The Yersinia YpkA Ser/Thr kinase is translocated and subsequently targeted to the inner surface of the HeLa cell plasma membrane

Molecular Microbiology

Volumn 20, Issue 3, 1996, Pages 593-603

  Håkansson, Sebastian ^a   Galyov, Edouard E ^a,b   Rosqvist, Roland ^a   Wolf Watz, Hans ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOTRANSFERASE;

ARTICLE; BACTERIAL VIRULENCE; CELL MEMBRANE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; HELA CELL; HUMAN; HUMAN CELL; NONHUMAN; PLASMID; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; YERSINIA PSEUDOTUBERCULOSIS;

EID: 0029930059     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1996.5251051.x     Document Type: Article

References (48)

1. Bergman, T., Håkansson, S., Forsberg, Å., Norlander, L., Macellaro, A., Bäckman, A., Bölin, I., and Wolf-Watz, H. (1991) Analysis of the V-antigen lcrGVH-yopBD operon of Yersinia pseudotuberculosis: evidence for a regulatory role of LcrH and LcrV. J Bacteriol 173: 1607-1616.
2. Bergman, T., Erickson, K., Galyov, E., Persson, C., and Wolf-Watz, H. (1994) The lcrB(yscN/U) gene cluster of Yersinia pseudotuberculosis is involved in Yop secretion and shows high homology to the spa gene clusters of Shigella flexneri and Salmonella typhimurium. J Bacteriol 176: 2619-2626.
3. Bliska, J.B., Guan, K., Dixon, J.E., and Falkow, S. (1991) Tyrosine phosphatase hydrolysis of host proteins by an essential Yersinia virulence determinant. Proc Natl Acad Sci USA 88: 1187-1191.
4. Bliska, J.B., Copass, M.C., and Falkow, S. (1993) The Yersinia pseudotuberculosis adhesin YadA mediates intimate bacterial attachment to and entry into HEp-2 cells. Infect Immun 61: 3914-3921.
5. Bölin, I., and Wolf-Watz, H. (1984) Molecular cloning of the temperature-inducible outer-membrane protein 1 of Yersinia pseudotuberculosis. Infect Immun 34: 72-78.
6. Bölin, I., and Wolf-Watz, H. (1988) The plasmid-encoded Yop2b protein of Yersinia pseudotuberculosis is a virulence determinant regulated by calcium and temperature at the level of transcription. Mol Microbiol 2: 237-245.
7. Bölin, I., Norlander, L., and Wolf-Watz, H. (1982) Temperature-inducible outer membrane protein of Y. pseudotuberculosis and Y. enterocolitica is associated with the virulence plasmid. Infect Immun 37: 506-512.
8. Cornelis, G.R. (1992) Yersiniae, finely tuned pathogens. In Molecular Biology of Bacterial Infection: Current Status and Future Perspectives. Hormaeche, C.E., Penn, C.W., and Smyth, C.J. (eds). Cambridge: Cambridge University Press, pp. 231-265.
9. Cornelis, G., Sluiters, C., Lambert de Rouvroit, C., and Michiels, T. (1989) Homology between VirF, the transcriptional activator of the Yersinia virulence regulon, and AraC, the Escherichia coli arabinose operon regulator. J Bacteriol 171: 254-262.
10. 2+ response (LCR) secretion (ysc) locus lies within the lcrB region of the LCR plasmid in Yersinia pestis. J Bacteriol 176: 569-579.
11. Finlay, B.B., and Falkow, S. (1988) Comparison of the invasion strategies used by Salmonella cholerae-suis, Shigella flexneri and Yersinia enterocolitica to enter cultured animal cells: endosome acidification is not required for bacterial invasion or intracellular replication. Biochimie 70: 1089-1099.
12. Forsberg, Å., and Wolf-Watz, H. (1988) The virulence protein Yop5 of Yersinia pseudotuberculosis is regulated at transcriptional level by plasmid-plB1-encoded trans-acting elements controlled by temperature and calcium. Mol Microbiol 2: 121-133.
13. Forsberg, Å., and Wolf-Watz, H. (1990) Genetic analysis of the yopE region of Yersinia spp.: identification of a novel conserved locus, yerA, regulating yopE expression. J Bacteriol 172: 1547-1555.
14. Forsberg, Å., Viitanen, A.-M., Skurnik, M., and Wolf-Watz, H. (1991) The surface-located YopN protein is involved in calcium signal transduction in Yersinia pseudotuberculosis. Mol Microbiol 5: 977-986.
15. Forsberg, Å., Rosqvist, R., and Wolf-Watz, H. (1994) Regulation and polarized transfer of the Yersinia outer proteins (Yops) involved in antiphagocytosis. Trends Microbiol 2: 14-19.
16. Frithz-Lindsten, E., Rosqvist, R., Johansson, L., and Forsberg, Å. (1995) The chaperone-like protein YerA of Yersinia pseudotuberculosis stabilizes YopE in the cytoplasm but is dispensable for targeting to the secretion loci. Mol Microbiol 16: 635-647.
17. Galyov, E.E., Håkansson, S., Forsberg, Å., and Wolf-Watz, H. (1993) A secreted protein kinase of Yersinia pseudotuberculosis is an indispensable virulence determinant. Nature 361: 730-732.
18. Galyov, E.E., Håkansson, S., and Wolf-Watz, H. (1994) Characterization of the operon encoding the YpkA Ser/Thr protein kinase and the YopJ protein of Yersinia pseudotuberculosis. J Bacteriol 176: 4543-4548.
19. Guan, K., and Dixon, J.E. (1990) Protein tyrosine phosphatase activity of an essential virulence determinant in Yersinia. Science 249: 553-556.
20. Haddix, P.L., and Straley, S. (1992) The structure and regulation of the Yersinia pestis yscBCDEF operon. J Bacteriol 74: 4820-4828.
21. Håkansson, S. (1995) YopB-mediated translocation of Yops and the YpkA Ser/Thr kinase of Yersinia. Thesis, University of Umeå, Sweden.
22. Holmström, A., Rosqvist, R., Wolf-Watz, H., and Forsberg, Å. (1995) Virulence plasmid-encoded YopK is essential for Yersinia pseudotuberculosis to cause systemic infection in mice. Infect Immun 63: 2269-2276.
23. Kihlström, E., and Nilsson, L. (1977) Endocytosis of Salmonella typhimurium 395 MS and MR10 by HeLa cells. Acta Path Microbiol Scand Sect B 85: 322-328.
24. Lambert de Rouvroit, C., Sluters, C., and Cornelis, G.R. (1992) Role of the transcriptional activator, VirF, and temperature in the expression of the pYV plasmid genes of Yersinia enterocolitica. Mol Microbiol 6: 395-409.
25. Leung, K.Y., Reisner, B.S., and Straley, S.C. (1990) YopM inhibits platelet aggregation and is necessary for virulence of Yersinia pestis in mice. Infect Immun 58: 3262-3271.
26. Michiels, T., and Cornelis, G.R. (1991) Secretion of hybrid proteins by the Yersinia Yop export system. J Bacteriol 173: 1677-1685.
27. Michiels, T., Vanooteghem, J.-C., Lambert de Rouvroit, C., China, B., Gustin, A., Boudry, P., and Cornelis, G.R. (1991) Analysis of virC, an operon involved in the secretion of Yop proteins by Yersinia enterocolitica. J Bacteriol 173: 4949-5009.
28. Mulder, B.T., Michiels, T., Simonet, M., Sory, M.-P., and Cornelis, G. (1989) Identification of additional virulence determinants on the pYV plasmid of Yersinia enterocolitica W227. Infect Immun 57: 2534-2541.
29. Persson, C., Nordfelth, R., Holmström, A., Håkansson, S., Rosqvist R., and Wolf-Watz, H. (1995) Cell-surface-bound Yersinia translocate the protein tyrosine phosphatase YopH by a polarized mechanism into the target cell. Mol Microbiol 18: 135-150.
30. Plano, G.V., and Straley, S.C. (1993) Multiple effects of lcrD mutations in Yersinia pestis. J Bacteriol 175: 3536-3545.
31. Plano, G.V., Barve, S.S., and Straley, S.C. (1991) LcrD, a membrane-bound regulator of the Yersinia pestis low-calcium response. J Bacteriol 173: 7293-7303.
32. Reisner, B.S., and Straley S.C. (1992) Yersinia pestis YopM: thrombin binding and overexpression. Infect Immun 60: 5242-5252.
33. Rimpiläinen, M., Forsberg, Å., and Wolf-Watz, H. (1992) A novel protein, LcrQ, involved in the low-calcium response of Yersinia pseudotuberculosis shows extensive homology to YopH. J Bacteriol 174: 3355-3363.
34. Rosqvist, R., and Wolf-Watz, H. (1986) Virulence plasmid-associated HeLa cell induced cytotoxicity of Yersinia pseudotuberculosis. Microb Pathogen 1: 229-240.
35. Rosqvist, R., Bölin, I., and Wolf-Watz, H. (1988) Inhibition of phagocytosis in Yersinia pseudotuberculosis: a virulence plasmid-encoded ability involving the Yop2b protein. Infect Immun 56: 2139-2143.
36. Rosqvist, R., Forsberg, Å., Rimpiläinen, M., Bergman, T., and Wolf-Watz, H. (1990) The cytotoxic protein YopE of Yersinia obstructs the primary host defence. Mol Microbiol 4: 657-667.
37. Rosqvist, R., Forsberg, Å., and Wolf-Watz, H. (1991) Intracellular targeting of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption. Infect Immun 59: 4562-4569.
38. Rosqvist, R., Magnusson, K.-E., and Wolf-Watz, H. (1994) Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J 13: 964-972.
39. Rosqvist, R., Håkansson, S., Forsberg, Å., and Wolf-Watz, H. (1995) Functional conservation of the secretion and translocation machinery for virulence proteins of Yersiniae, Salmonellae and Shigellae. EMBO J 14: 4187-4195.
40. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press,.
41. Simon, R., Priefer, U., and Pühler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Biol Technology 1: 784-791.
42. Sory, M.-P., and Cornelis, G.R. (1994) Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol Microbiol 14: 583-594.
43. 2+ in Yersinia pestis include structural genes for outer membrane proteins. Infect Immun 51: 445-454.
44. - Yersinia pestis in BALB/c mice. Infect Immun 57: 1200-1210.
45. 2+ response. Mol Microbiol 8: 1005-1010.
46. Straley, S.C., Skrzypek, E., Plano, G.V., and Bliska, J.B. (1993b) Yops of Yersinia spp. pathogenic for humans. Infect Immun 61: 3105-3110.
47. Vaudaux, P., and Waldvogel, F.A. (1979) Gentamicin antibacterial activity in presence of human polymorphonuclear leukocytes. Antimicrob Agents Chemother 16: 743-749.
48. Wattiau, P., and Cornelis G.R. (1993) SycE, a chaperone-like protein of Yersinia enterocolitica involved in the secretion of YopE. Mol Microbiol 8: 123-131.