Host cell death due to enteropathogenic Escherichia coli has features of apoptosis

Infection and Immunity

Volumn 67, Issue 5, 1999, Pages 2575-2584

  Crane, John K ^a,b   Majumdar, Swastika ^a   Pickhardt III, Donald F ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b Dept of Microbiology and Immunology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; GENISTEIN; LACTATE DEHYDROGENASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLSERINE; PROPIDIUM IODIDE; PROTEIN TYROSINE KINASE; TRYPAN BLUE; WORTMANNIN;

APOPTOSIS; ARTICLE; BACTERIUM ADHERENCE; COLON; CONTROLLED STUDY; DIARRHEA; EPITHELIUM CELL; ESCHERICHIA COLI; FLUORESCENCE; HELA CELL; HOST CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; QUANTITATIVE ASSAY;

EID: 0032925379     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.67.5.2575-2584.1999     Document Type: Article

References (51)

1. Baker, B., P. Zambryski, B. Staskawicz, and S. Dinesh-Kumar. 1997. Signaling in plant-microbe interactions. Science 276:726-733.
2. Baldwin, T., M. Lee-Delaunay, S. Knutton, and P. Williams. 1993. Calcium-calmodulin dependence of actin accretion and lethality in cultured HFp-2 cells infected with enteropathogenic Escherichia coli. Infect. Immun. 61:760-763.
3. Barnett-Foster, D., D. Philpott, M. Huesca, P. Sherman, and C. Lingwood. Comparison of enteropathogenic E. coli and enterohemorrhagic E. coli binding to lipid receptors. Gastroenterology, in press.
4. Beg, A., and D. Baltimore. 1996. An essential role for NF-κB in preventing TNF-α induced cell death. Science 274:782-784.
5. Bieber, D., S. Ramer, C.-Y. Wu, W. Murray, T. Tobe, R. Fernandez, and G. Schoolnik. 1998. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science 280:2114-2118.
6. Chen, Y., M. Smith, K. Thirumalai, and A. Zychlinsky. 1996. A bacterial invasin induces macrophage apoptosis by directly binding ICE. EMBO J. 15:3853-3860.
7. Clifton, D., R. Goss, S. Sahni, D. van Antwerp, R. Baggs, V. Marder, D. Silverman, and L. Sporn. 1998. NF-κB dependent inhibition of apoptosis is essential for host cell survival during Rickettsia rickettsii infection. Proc. Natl. Acad. Sci. USA 95:4646-4651.
8. Crane, J. K., and J. S. Oh. 1997. Activation of host cell protein kinase C by enteropathogenic Escherichia coli. Infect. Immun. 65:3277-3285.
9. DeLuca, C., H. Kwon, N. Pelletier, M. A. Wainberg, and J. Hiscott. 1998. NF-kappaB protects HIV-1-infected myeloid cells from apoptosis. Virology 244:27-38.
10. Donnenberg, M., and J. Kaper. 1991. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect. Immun. 59:4310-4317.
11. Elsinghorst, E. 1994. Measurement of invasion by gentamicin resistance. Methods Enzymol. 236:405-420.
12. Evans, C. A., J. M. Lord, P. J. Owen-Lynch, G. Johnson, C. Dive, and A. D. Whetton. 1995. Suppression of apoptosis by v-ABL protein tyrosine kinase is associated with nuclear translocation and activation of protein kinase C in an interleukin-3-dependent haemopoietic cell line. J. Cell Sci. 108:2591-2598.
13. Fagundes-Neto, U., E. Freymuller, L. Schimitz, and I. Scaletsky. 1996. Nutritional impact and ultrastructural intestinal alterations in severe infections due to enteropathogenic Escherichia coli strains in infants. J. Am. Coll. Nutr. 15:180-185.
14. Fan, T. H. Lu, H. Hu, L. Shi, G. McLarty, D. Nance, A. Greenberg, and G. Zhong. 1998. Inhibition of apoptosis in chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation. J. Exp. Med. 187:487-496.
15. Fernandez-Prada, C., B. Tall, S. Elliott, D. Hoover, J. Nataro, and M. Venkatesan. 1998. Hemolysin-positive enteroaggregative and cell-detaching Escherichia coli strains cause oncosis of human monocyte-derived macrophages and apoptosis of murine J774 cells. Infect. Immun. 66:3918-3924.
16. Fox, J. 1997. Current topics: some microbes elicit, others block apoptosis. ASM News 63:412-413.
17. Frankel, G., A. Phillips, I. Rosenshine, G. Dougan, J. Kaper, and S. Knutton. 1998. Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements. Mol. Microbiol. 30:911-921.
18. Gong, J., F. Traganos, and Z. Darzynkiewkz. 1994. A selective procedure for DNA extraction from apoptotic cells applicable for gel electrophoresis and flow cytometry. Anal. Biochem. 218:314-319.
19. Hall, P., P. J. Coates, B. Ansari, and D. Hopwood. 1994. Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis. J. Cell Sci. 107:3569-3577.
20. Iimuro, Y., T. Nishiura, C. Hellerbrand, K. E. Behrns, R. Schoonhoven, J. W. Grisham, and D. A. Brenner. 1998. NFkappaB prevents apoptosis and liver dysfunction during liver regeneration. J. Clin. Investig. 101:802-811.
21. Ireton, K., B. Payrastre, H. Chap, W. Ogawa, H. Sakaue, M. Kasuga, and P. Cossart. 1996. A role for phosphoinositide 3-kinase in bacterial invasion. Science 274:780-782.
22. Karnes, W. E., Jr., S. G. Weller, P. N. Adjei, T. J. Kottke, K. S. Glenn, G. J. Gores, and S. H. Kaufmann. 1998. Inhibition of epidermal growth factor receptor kinase induces protease-dependent apoptosis in human colon cancer cells. Gastroenterology 114:930-939.
23. Kerr, J., A. Wyllie, and A. Currie. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26:239-257.
24. Knutton, S., I. Rosenshine, M. J. Pallen, I. Nisan, B. C. Neves, C. Bain, C. Wolff, G. Dougan, and G. Frankel. 1998. A novel Espa-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. EMBO J. 17:2166-2176.
25. Kulik, G., A. Klippel, and M. Weber. 1997. Antiapoptotic signalling by the insulin-like growth factor I receptor, phosphatidylinositol 3-kinase, and Akt. Mol. Cell. Biol. 17:1595-1606.
26. Levine, M., D. Nalin, R. Hornick, E. Bergquist, D. Waterman, C. Young, S. Sotman, and B. Rowe. 1978. Escherichia coli strains that cause diarrhea but do not produce heat-labile or heat-stable enterotoxins and are not invasive. Lancet i:1119-1122.
27. Levine, M., J. Nataro, H. Karch, M. Baldini, J. Kaper, R. Black, M. Clements, and A. O'Brien. 1985. The diarrheal response of humans to some classic serotypes of enteropathogenic Escherichia coli is dependent on a plasmid encoding an enteroadhesiveness factor. J. Infect. Dis. 152:550-559.
28. Lindgren, S., and F. Heffron. 1997. To sting or be stung: bacteria-induced apoptosis. Trends Microbiol. 5:263-264.
29. Mannick, E. E., L. E. Bravo, G. Zarama, J. L. Realpe, X. J. Zhang, B. Ruiz, E. T. Fontham, R. Mera, M. J. Miller, and P. Correa. 1996. Inducible nitric oxide synthase, nitrotyrosine, and apoptosis in Helicobacter pylori gastritis: effect of antibiotics and antioxidants. Cancer Res. 56:3238-3243.
30. Messmer, U. K., E. G. Lapetina, and B. Brune. 1995. Nitric oxide-induced apoptosis in RAW 264.7 macrophages is antagonized by protein kinase C- and protein kinase A-activating compounds. Mol. Pharmacol. 47:757-765.
31. Monack, D., J. Mecsas, N. Ghori, and S. Falkow. 1997. Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death. Proc. Natl. Acad. Sci. USA 94:10385-10390.
32. Monack, D. M., B. Raupach, A. E. Hromockyj, and S. Falkow. 1996. Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc. Natl. Acad. Sci. USA 93:9833-9838.
33. Moss, S. F., J. Calam, B. Agarwal, S. Wang, and P. R. Holt. 1996. Induction of gastric epithelial apoptosis by Helicobacler pylori. Gut 38:498-501.
34. Oberdoerster, J., A. Kamer, and R. Rabin. 1998. Differential effect of ethanol on PC12 cell death. J. Pharmacol. Exp. Ther. 287:359-365.
35. Oberhammer, F., J. Wilson, C. Dive, I. Morris, J. Hickman, A. Wakeling, P. Walker, and M. Sikorska. 1993. Apoptotic death in epithelial cells: cleavage of DNA to 300 and/or 50 kb fragments prior to or in the absence of internucleosomal fragmentation. EMBO J. 12:3679-3684.
36. Perry, S., L. Epstein, and H. Gelbard. 1997. Simultaneous in situ detection of apoptosis and necrosis in monolayer cultures by TUNEL and trypan blue staining. BioTechniques 22:1102-1106.
37. Rosenshine, I., M. Donnenberg, J. Kaper, and B. Finlay. 1992. Signal transduction between enteropathogenic Escherichia coli (EPEC) and epithelial cells: EPEC induces tyrosine phosphorylation of host cell proteins to initiate cytoskeletal rearrangement and bacterial uptake. EMBO J. 11:3551-3560.
38. Rothbaum, R., A. McAdams, R. Giannella, and J. Partin. 1982. A clinicopathologic study of enterocyte-adherent Escherichia coli: a cause of protracted diarrhea in infants. Gastroenterology 83:441-454.
39. Rothbaum, R., J. Partin, K. Saalfield, and A. McAdams. 1983. An ultrastructural study of enteropathogenic Escherichia coli infection in human infants. Ultrastruct. Pathol. 4:291-304.
40. Ruckdeschel, K., S. Harb, A. Roggenkamp, M. Hornef, R. Zumbihl, S. Kohler, J. Heesemann, and B. Rouot. 1998. Yersinia enterocolitica impairs activation of transcription factor NF-kappaB: involvement in the induction of programmed cell death and in the suppression of the macrophage tumor necrosis factor alpha production. J. Exp. Med. 187:1069-1079.
41. Savkovic, S. D., A. Koutsouris, and G. Hecht 1997. Activation of NF-kappa-B in intestinal epithelial cells by enteropathogenic Escherichia coli. Am. J. Physiol. 42:C1160-C1167.
42. Van Antwerp, D., S. Martin, T. Kafri, D. Green, and I. Verma. 1996. Suppression of TNF-α-induced apoptosis by NF-κB. Science 274:787-789.
43. Vuopio-Varkila, J., and G. Schoolnik. 1991. Localized adherence by enteropathogenic Escherichia coli is an inducible phenotype associated with the expression of new outer membrane proteins. J. Exp. Med. 174:1167-1177.
44. Whelan, R. D., and P. J. Parker. 1998. Loss of protein kinase C function induces an apoptotic response. Oncogene 16:1939-1944.
45. Wooldridge, K. G., P. H. Williams, and J. M. Ketley. 1996. Host signal transduction and endocytosis of Campylobacter jejuni. Microb. Pathog. 21: 299-305.
46. Wu, M., Z. Ao, K. Prasad, R. Wu, and S. Schlossman. 1998. IEX-1L, an apoptosis inhibitor involved in NF-KB mediated cell survival. Science 281: 998-1001.
47. Zhang, G., V. Gurtu, S. Kain, and G. Van. 1997. Early detection of apoptosis using a fluorescent conjugate of Annexin V. BioTechniques 23:525-532.
48. Zychlinsky, A., and J. Moss. Personal communication.
49. Zychlinsky, A., M. Prevost, and P. Sansonetti. 1992. Shigella flexneri induces apoptosis in infected macrophages. Nature 358:167-169.
50. Zychlinsky, A., and P. J. Sansonetti. 1997. Apoptosis as a proinflammatory event: what can we learn from bacteria-induced cell death? Trends Microbiol. 5:201-204.
51. Zychlinsky, A., K. Thirumalai, J. Arondel, J. R. Cantey, A. O. Aliprantis, and P. J. Sansonetti. 1996. In vivo apoptosis in Shigella flexneri infections. Infect. Immun. 64:5357-5365.