 17:203-209.
4. Ceponis, P. J., D. M. McKay, J. C. Ching, P. Pereira, and P. M. Sherman. 2003. Enterohemorrhagic Escherichia coli O157:H7 disrupts Stat1-mediated gamma IFN signal transduction in epithelial cells. Infect. Immun. 71:1396-1404.
5. Coombes, B. K., and J. B. Mahony. 1999. Chlamydia pneumoniae infection of human endothelial cells induces proliferation of smooth muscle cells via an endothelial cell-derived soluble factor(s). Infect. Immun. 67:2909-2915.
6. Cornelis, G. R. 2002. Yersinia type III secretion: send in the effectors. J. Cell Biol. 158:401-408.
7. Dahan, S., V. Busuttil, V. Imbert, J. F. Peyron, P. Rampal, and D. Czerucka. 2002. Enterohemorrhagic Escherichia coli infection induces interleukin-8 production via activation of mitogen-activated protein kinases and the transcription factors NF-κB and AP-1 in T84 cells. Infect. Immun. 70:2304-2310.
8. Dalpke, A. H., S. Eckerle, M. Frey, and K. Heeg. 2003. Triggering of Toll-like receptors modulates IFN-gamma signaling: involvement of serine 727 STAT1 phosphorylation and suppressors of cytokine signaling. Eur. J. Immunol. 33:1776-1787.
9. DeVinney, R., J. L. Puente, A. Gauthier, D. Goosney, and B. B. Finlay. 2001. Enterohaemorrhagic and enteropathogenic Escherichia coli use a different Tir-based mechanism for pedestal formation. Mol. Microbiol. 41:1445-1458.
10. Donnenberg, M. S., and T. S. Whittam. 2001. Pathogenesis and evolution of virulence in enteropathogenic and enterohemorrhagic Escherichia coli. J. Clin. Investig. 107:539-548.
11. Dytoc, M. T., A. Ismaili, D. J. Philpott, R. Soni, J. L. Brunton, and P. M. Sherman. 1994. Distinct binding properties of eae4-negative verocytotoxin-producing Escherichia coli of serotype O113:H21. Infect. Immun. 62:3494-3505.
12. Dytoc, M., L. Fedorko, and P. M. Sherman. 1994. Signal transduction in human epithelial cells infected with attaching and effacing Escherichia coli in vitro. Gastroenterology 106:1150-1161.
13. Feng, P., K. A. Lampel, H. Karch, and T. S. Whittam. 1988. Genotypic and phenotypic changes in the emergence of Escherichia coli O157:H7. J. Infect. Dis. 177:1750-1753.
14. Finlay, B. B., and S. Falkow. 1997. Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 61:136-169.
15. George, K. M., L. P. Barker, D. M. Welty, and P. L. Small. 1998. Partial purification and characterization of biological effects of a lipid toxin produced by Mycobacterium ulcerans. Infect. Immun. 66:587-593.
16. Gewirtz, A. T., P. O. Simon, Jr., C. K. Schmitt, L. J. Taylor, C. H. Hagedorn, A. D. O'Brien, A. S. Neish, and J. L. Madara. 2001. Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J. Clin. Investig. 107:99-109.
17. Haque, S. J., Q. Wu, W. Kammer, K. Friedrich, J. M. Smith, I. M. Kerr, G. R. Stark, and B. R. Williams. 1997. Receptor-associated constitutive protein tyrosine phosphatase activity controls the kinase function of JAK1. Proc. Natl. Acad. Sci. USA 94:8563-8568.
18. Haspel, R. L., and J. E. Darnell, Jr. 1999. A nuclear protein tyrosine phosphatase is required for the inactivation of Stat1. Proc. Natl. Acad. Sci. USA 96:10188-10193.
19. Higgins, L. M., G. Frankel, G. Douce, G. Dougan, and T. T. MacDonald. 1999. Citrobacter rodentium infection in mice elicits a mucosal Th1 cytokine response and lesions similar to those in murine inflammatory bowel disease. Infect. Immun. 67:3031-3039.
20. Hussain, S., B. S. Zwilling, and W. P. Lafuse. 1999. Mycobacterium avium infection of mouse macrophages inhibits IFN-gamma Janus kinase-STAT signaling and gene induction by down-regulation of the IFN-gamma receptor. J. Immunol. 163:2041-2048.
21. Ismaili, A., D. J. Philpott, M. T. Dytoc, and P. M. Sherman. 1995. Signal transduction responses following adhesion of verocytotoxin-producing Escherichia coli. Infect. Immun. 63:3316-3326.
22. Ismaili, A., J. B. Meddings, S. Ratnam, and P. M. Sherman. 1999. Modulation of host cell membrane fluidity: a novel mechanism for preventing bacterial adhesion. Am. J. Physiol. 277:G201-208.
23. Jelacic, J. K., T. Damrow, G. S. Chen, S. Jelacic, M. Bielaszewska, M. Ciol, H. M. Carvalho, A. R. Melton-Celsa, A. D. O'Brien, and P. I. Tarr. 2003. Shiga toxin-producing Escherichia coli in Montana: bacterial genotypes and clinical profiles. J. Infect. Dis. 188:719-729.
24. Joseph, T. D., and D. C. Look. 2001. Specific inhibition of interferon signal transduction pathways by adenoviral infection. J. Biol. Chem. 276:47136-47142.
25. Kaper, J. B., J. P. Nataro, and H. L. Mobley. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2:123-140.
26. Karmali, M. A., M. Petric, C. Lim, P. C. Fleming, G. S. Arbus, and H. Lior. 1985. The association between idiopathic hemolytic uremic syndrome and infection by verotoxin-producing Escherichia coli. J. Infect. Dis. 151:775-782.
27. Keire, D. A., P. Anton, K. F. Faull, E. Ruth, J. H. Walsh, P. Chew, D. Quisimoro, M. Territo, and J. R. Reeve, Jr. 2001. Diethyl phthalate, a chemotactic factor secreted by Helicobacter pylori. J. Biol. Chem. 276:48847-48853.
28. Khine, A. A., and C. A. Lingwood. 2000. Functional significance of globotriaosyl ceramide in interferon-alpha(2)/type 1 interferon receptor-mediated antiviral activity. J. Cell. Physiol. 182:97-108.
29. Kincaid, E. Z., and J. D. Ernst. 2003. Mycobacterium tuberculosis exerts gene-selective inhibition of transcriptional responses to IFN-gamma without inhibiting STAT1 function. J. Immunol. 171:2042-2049.
30. Kowalski, M. P., and G. B. Pier. 2004. Localization of cystic fibrosis transmembrane conductance regulator to lipid rafts of epithelial cells is required for Pseudomonas aeruginosa-induced cellular activation. J. Immunol. 172:418-425.
31. Lafont, F., L. Abrami, and F. G. van der Goot. 2004. Bacterial subversion of lipid rafts. Curr. Opin. Microbiol. 7:4-10.
32. Li, X., P. E. Massa, A. Hanidu, G. W. Peet, P. Aro, A. Savitt, S. Mische, J. Li, and K. B. Marcu. 2002. IKKalpha, IKKbeta, and NEMO/IKKgamma are each required for the NF-kappa B-mediated inflammatory response program. J. Biol. Chem. 277:45129-45140.
33. Manes, S., G. del Real, and A. C. Martinez. 2003. Pathogens: raft hijackers. Nat. Rev. Immunol. 3:557-568.
34. Nagabhushanam, V., A. Solache, L. M. Ting, C. J. Escaron, J. Y. Zhang, and J. D. Ernst. 2003. Innate inhibition of adaptive immunity: Mycobacterium tuberculosis induced IL-6 inhibits macrophage responses to IFN-gamma. J. Immunol. 171:4750-4757.
35. Newton, H. J., J. Sloan, V. Bennett-Wood, L. M. Adams, R. M. Robins-Browne, and E. L. Hartland. 2004. Contribution of long polar fimbriae to the virulence of rabbit-specific enteropathogenic Escherichia coli. Infect. Immun. 72:1230-1239.
36. Nguyen, D. H., and D. Taub. 2002. Cholesterol is essential for macrophage inflammatory protein 1 beta binding and conformational integrity of CC chemokine receptor 5. Blood 99:4298-4306.
37. Ramaswamy, M., L. Shi, M. M. Monick, G. W. Hunninghake, and D. C. Look. 2004. Specific inhibition of type I interferon signal transduction by respiratory syncytial virus. Am. J. Respir. Cell. Mol. Biol. 30:893-900.
38. Riff, J. D., J. W. Callahan, and P. M. Sherman. 2005. Cholesterol-enriched membrane microdomains are required for inducing host cell cytoskeleton rearrangements in response to attaching-effacing Escherichia coli. Infect. Immun. 73:7113-7125.
39. Schraw, W., Y. Li, M. S. McClain, F. G. van der Goot, and T. L. Cover. 2002. Association of Helicobacter pylori vacuolating toxin (VacA) with lipid rafts. J. Biol. Chem. 277:34642-34650.
40. Sehgal, P. B., G. G. Guo, M. Shah, V. Kumar, and K. Patel. 2002. Cytokine signaling: STATS in plasma membrane rafts. J. Biol. Chem. 277:12067-12074.
41. Sehgal, P. B., V. Kumar, G. Guo, and W. C. Murray. 2003. Different patterns of regulation of Tyr-phosphorylated STAT1 and STAT3 in human hepatoma Hep3B cells by the phosphatase inhibitor orthovanadate. Arch. Biochem. Biophys. 412:242-250.
42. Shen, Y., M. Naujokas, M. Park, and K. Ireton. 2000. InIB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell 103:501-510.
43. Sherman, P., R. Soni, M. Petric, and M. Karmali. 1987. Surface properties of the Vero cytotoxin-producing Escherichia coli O157:H7. Infect. Immun. 55:1824-1829.
44. Shtrichman, R., and C. E. Samuel. 2001. The role of gamma interferon in antimicrobial immunity. Curr. Opin. Microbiol. 4:251-259.
45. Shuai, K., and B. Liu. 2003. Regulation of JAK-STAT signalling in the immune system. Nat. Rev. Immunol. 3:900-911.
46. Simoncic, P. D., A. Lee-Loy, D. L. Barber, M. L. Tremblay, and C. J. McGlade. 2002. The T cell protein tyrosine phosphatase is a negative regulator of janus family kinase 1 and 3. Curr. Biol. 12:446-453.
47. + T cells in immunity to infection by the attaching and effacing pathogen Citrobacter rodentium. Infect. Immun. 71:5077-5086.
48. Simons, K., and D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell. Biol. 1:31-39.
49. (Erratum, Nat. Rev. Mol. Cell. Biol. 2:216.)
50. Sperandio, V., A. G. Torres, B. Jarvis, J. P. Nataro, and J. B. Kaper. 2003. Bacteria-host communication: the language of hormones. Proc. Natl. Acad. Sci. USA 100:8951-8956.
51. Stoiber, D., S. Stockinger, P. Steinlein, J. Kovarik, and T. Decker. 2001. Listeria monocytogenes modulates macrophage cytokine responses through STAT serine phosphorylation and the induction of suppressor of cytokine signaling 3. J. Immunol. 166:466-472.
52. Subramaniam, P. S., and H. M. Johnson. 2002. Lipid microdomains are required sites for the selective endocytosis and nuclear translocation of IFN-gamma, its receptor chain IFN-gamma receptor-1, and the phosphorylation and nuclear translocation of STAT1alpha. J. Immunol. 169:1959-1969.
53. Takaoka, A., Y. Mitani, H. Suemori, M. Sato, T. Yokochi, S. Noguchi, N. Tanaka, and T. Taniguchi. 2000. Cross talk between interferon-gamma and -alpha/beta signaling components in caveolar membrane domains. Science 288:2357-2360.
54. ten Hoeve, J., M. de Jesus Ibarra-Sanchez, Y. Fu, W. Zhu, M. Tremblay, M. David, and K. Shuai. 2002. Identification of a nuclear Stat1 protein tyrosine phosphatase. Mol. Cell. Biol. 22:5662-5668.
55. Ting, L. M., A. C. Kim, A. Cattamancbi, and J. D. Ernst. 1999. Mycobacterium tuberculosis inhibits IFN-gamma transcriptional responses without inhibiting activation of STAT1. J. Immunol. 163:3898-3906.
56. Torres, A. G., J. A. Giron, N. T. Perna, V. Burland, F. I. Blattner, F. Avelino-Flores, and J. B. Kaper. 2002. Identification and characterization of lpfABCC'DE, a fimbrial operon of enterohemorrhagic Escherichia coli O157: H7. Infect. Immun. 70:5416-5427.
57. Wong, C. S., S. Jelacic, R. L. Habeeb, S. L. Watkins, and P. I. Tarr. 2000. The risk of the hemolytic-uremic syndrome after antibiotic treatment of Escherichia coli O157:H7 infections. N. Engl. J. Med. 342:1930-1936.
58. Yu, Y., and K. Chadee. 1997. Entamoeba histolytica stimulates interleukin 8 from human colonic epithelial cells without parasite-enterocyte contact. Gastroenterology 112:1536-1547.
59. Zareie, M., J. Riff, K. Donato, D. M. McKay, M. H. Perdue, J. D. Soderholm, M. A. Karmali, M. B. Cohen, J. Hawkins, and P. M. Sherman. 2005. Novel Effects of the prototype translocating Escherichia coli, strain C25, on intestinal epithelial structure and barrier function. Cell. Microbiol. 7:1782-1797.
60. Zobiack, N., U. Rescher, S. Laarmann, S. Michgehl, M. A. Schmidt, and V. Gerke. 2002. Cell-surface attachment of pedestal-forming enteropathogenic E. coli induces a clustering of raft components and a recruitment of annexin 2. J. Cell Sci. 115:91-98.