Effect of Escherichia coli STb toxin on NIH-3T3 cells

FEMS Immunology and Medical Microbiology

Volumn 55, Issue 3, 2009, Pages 432-441

  Gonçalves, Carina ^a   Dubreuil, J Daniel ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Cell alteration; Escherichia coli; Mitochondria; Permeabilization; STb toxin

Indexed keywords

BACTERIAL TOXIN; CARBOXYFLUORESCEIN DIACETATE SUCCINIMIDYL ESTER; ESTERASE; FLUORESCEIN ISOTHIOCYANATE; PROPIDIUM IODIDE; TOXIN STB; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL STRAIN 3T3; CELL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ESCHERICHIA COLI; FLOW CYTOMETRY; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BACTERIAL TOXINS; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CYTOPLASM; ENTEROTOXINS; ESCHERICHIA COLI; ESTERASES; FIBROBLASTS; FLOW CYTOMETRY; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICROSCOPY, CONFOCAL; MITOCHONDRIA; NIH 3T3 CELLS; ORGANELLES;

EID: 62149105097     PISSN: 09288244     EISSN: 1574695X     Source Type: Journal    
DOI: 10.1111/j.1574-695X.2009.00541.x     Document Type: Article

References (48)

1. Arriaga YL, Harville BA Dreyfus LA (1995) Contribution of individual disulfide bonds to biological action of Escherichia coli heat-stable enterotoxin B. Infect Immun 63 : 4715 4720.
2. Beausoleil HE Dubreuil JD (2001) In vitro binding characteristics and affinity for sulfatide of Escherichia coli STb enterotoxin. Receptor Channels 7 : 401 411.
3. Beausoleil HE, Labrie V Dubreuil JD (2002) Trypan blue uptake by chinese hamster ovary cultured epithelial cells: a cellular model to study Escherichia coli STb enterotoxin. Toxicon 40 : 185 191.
4. Blanke SR (2005) Micro-managing the executioner: pathogen targeting of mitochondria. Trends Microbiol 13 : 64 71.
5. Braun JS, Hoffmann O, Schickhaus M, Freyer D, Dagand E, Bermpohl D, Mitchell TJ, Bechmann I Weber JR (2007) Pneumolysin causes neuronal cell death through mitochondrial damage. Infect Immun 75 : 4245 4254.
6. Chao KL Dreyfus LA (1997) Interaction of Escherichia coli heat-stable enterotoxin B with cultured human intestinal epithelial cells. Infect Immun 65 : 3209 3217.
7. Chao KL Dreyfus LA (1999) Interaction of Escherichia coli heat-stable enterotoxin B with rat intestinal epithelial cells and membrane lipids. FEMS Microbiol Lett 172 : 91 97.
8. Cossarizza A Salvioli S (2001) Analysis of mitochondria during cell death. Method Cell Biol 63 : 467 486.
9. Cover TL Blanke SR (2005) Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat Rev 3 : 320 332.
10. Dreyfus LA, Harville B, Howard DE, Shaban R, Beatty DM Morris SJ (1993) Calcium influx mediated by the Escherichia coli heat-stable enterotoxin B (STB). P Natl Acad Sci USA 90 : 3202 3206.
11. Dubreuil JD (1997) Escherichia coli STb enterotoxin. Microbiology 143 : 1783 1795.
12. Dubreuil JD (2008) Escherichia coli STb toxin and colibacillosis: knowing is half the battle. FEMS Microbiol Lett 278 : 137 145.
13. Dubreuil JD, Penel S Gonçalves C (2007) Escherichia coli STb enterotoxin toxicity and internalization investigations: a mini-review. Res J Microbiol 2 : 209 215.
14. Fujii Y, Kondo Y Okamoto K (1995) Involvement of prostaglandin E2 synthesis in the intestinal secretory action of Escherichia coli heat-stable enterotoxin II. FEMS Microbiol Lett 130 : 259 265.
15. Fujii Y, Nomura T, Yamanaka H Okamoto K (1997) Involvement of Ca(2+)-calmodulin-dependent protein kinase II in the intestinal secretory action of Escherichia coli heat-stable enterotoxin II. Microbiol Immunol 41 : 633 636.
16. Gerhardt R, Burger S, Tatge H, Genth H, Just I Hofman F (2005) Comparison of wild type with recombinant Clostridium difficile toxin A. Microb Pathogenesis 38 : 77 83.
17. Giovannini C, Mataresse P, Scazzocchio B, Sanchez M, Masella R Malorni W (2002) Mitochondria hyperpolarization is an early event in oxidized low-density lipoprotein-induced apoptosis in Caco-2 intestinal cells. FEBS Lett 523 : 200 206.
18. Gogvadze V Orrenius S (2006) Mitochondrial regulation of apoptotic cell death. Chem-Biol Interact 163 : 4 14.
19. Gonçalves C, Vachon V, Schwartz JL Dubreuil JD (2007) The Escherichia coli enterotoxin STb permeabilizes piglet jejunal brush border membrane vesicles. Infect Immun 75 : 2208 2213.
20. Gonçalves C, Berthiaume F, Mourez M Dubreuil JD (2008) Escherichia coli STb toxin binding to sulfatide and its inhibition by carragenan. FEMS Microbiol Lett 281 : 30 35.
21. Handl CE, Harel J, Flock JI Dubreuil JD (1993) High yield of active STb enterotoxin from a fusion protein (MBP-STb) expressed in Escherichia coli. Protein Expres Purif 4 : 275 281.
22. Harel J, Lapointe H, Fallara A, Lortie LA, Bigras-Poulin M, Larivière S Fairbrother JM (1991) Detection of genes for fimbrial antigens and enterotoxins associated with Escherichia coli serogroups isolated from pigs with diarrhea. J Clin Microbiol 29 : 745 752.
23. Hitotsubashi S, Fujii Y, Yamanaka H Okamoto K (1992) Some properties of purified Escherichia coli heat-stable enterotoxin II. Infect Immun 60 : 4468 4474.
24. Kupersztoch YM, Tachias K, Moomaw CR, Dreyfus LA, Urban R, Slaughter C Whipp S (1990) Secretion of methanol-insoluble heat-stable enterotoxin (STB): energy- and secA-dependent conversion of pre-STB to an intermediate indistinguishable from the extracellular toxin. J Bacteriol 172 : 2427 2432.
25. Labrie V, Beausoleil HE, Harel J Dubreuil JD (2001a) Binding to sulfatide and enterotoxicity of various Escherichia coli STb mutants. Microbiology 147 : 3141 3148.
26. Labrie V, Harel J Dubreuil JD (2001b) Oligomerization of Escherichia coli enterotoxin b through its C-terminal hydrophobic alpha-helix. Biochim Biophys Acta 1535 : 128 133.
27. Labrie V, Harel J Dubreuil JD (2002) Escherichia coli heat-stable enterotoxin b (STb) in vivo internalization within rat intestinal epithelial cells. Vet Res 33 : 223 228.
28. Le PU Nabi IR (2003) Distinct caveolae-mediated endocytic pathways target the Golgi apparatus and the endoplasmic reticulum. J Cell Sci 116 : 1059 1071.
29. Lee CH, Moseley SL, Moon HW, Whipp SC, Gyles CL So M (1983) Characterization of the gene encoding heat-stable toxin II and preliminary molecular epidemiological studies of enterotoxigenic Escherichia coli heat-stable toxin II producers. Infect Immun 42 : 264 268.
30. Lugli E, Troiano L, Ferraresi R, Roat E, Prada N, Nasi M, Pinti M, Cooper EL Cossarizza A (2005) Characterization of cells with different mitochondrial membrane potential during apoptosis. Cytometry A 68 : 28 35.
31. Lyamzaev KG, Nepryakhina OK, Saprunova VB, Bakeeva LE, Pletjushkina OY, Chernyak BV Skulachev VP (2008) Novel mechanism of elimination of malfunctioning mitochondria (mitopsis): formulation of mitoptic bodies and extrusion of mitochondrial material from the cell. Biochim Biophys Acta 1777 : 817 825.
32. Matarrese P, Falzano L, Fabbri A, Gambardella L, Frank C, Geny B, Popoff MR, Malorni W Fiorentini C (2007) Clostridium difficile toxin B causes apoptosis in epithelial cells thrilling mitochondria. J Biol Chem 282 : 9029 9041.
33. Müller A, Gunther D, Brinkmann V, Hurwitz R, Meyer TF Rudel T (2000) Targeting of the pro-apoptotic VDAC-like porin (PorB) of Neisseria gonorrhoeae to mitochondria of infected cells. EMBO J 19 : 5332 5343.
34. Ohnishi H, Miyake M, Kamitani S Horiguchi Y (2008) The morphological changes in cultured cells caused by Bordetella pertussis adenylate cyclase toxin. FEMS Microbiol Lett 279 : 174 179.
35. Okamoto K, Baba T, Yamanaka H, Akashi N Fujii Y (1995) Disulfide bond formation and secretion of Escherichia coli heat-stable enterotoxin II. J Bacteriol 177 : 4579 4586.
36. Peterson JW Whipp SC (1995) Comparison of the mechanisms of action of cholera toxin and the heat-stable enterotoxins of Escherichia coli. Infect Immun 63 : 1452 1461.
37. Reers M, Smiley ST, Mottola-Hartshorn C, Chen A, Lin M Chen LB (1995) Mitochondrial membrane potential monitored by JC-1 dye. Method Enzymol 260 : 406 417.
38. Rose R, Whipp SC Moon HW (1987) Effects of Escherichia coli heat-stable enterotoxin b on small intestinal villi in pigs, rabbits, and lambs. Vet Pathol 24 : 71 79.
39. Rousset E, Harel J Dubreuil JD (1998) Sulfatide from the pig jejunum brush border epithelial cell surface is involved in binding of Escherichia coli enterotoxin b. Infect Immun 66 : 5650 5658.
40. Santos JH, Hunakova L, Chen Y, Bortner C Van Houten B (2003) Cell sorting experiments link persistent mitochondrial DNA damage with loss of mitochondrial membrane potential and apoptotic cell death. J Biol Chem 278 : 1728 1734.
41. Schwarz M, Andrade-Navarro MA Gross A (2007) Mitochondrial carriers and pores: key regulators of the mitochondrial apoptotic program? Apoptosis 12 : 869 876.
42. Skulachev VP (2006) Bioenergetic aspects of apoptosis, necrosis and mitoptosis. Apoptosis 11 : 473 485.
43. Smiley ST, Reers M, Mottola-Hartshorn C, Lin M, Chen A, Smith TW, Steele Jr. GD Chen LB (1991) Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. P Natl Acad Sci USA 88 : 3671 3675.
44. Sukumar M, Rizo J, Wall M, Dreyfus LA, Kupersztoch YM Gierasch LM (1995) The structure of Escherichia coli heat-stable enterotoxin b by nuclear magnetic resonance and circular dichroism. Protein Sci 4 : 1718 1729.
45. Thress K, Kornbluth S Smith JJ (1999) Mitochondria at the crossroad of apoptotic cell death. J Bioenerg Biomembr 31 : 321 326.
46. Whipp SC, Moseley SL Moon HW (1986) Microscopic alterations in jejunal epithelium of 3-week-old pigs induced by pig-specific, mouse-negative, heat-stable Escherichia coli enterotoxin. Am J Vet Res 47 : 615 618.
47. Whipp SC, Kokue E, Morgan RW, Rose R Moon HW (1987) Functional significance of histologic alterations induced by Escherichia coli pig-specific, mouse-negative, heat-stable enterotoxin (STb). Vet Res Commun 11 : 41 55.
48. Willhite DC Blanke SR (2004) Helicobacter pylori vacuolating cytotoxin enters cells, localizes to the mitochondria, and induces mitochondrial membrane permeability changes correlated to toxin channel activity. Cell Microbiol 6 : 143 154.