A third secreted protein that is encoded by the enteropathogenic Escherichia coli pathogenicity island is required for transduction of signals and for attaching and effacing activities in host cells

Infection and Immunity

Volumn 65, Issue 6, 1997, Pages 2211-2217

  Lai, Li Ching ^a   Wainwright, Leslie A ^b   Stone, Kelly D ^a   Donnenberg, Michael S ^a  

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

^b University of Maryland School of Medicine Center for Vaccine Development   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; OUTER MEMBRANE PROTEIN;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL OUTER MEMBRANE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CONTROLLED STUDY; GENE LOCUS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN SECRETION; SIGNAL TRANSDUCTION;

EID: 0031009562     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.65.6.2211-2217.1997     Document Type: Article

References (50)

1. Allaoui, A., P. J. Sansonettl, and C. Pursot. 1993. MxiD, an outer membrane protein necessary for the secretion of the Shigclla flexneri Ipa invasins. Mol. Microbiol. 7:59-68.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
3. Andrews, G. P., and A. T. Maurelli. 1992. mxiA of Shigella flexneri 2a, which facilitates export of invasion plasmid antigens, encodes a homolog of the low-calcium-rcsponsc protein. LcrD, of Yersinia pestis. Infect. Immun. 60:3287-3295.
4. Chen, E. Y., and P. H. Seeburg. 1985. Supercoil sequencing: a fast and simple method for sequencing plasmid DNA. DNA 4:165-170.
5. Chikami, G. K., J. Fierer, and D. G. Guiney. 1985. Plasmid-mediated virulence in Salmonella dublin demonstrated by use of a Tn5-oriT construct. Infect. Immun. 50:420-424.
6. Collazo, C. M., and J. E. Galán. 1996. Requirement for exported proteins in secretion through the invasion-associated type III system of Salmonella typhimurium. Infect. Immun. 64:3524-3531.
7. Donnenberg, M. S. 1995. Enteropathogenic Escherichia coli, p. 709-726. In M. J. Blaser, P. D. Smith, J. I. Ravdin, H. B. Greenberg, and R. L. Guerrant (ed.), Infections of the gastrointestinal tract. Raven Press. Ltd., New York, N.Y.
8. Donnenberg, M. S., S. B. Calderwood, A. Donuhue-Rolfe, G. T. Keusch, and J. B. Kaper. 1990. Construction and analysis of TnphoA mutants of enteropathogenic Escherichia coli unable to invade HEp-2 cells. Infect. Immun. 58:1565-1571.
9. Donnenberg, M. S., and J. B. Kaper. 1991. Construction of an eae deletion mutant of entrropathogenic Escherichia coli by using a positive-selection suicide vector. Infect. Immun. 59:4310-4317.
10. Donnenberg, M. S., and J. P. Nataro. 1995. Methods for studying adhesion of diarrheagenic Escherichia coli. Methods Enzymol. 253:324-336.
11. Donnenberg, M. S., J. Yu, and J. B. Kaper. 1993. A second chromosomal gene necessary for intimate attachment of enteropathogenic Escherichia coli to epithelial cells. J. Bacteriol. 175:4670-4680.
12. Ebel, F., C. Deibel, A. U. Kresse, C. A. Guzmán, and T. Chakruborty. 1996. Temperature- and medium-dependent secretion of proteins by Shiga toxin-producing Escherichia coli. Infect. Immun. 64:4472-4479.
13. Finlay, B. B., I. Rosensninc, M. S. Donnenberg, and J. B. Kaper. 1992. Cytoskeletal composition of attaching and effacing lesions associated with enteropathogenic Escherichia coli adherence to HeLa cells. Infect. Immun. 60:2541-2543.
14. Foubister, V., I. Rosenshine, M. S. Donnenberg, and B. B. Finlay. 1994. The eaeB gene of enteropathogenic Escherichia coli is necessary for signal transduction in epithelial cells. Infect. Immun. 62:3038-3040.
15. Groisman, E. A., and H. Ochman. 1996. Pathogenicity islands: bacterial evolution in quantum leaps. Cell 87:791-794.
16. Hakansson, S., E. E. Galyov, R. Rosqvist, and H. Wolf-Watz. 1996. The Yersinia YpkA Ser/Thr kinase is translocated and subsequently targeted to the inner surface of the HeLa cell plasma membrane. Mol. Microbiol. 20:593-603.
17. Hueck, C. J., M. J. Hantman, V. Bajaj, C. Johnston, C. A. Lee, and S. I. Miller. 1995. Salmonella typhimurium secreted invasion determinants are homologous to Shigella Ipa proteins. Mol. Microbiol. 18:479-490.
18. Jarvis, K. G., J. A. Girón, A. E. Jerse, T. K. McDaniel, M. S. Donncnberg, and J. B. Kaper. 1995. Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc. Natl. Acad. Sci. USA 92:7996-8000.
19. Jurvis, K. G., and J. B. Kaper. 1996. Secretion of extracellular proteins by enterohcmorrhagic Escherichia coli via a putative type III secretion system. Infect. Immun. 64:4826-4829.
20. Jerse, A. E., and J. B. Kaper. 1991. The eae gene of enteropathogenic Escherichia coli encodes a 94-kilodalton membrane protein, the expression of which is influenced by the EAF plasmid. Infect. Immun. 59:4302-4309.
21. Kaniga, K., D. Trollinger, and J.E. Galán. 1995. Identification of two targets of the type III protein secretion system encoded by the inv and spa loci of Salmonella typhimurium that have homology to the Shigella IpaD and IpaA proteins. J. Bacteriol. 177:7078-7085.
22. Kaniga, K., S. Tucker, D. Trollinger, and J. E. Galán. 1995. Homologs of the Shigella IpaB and IpaC invasins are required for Salmonella typhimuriun entry into cultured epithelial cells. J. Bacteriol. 177:3965-3971.
23. Kenny, B., and B. B. Finlay. 1445. Protein secretion by enteropathogenic Escherichia coli is essential for transducing signals to epithelial cells. Proc. Natl. Acad. Sci. USA 92:7991-7995.
24. Kenny, B., L.-C. Lai, B. B. Finlay, and M. S. Donnenberg. 1996. EspA, a protein secreted by enteropathogenic Escherichia coli (EPEC), is required to induce signals in epithelial cells. Mol. Mierobiol. 20:313-323.
25. Knutton, S., T. Baldwin, P. H. Williams, and A. S. McNeish. 1989. Actin accumulation at sites of bacterial adhesion to tissue culture cells: basis of a new diagnostic test tor enteropathogenic and enterohemorrhagic Escherichia coli. Infect. Immun. 57:1290-1298.
26. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
27. Levine, M. M., J. P. Nataro, H. Karch, M. M. Baldini, J. B. Kaper, R. E. Black, M. L. Clements, and A. D. O'Brien. 1485. The diarrheal response of humans to some classic serotypes of enteropathogenic Eschtrichia coli is dependent on a plasmid encoding an enteroadhesiveness factor. J. Infect. Dis. 152:550-559.
28. Manjarrez-Hernandez, H. A., T. J. Baldwin, P. H. Williams, R. Halgh, S. Knutton, and A. Aitken. 1996. Phosphorylation of myosin light chain at distinct sites and its association with the cytoskeleton during enteropathogenic Escherichia colt infection. Infect. Immun. 64:2368-2370.
29. Matsudaira, P. 1987. Sequence from picomole quantities of proteins electronblotted onto polyvinylidene difluoride membranes. J. Biol. Chem. 262:10035-10038.
30. McDaniel, T. K. 1996. Ph.D. thesis. University of Maryland at Baltimore, Baltimore, Md.
31. McDaniel, T. K., K. G. Jarvis, M. S. Donnenberg, and J. B. Kaper. 1995. A genetic locus of enterocytc effacement conserved among diverse enterobacterial pathogens. Proc. Natl. Acad. Sci. USA 92:1664-1668.
32. McDaniel, T. K., and J. B. Kaper. 1997. A cloned pathogenicity island from enteropathogenic Escherichiu coli confers the attaching and effacing phenotype on K-12 E. coli. Mol. Mierobiol. 23:399-407.
33. Mecsas, J. J., and E. J. Strauss. 1996. Molecular mechanisms of bacterial virulence: type III secretion and pathogenicity islands. Emerg. Infect. Dis. 2:270-288.
34. Ménard, R., P. Sansonetti, and C. Parsot. 1994. The secretion of the Shigella flexneri Ipu invasins is activated by epithelial cells and controlled by IpaB and IpaD. EMBO J. 13:5293-5302.
35. Ménard, R., P. J. Sansonetti, and C. Parsot. 1993. Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J. Bacteriol. 175:5899-5906.
36. Michiels, T., P. Wattiau, R. Brasseur, J. M. Ruysschaert, and G. Cornelis. 1990. Secretion of Yop proteins by Yersiniac. Infect. Immun. 58:2840-2849.
37. Rabinowitz, R. P., L.-C. Lai, K. Jarvis, T. K. McDaniel, J. B. Kaper, K. D. Stone, and M. S. Donnenberg. 1996. Attaching and effacing of host cells by enteropathogenic Escherichia coli in the absence of detectable tyrosine kinase mediated signal transduction. Microb. Pathog. 21:157-171.
38. Rosenshine, I., M. S. Donnenberg, J. B. Kaper, and B. B. Finlay. 1992. Signal exchange between enteropathogenic Escherichia coli (EPEC) and epithelial cells: EPEC induce tyrosine phosphorylation of host cell protein to initiate cytoskeletal rearrangement and bacterial uptake. EMBO J. 11:3551-3560.
39. Rosenshine, I., S. Ruschkowski, M. Stein, D. J. Reinscheid, S. D. Mills, and B. B. Finlay. 1996. A pathogenic bacterium triggers epithelial signals to form a functional bacterial receptor that mediates actin pseudopod formation. EMBO J. 15:2613-2624.
40. Rosqvist, R., K.-E. Magnusson, and H. Wolf-Watz. 1994. Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J. 13:964-972.
41. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
42. Sory, M.-P., and G. R. Cornelis. 1994. Translocation of a hybrid YopE-adenylatc cyclasc from Yersinia enterocolitica into HeLa cells. Mol. Microbiol. 14:583-594.
43. Sory, M. P., A. Boland, I. Lambermont, and G. R. Cornelis. 1995. Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach. Proc. Natl. Acad. Sci. USA 92:11998-12002.
44. Stein, M., B. Kenny, M. A. Stein, and B. B. Finlay. 1996. Characterization of EspC. a 110-kilodalton protein secreted by enteropathogenic Escherichia coli which is homologous to members of the immunoglobulin A protease-like family of secreted proteins. J. Bacteriol. 178:6546-6554.
45. Stone, K. D., H.-Z. Zhang, L. K. Carlson, and M. S. Donnenberg. 1996. A cluster of fourteen genes from enteropathogenic Escherichia coli is sufficient for biogenesis of a type IV pilus. Mol. Mierobiol. 20:325-337.
46. Studier, F. W., and B. A. Moffatt. 1986. Use of bacteriophage T7 RNA polymerasc to direct selective high-level expression of cloned genes. J. Mol. Biol. 189:113-130.
47. Tabor, S., and C. C. Richardson. 1985. A hacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl. Acad. Sec. USA 82:1074-1078.
48. Watarai, M. T. Tobe, M. Yoshikawa, and C. Sasakawa. 1995. Contact of Shigella with host cells triggers release of Ipa invasins and is an essential function of invasiveness. EMBO J. 14:2461-2470.
49. Yahr, T. L., J. Goranson, and D. W. Frank. 1996. Exoenzymc S of Pseudomonas aeruginosa is secreted by a type III pathway. Mol. Microbiol. 22:991-1003.
50. Zierler, M. K., and J. E. Galán. 1995. Contact with cultured epithelial cells stimulates secretion of Salmonella typhimurium invasion protein InvJ. Infect. Immun. 63:4024-4028.