Heat-labile enterotoxin-induced activation of NF-κB and MAPK pathways in intestinal epithelial cells impacts enterotoxigenic Escherichia coli (ETEC) adherence

Cellular Microbiology

Volumn 14, Issue 8, 2012, Pages 1231-1241

  Wang, Xiaogang ^a   Gao, Xiaofei ^a   Hardwidge, Philip R ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; ENTEROTOXIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; RAP1 PROTEIN; STRESS ACTIVATED PROTEIN KINASE;

ARTICLE; BACTERIUM ADHERENCE; CONTROLLED STUDY; ENTEROTOXIGENIC ESCHERICHIA COLI; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

BACTERIAL ADHESION; BACTERIAL TOXINS; CELL LINE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENTEROTOXIGENIC ESCHERICHIA COLI; ENTEROTOXINS; ENZYME ACTIVATION; EPITHELIAL CELLS; ESCHERICHIA COLI PROTEINS; HOST-PATHOGEN INTERACTIONS; INTESTINAL MUCOSA; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; TELOMERE-BINDING PROTEINS;

ESCHERICHIA COLI;

EID: 84863993438     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2012.01793.x     Document Type: Article

References (35)

1. Allen, K.P., Randolph, M.M., and Fleckenstein, J.M. (2006) Importance of heat-labile enterotoxin in colonization of the adult mouse small intestine by human enterotoxigenic Escherichia coli strains. Infect Immun 74: 869-875.
2. Arthur, W.T., Quilliam, L.A., and Cooper, J.A. (2004) Rap1 promotes cell spreading by localizing Rac guanine nucleotide exchange factors. J Cell Biol 167: 111-122.
3. Bandyopadhaya, A., Das, D., and Chaudhuri, K. (2009) Involvement of intracellular signaling cascades in inflammatory responses in human intestinal epithelial cells following Vibrio cholerae infection. Mol Immunol 46: 1129-1139.
4. Beatty, M.E., Adcock, P.M., Smith, S.W., Quinlan, K., Kamimoto, L.A., Rowe, S.Y., etal. (2006) Epidemic diarrhea due to enterotoxigenic Escherichia coli. Clin Infect Dis 42: 329-334.
5. Berberov, E., Zhou, Y., Francis, D., Scott, M., Kachman, S., and Moxley, R. (2004) Relative importance of heat-labile enterotoxin in the causation of severe diarrheal disease in the gnotobiotic piglet model by a strain of enterotoxigenic Escherichia coli that produces multiple enterotoxins. Infect Immun 72: 3914-3924.
6. Borland, G., Smith, B.O., and Yarwood, S.J. (2009) EPAC proteins transduce diverse cellular actions of cAMP. Br J Pharmacol 158: 70-86.
7. Caron, E. (2003) Cellular functions of the Rap1 GTP-binding protein: a pattern emerges. J Cell Sci 116: 435-440.
8. Chakraborty, K., Ghosh, S., Koley, H., Mukhopadhyay, A.K., Ramamurthy, T., Saha, D.R., etal. (2008) Bacterial exotoxins downregulate cathelicidin (hCAP-18/LL-37) and human beta-defensin 1 (HBD-1) expression in the intestinal epithelial cells. Cell Microbiol 10: 2520-2537.
9. Chutkan, H., and Kuehn, M.J. (2011) Context-dependent activation kinetics elicited by soluble versus outer membrane vesicle-associated heat-labile enterotoxin. Infect Immun 79: 3760-3769.
10. Evans, D.G., Silver, R.P., Evans, D.J., Jr, Chase, D.G., and Gorbach, S.L. (1975) Plasmid-controlled colonization factor associated with virulence in Esherichia coli enterotoxigenic for humans. Infect Immun 12: 656-667.
11. Finkelstein, R.A., Boesman, M., Neoh, S.H., LaRue, M.K., and Delaney, R. (1974) Dissociation and recombination of the subunits of the cholera enterotoxin (choleragen). J Immunol 113: 145-150.
12. Fleckenstein, J.M., Hardwidge, P.R., Munson, G.P., Rasko, D.A., Sommerfelt, H., and Steinsland, H. (2010) Molecular mechanisms of enterotoxigenic Escherichia coli infection. Microbes Infect 12: 89-98.
13. Guha, M., and Mackman, N. (2001) LPS induction of gene expression in human monocytes. Cell Signal 13: 85-94.
14. Huang, D.B., DuPont, H.L., Jiang, Z.D., Carlin, L., and Okhuysen, P.C. (2004) Interleukin-8 response in an intestinal HCT-8 cell line infected with enteroaggregative and enterotoxigenic Escherichia coli. Clin Diagn Lab Immunol 11: 548-551.
15. Jin, A., Kurosu, T., Tsuji, K., Mizuchi, D., Arai, A., Fujita, H., etal. (2006) BCR/ABL and IL-3 activate Rap1 to stimulate the B-Raf/MEK/Erk and Akt signaling pathways and to regulate proliferation, apoptosis, and adhesion. Oncogene 25: 4332-4340.
16. Johnson, A., Kaushik, R., Francis, D., Fleckenstein, J., and Hardwidge, P. (2009) Heat-labile enterotoxin promotes Escherichia coli adherence to intestinal epithelial cells. J Bacteriol 191: 178-186.
17. Lalli, E., and Sassone-Corsi, P. (1994) Signal transduction and gene regulation: the nuclear response to cAMP. J Biol Chem 269: 17359-17362.
18. Li, Q., and Verma, I.M. (2002) NF-kappaB regulation in the immune system. Nat Rev Immunol 2: 725-734.
19. Lin, C.H., Cheng, H.W., Ma, H.P., Wu, C.H., Hong, C.Y., and Chen, B.C. (2011) Thrombin induces NF-{kappa}B activation and IL-8/CXCL8 expression in lung epithelial cells by a Rac1-dependent PI3K/Akt pathway. J Biol Chem 286: 10483-10494.
20. Madrid, L.V., Mayo, M.W., Reuther, J.Y., and Baldwin, A.S., Jr (2001) Akt stimulates the transactivation potential of the RelA/p65 Subunit of NF-kappa B through utilization of the Ikappa B kinase and activation of the mitogen-activated protein kinase p38. J Biol Chem 276: 18934-18940.
21. Matos, P., and Jordan, P. (2006) Rac1, but not Rac1B, stimulates RelB-mediated gene transcription in colorectal cancer cells. J Biol Chem 281: 13724-13732.
22. Misra, U.K., Kaczowka, S., and Pizzo, S.V. (2008) The cAMP-activated GTP exchange factor, Epac1 upregulates plasma membrane and nuclear Akt kinase activities in 8-CPT-2-O-Me-cAMP-stimulated macrophages: gene silencing of the cAMP-activated GTP exchange Epac1 prevents 8-CPT-2-O-Me-cAMP activation of Akt activity in macrophages. Cell Signal 20: 1459-1470.
23. Moen, S.T., Blumentritt, C.A., Slater, T.M., Patel, S.D., Tutt, C.B., Estrella-Jimenez, M.E., etal. (2010) Testing the efficacy and toxicity of adenylyl cyclase inhibitors against enteric pathogens using in vitro and in vivo models of infection. Infect Immun 78: 1740-1749.
24. Moon, E.Y., and Pyo, S. (2007) Lipopolysaccharide stimulates Epac1-mediated Rap1/NF-kappaB pathway in Raw 264.7 murine macrophages. Immunol Lett 110: 121-125.
25. Moxley, R.A., Berberov, E.M., Francis, D.H., Xing, J., Moayeri, M., Welch, R.A., etal. (1998) Pathogenicity of an enterotoxigenic Escherichia coli hemolysin (hlyA) mutant in gnotobiotic piglets. Infect Immun 66: 5031-5035.
26. Ponsioen, B., Gloerich, M., Ritsma, L., Rehmann, H., Bos, J.L., and Jalink, K. (2009) Direct spatial control of Epac1 by cyclic AMP. Mol Cell Biol 29: 2521-2531.
27. de Rooij, J., Zwartkruis, F.J., Verheijen, M.H., Cool, R.H., Nijman, S.M., Wittinghofer, A., and Bos, J.L. (1998) Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396: 474-477.
28. Rothermel, J.D., Stec, W.J., Baraniak, J., Jastorff, B., and Botelho, L.H. (1983) Inhibition of glycogenolysis in isolated rat hepatocytes by the Rp diastereomer of adenosine cyclic 3′, 5′-phosphorothioate. J Biol Chem 258: 12125-12128.
29. Rowe, B., Taylor, J., and Bettelheim, K.A. (1970) An investigation of traveller's diarrhoea. Lancet 1: 1-5.
30. Sanlioglu, S., Williams, C.M., Samavati, L., Butler, N.S., Wang, G., McCray, P.B., Jr, etal. (2001) Lipopolysaccharide induces Rac1-dependent reactive oxygen species formation and coordinates tumor necrosis factor-alpha secretion through IKK regulation of NF-kappa B. J Biol Chem 276: 30188-30198.
31. Sears, C.L., and Kaper, J.B. (1996) Enteric bacterial toxins: mechanisms of action and linkage to intestinal secretion. Microbiol Rev 60: 167-215.
32. Sehrawat, S., Cullere, X., Patel, S., Italiano, J., Jr, and Mayadas, T.N. (2008) Role of Epac1, an exchange factor for Rap GTPases, in endothelial microtubule dynamics and barrier function. Mol Biol Cell 19: 1261-1270.
33. Tompkins, W.A., Watrach, A.M., Schmale, J.D., Schultz, R.M., and Harris, J.A. (1974) Cultural and antigenic properties of newly established cell strains derived from adenocarcinomas of the human colon and rectum. J Natl Cancer Inst 52: 1101-1110.
34. Turner, S.M., Scott-Tucker, A., Cooper, L.M., and Henderson, I.R. (2006) Weapons of mass destruction: virulence factors of the global killer enterotoxigenic Escherichia coli. FEMS Microbiol Lett 263: 10-20.
35. Vossler, M.R., Yao, H., York, R.D., Pan, M.G., Rim, C.S., and Stork, P.J. (1997) cAMP activates MAP kinase and Elk-1 through a B-Raf- and Rap1-dependent pathway. Cell 89: 73-82.