YopD of Yersinia pseudotuberculosis is translocated into the cytosol of HeLa epithelial cells: Evidence of a structural domain necessary for translocation

Molecular Microbiology

Volumn 29, Issue 3, 1998, Pages 799-813

  Francis, Matthew S ^a   Wolf Watz, Hans ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; DELETION MUTANT; GENE EXPRESSION REGULATION; GENE TRANSLOCATION; HELA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; YERSINIA PSEUDOTUBERCULOSIS;

BACTERIAL OUTER MEMBRANE PROTEINS; BINDING SITES; BIOLOGICAL TRANSPORT; CYTOSOL; EPITHELIAL CELLS; HELA CELLS; HUMANS; MODELS, BIOLOGICAL; MUTAGENESIS; STRUCTURE-ACTIVITY RELATIONSHIP; YERSINIA PSEUDOTUBERCULOSIS;

NEGIBACTERIA; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS;

EID: 0031928329     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1998.00973.x     Document Type: Article

References (76)

1. Allaoui, A., Schulte, R., and Cornelis, G.R. (1995) Mutational analysis of the Yersinia enterocolitica virC operon: characterisation of yscE, F, G, I, J, K required for Yop secretion and yscH encoding YopR. Mol Microbiol 18: 343-355.
2. Anderson, D.M., and Schneewind, O. (1997) A mRNA signal for the type III secretion of Yop proteins by Yersinia enterocolitica. Science 278: 1140-1143.
3. Bergman, T., Håkansson, S., Forsberg, Å., Norlander, L., Macellaro, A., Bäckman, A., Bölin, I., and Wolf-Watz, H. (1991) Analysis of the V-antigen IcrGVH-yopBD operon of Yersinia pseudotuberculosis: evidence for a regulatory role of LcrH and LcrV. J Bacteriol 173: 1607-1616.
4. Bergman, T., Erickson, K., Galyov, E., Persson, C., and Wolf-Watz, H. (1994) The IcrB (yscN/U) gene cluster of Yersinia pseudotuberculosis is involved in Yop secretion and shows high homology with the spa gene cluster of Shigella flexneri and Salmonella typhimurium. J Bacteriol 176: 2619-2626.
5. Cas as a substrate of Yersinia YopH (Yop51), a bacterial protein tyrosine phosphatase that translocates into mammalian cells and targets focal adhesions. EMBO J 16: 2730-2744.
6. Boland, A., Sory, M-P., Iriarte, M., Kerbourch, C., Wattiau, P., and Cornelis, G.R. (1996) Status of YopM and YopN in the Yersinia Yop virulon: YopM of Y. enterocolitica is internalised inside the cytosol of PU5-1.8 macrophages by the YopB, D, N, delivery apparatus. EMBO J 15: 5191-5201.
7. Bölin, I., and Wolf-Watz, H. (1984) Molecular cloning of the temperature-inducible outer membrane protein 1 of Yersinia pseudotuberculosis. Infect Immun 43: 72-78.
8. Bottone, E.J. (1977) Yersinia enterocolitica: a panoramic view of a charismatic microorganism. Crit Rev Microbiol 5: 211-241.
9. Boyd, A.P., Sory, M-P., Iriarte, M., and Cornelis, G.R. (1998) Heparin interferes with translocation of Yop proteins into HeLa cells and binds LcrG, a regulatory component of the Yersinia Yop apparatus. Mol Microbiol 27: 425-436.
10. Brubaker, R.R. (1972) The genus yersiniae. Biochemistry and genetics of virulence. Curr Top Microbiol Immunol 57: 111-158.
11. Collazo, C., and Galán, J.E. (1997) The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host. Mol Microbiol 24: 747-756.
12. Cornelis, G.R. (1992) Yersinia, finely tuned pathogens. In Molecular Biology of Bacterial Infections. Hormache, C.E., Penn, C.W., and Smythe, C.J. (eds). Cambridge: Cambridge University Press, pp. 231-265.
13. Cornelis, G.R., and Wolf-Watz, H. (1997) The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol Microbiol 23: 861-867.
14. Cover, T.L., and Aber, R.C. (1989) Yersinia enterocolitica. N Engl J Med 321: 16-24.
15. Fällman, M., Andersson, K., Håkansson, S., Magnusson, K-E., Stendahl, O., and Wolf-Watz, H. (1995) Yersinia pseudotuberculosis inhibits Fc receptor-mediated phagocytosis in J774 cells. Infect Immun 63: 3117-3124.
16. Fällman, M., Persson, C., and Wolf-Watz, H. (1997) Yersinia proteins that target host cell signaling pathways. J Clin Invest 99: 1153-1157.
17. 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. Biochemie 70: 1089-1099.
18. Forsberg, Å., and Wolf-Watz, H. (1988) The virulence of 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.
19. 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.
20. Forsberg, Å., Vitanen, A-M., Skurnik, M., Wolf-Watz, H. (1991) The surface-located YopN protein is involved in calcium signal transduction in Yersinia pseudotuberculosis. Mol Microbiol 5: 977-986.
21. Forsberg, Å., Rosqvist, R., and Wolf-Watz, H. (1994) Regulation and polarised transfer of the Yersinia outer proteins (Yops) involved in antiphagocytosis. Trends Microbiol 2: 14-19.
22. Fu, Y., and Galán, J.E. (1998) The Salmonella typhimurium tyrosine phosphatase SptP is translocated into host cells and disrupts the actin cytoskeleton. Mol Microbiol 27: 359-368.
23. Håkansson, S., Bergman, T., Vanootteghem, V-C., Cornelis, G.R., and Wolf-Watz, H. (1993) YopB and YopD, a novel class of Yop proteins of Yersinia. Infect Immun 61: 71-80.
24. Håkansson, S., Galyov, E.E., Rosqvist, R., and Wolf-Watz, H. (1996a) 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.
25. Håkansson, S., Schesser, K., Persson, C., Galyov, E.E., Rosqvist, R., Homblé, F., and Wolf-Watz, H. (1996b) The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane and displays a contact-dependent membrane disrupting activity. EMBO J 15: 5812-5823.
26. Hanski, C., Kutschka, U., and Schmoranzer, H.P. (1989) Immunohistochemical and electron microscopic study of interaction of Yersinia enterocolitica serotype 0:8 with intestinal mucosa during experimental enteritis. Infect Immun 57: 673-678.
27. Hardt, W-D., and Galán, J.E. (1997) A secreted Salmonella protein with homology to an avirulence determinant of plant pathogenic bacteria. Proc Natl Acad Sci USA 94: 9887-9892.
28. Hartland, E.L., Green, S.P., Phillips, W.A., and Robins-Browne, R.M. (1994) Essential role of YopD in inhibition of respiratory burst of macrophages by Yersinia enterocolitica. Infect Immun 62: 4445-4453.
29. Hartland, E.L., Bordun, A-M., and Robins-Browne, R.M. (1996) Contribution of YopB to virulence of Yersinia enterocolitica. Infect Immun 64: 2308-2314.
30. Heesemann, J., Algermissen, B., and Laufs, R. (1984) Genetically manipulated virulence of Yersinia enterocolitica. Infect Immun 46: 105-110.
31. Holmström, A., Pettersson, J., Rosqvist, P., Håkansson, S., Tafazoli, F., Fällman, M., et al. (1997) YopK of Yersinia pseudotuberculosis controls translocation of Yop effectors across the eukaryotic cell membrane. Mol Microbiol 24: 73-91.
32. Horton, R.M., and Pease, L.R. (1991) Recombination and mutagenesis of DNA sequences using PCR, In Directed Mutagenesis: a Practical Approach. McPherson M.J. (ed). New York: Oxford University Press, pp. 217-247.
33. Isberg, R.R., and Falkow, S. (1985) A single genetic locus encoded by Yersinia pseudotuberculosis permits invasion of cultured animal cells by Escherichia coli K-12. Nature 317: 262-264.
34. Isberg, R.R., Voorhis, D.L., and Falkow, S. (1987) Analysis of expression and thermoregulation of the Yersinia pseudotuberculosis inv gene with hybrid proteins. Infect Immun 56: 2133-2138.
35. Kaniga, K.S., Trollinger, D., and Galán, J.E. (1995a) 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.
36. Kaniga, K.S., Tucker, S., Trollinger, D., and Galán, J.E. (1995b) Homologs of the Shigella IpaB and IpaC invasins are required for Salmonella typhimurium entry into cultured epithelial cells. J Bacteriol 177: 3965-3971.
37. 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.
38. Landschulz, W.H., Johnson, P.F., and McKnight, S.L. (1988) The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science 240: 1759-1764.
39. Lee, C.A. (1997) Type III secretion systems: machines to deliver bacterial proteins into eukaryotic cells? Trends Microbiol 5: 148-156.
40. Lupas, A. (1996) Coiled coils: new structures and new functions. Trends Biochem Sci 21: 375-382.
41. Michels, T., Vanooteghem, J-C., and Cornelis, G.R. (1992) Analysis of virC, an operon involved in the secretion of Yop proteins by Yersinia enterocolitica. J Bacteriol 173: 4994-5009.
42. Miller, V.L., and Mekalanos, J.J. (1988) A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 170: 2575-2583.
43. Mills, S.D., Boland, A., Sory, M-P., Van Der Smissen, P., Kerbourch, C., Finlay, B.B., and Cornelis, G.R. (1997) Versinia enterocolitica induces apoptosis in macrophages by a process requiring functional type III secretion and translocation mechanisms and involving YopP, presumably acting as an effector protein. Proc Natl Acad Sci USA 94: 12638-12643.
44. Milton, D.L., O'Toole, R., Hörstedt, P., and Wolf-Watz, H. (1996) Flagellin A is essential for the virulence of Vibrio anguillarum. J Bacteriol 178: 1310-1319.
45. Monack, D.M., Mecsas, J., Ghori, N., and Falkow, S. (1997) Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death. Proc Natl Acad Sci USA 94: 10385-10390.
46. Motin, V.L., Nakajima, R., Smirnov, G.B., and Brubaker, R.R. (1994) Passive immunity to Yersiniae mediated by anti-recombinant V-antigen and Protein A-V antigen fusion peptide. Infect Immun 62: 4192-4201.
47. Nakajima, R., and Brubaker, R.R. (1993) Association between virulence of Yersinia pestis and suppression of gamma interferon and tumor necrosis factor alpha. Infect Immun 61: 23-31.
48. Nakajima, R., Motin, V.L., and Brubaker, R.R. (1995) Suppression of cytokines in mice by protein A-V antigen fusion peptide and restoration of synthesis by active immunisation. Infect Immun 63: 3021-3029.
49. Pallen, M.J., Dougan, G., and Frankel, G. (1997) Coiled-coil domains in proteins secreted by type III secretion systems. Mol Microbiol 25: 423-425.
50. 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 polarised mechanism into the target cell. Mol Microbiol 18: 135-150.
51. Cas and FAK, and the associated accumulation of these proteins in peripheral focal adhesions. EMBO J 16: 2307-2318.
52. Portnoy, D., Blank, H.F., Kingsbury, D.T., and Falkow, S. (1983) Genetic analysis of essential plasmid determinants of pathogenicity in Yersinia pestis. J Infect Dis 148: 297-304.
53. Portnoy, D.A., Wolf-Watz, H., Bölin, I., Beeder, A.B., and Falkow, S. (1984) Characterisation of a common virulence plasmid in Yersinia species and their role in the expression of outer membrane proteins. Infect Immun 43: 108-114.
54. 2+ response genes. J Bacteriol 173: 2649-2657.
55. Rosqvist, R., and Wolf-Watz, H. (1986) Virulence plasmid-associated HeLa cell induced cytotoxicity of Yersinia pseudotuberculosis. Microb Pathog 1: 229-240.
56. Rosqvist, R., Bölin, I., and Wolf-Watz, H. (1988) Inhibition of phagocytosis is a virulence plasmid ability involving the Yop2b protein of Yersinia pseudotuberculosis. Infect Immun 56: 2139-2143.
57. 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.
58. 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.
59. Rosqvist, R., Magnusson, K-E., and Wolf-Watz, H. (1994) Target cell contact triggers expression and polarised transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J 13: 964-972.
60. Ruckdeschel, K., Roggenkamp, A., Schubert, S., and Heesemann, J. (1996) Differential contribution of Yersinia enterocolitica virulence factors to evasion of microbicidal action of neutriphils. Infect Immun 64: 724-733.
61. Ruckdeschel, K., Roggenkamp, A., Lafont, V., Mangeat, P., Heesemann, J., and Rouot, B. (1997) Interaction of Yersinia enterocolitica with macrophages leads to macrophage cell death through apoptosis. Infect Immun 65: 4813-4821.
62. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
63. Schesser, K., Frithz-Lindsten, E., and Wolf-Watz, H. (1996) Delineation and mutational analysis of the Yersinia pseudotuberculosis YopE domains which mediate translocation across bacterial and eukaryotic cellular membranes. J Bacteriol 178: 7227-7233.
64. Silhavy, T.J. (1997) Death by lethal injection. Science 278: 1085-1086.
65. Simon, R., Priefer, U., and Pühler, A. (1983) A broad host range mobilisation system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Biotechnology 1: 787-796.
66. Simonet, M., Richard, S., and Berche, P. (1990) Electron microscopic evidence for in vivo extracellular localization of Yersinia pseudotuberculosis harbouring the pYV plasmid. Infect Immun 58: 841-845.
67. 2+ response, and virulence of Yersinia pestis. J Bacteriol 177: 2530-2542.
68. 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.
69. Sory, M-P., Boland, A., Lambermont, I., and Cornelis, G.R. (1995) Identification of the YopE and YopH domains required for secretion and internalisation into the cytosol of macrophages, using the cyaA gene fusion approach. Proc Natl Acad Sci USA 92: 11998-12002.
70. 2+ response. Mol Microbiol 8: 1005-1010.
71. Une, T. (1977) Studies on the pathogenicity of Yersinia enterocolitica. III. Comparative studies between Y. enetrocolitica and Y. pseudotuberculosis. Microbiol Immunol 21: 505-506.
72. Une, T., and Brubaker, R.R. (1984) Role of V antigen in promoting virulence and immunity in Yersiniae. J Immunol 133: 2226-2230.
73. Vaudaux, P., and Waldvogel, F.A. (1979) Gentamicin antibacterial activity in presence of human polymorphonuclear leukocytes. Antimicrob Agents Chemother 16: 743-749.
74. Williams, A.W., and Straley, S.C. (1998) YopD of Yersinia pestis plays a role in negative regulation of the low-calcium response in addition to its role in translocation of Yops. J Bacteriol 180: 350-358.
75. Wolf-Watz, H., Portnoy, D.A., Bölin, I., and Falkow, S. (1985) Transfer of the virulence plasmid of Yersinia pestis to Yersinia pseudotuberculosis. Infect Immun 48: 241-243.
76. Wood, M.W., Rosqvist, R., Mullan, P.B., Edwards, M.H., and Galyov, E.E. (1996) SopE, a secreted protein of Salmonella dublin, is translocated into the target eukaryotic cell via a sip-dependent mechanism and promotes bacterial entry. Mol Microbiol 22: 327-338.