Inhibition of Cdc42-dependent signalling in Saccharomyces cerevisiae by phosphatase-dead SigD/SopB from Salmonella typhimurium

Microbiology

Volumn 152, Issue 11, 2006, Pages 3437-3452

  Rodríguez Escudero, Isabel ^a   Rotger, Rafael ^a   Cid, Victor J ^a   Molina, María ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; COMPLEMENTARY DNA; GUANOSINE TRIPHOSPHATASE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATASE; PROTEIN CDC42; PROTEIN KSS1; PROTEIN SIGD; PROTEIN SLT2; PROTEIN SOPB; PROTEIN SWE1; SEPTIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL INFECTION; CELL BUDDING; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL LYSATE; CONTROLLED STUDY; DNA LIBRARY; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE OVEREXPRESSION; GROWTH INHIBITION; MORPHOGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; SACCHAROMYCES CEREVISIAE; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CDC42 GTP-BINDING PROTEIN, SACCHAROMYCES CEREVISIAE; CELL CYCLE; CELL POLARITY; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHORIC MONOESTER HYDROLASES; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); SACCHAROMYCES CEREVISIAE; SALMONELLA; SALMONELLA TYPHIMURIUM;

EID: 33750945808     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.29186-0     Document Type: Article

References (65)

1. Aili, M., Telepnev, M., Hallberg, B., Wolf-Watz, H. & Rosqvist R. (2003). In vitro GAP activity towards RhoA, Rac1 and Cdc42 is not a prerequisite for YopE induced HeLa cell cytotoxicity. Microb Pathog 34, 297-308.
2. Alemán, A., Rodriguez-Escudero, I., Mallo, G. V., Cid, V. J., Molina, M. & Rotger, R. (2005). The amino-terminal non-catalytic region of Salmonella typhimurium SigD affects actin organization in yeast and mammalian cells. Cell Microbiol 7, 1432-1446.
3. Audhya, A., Loewith, R., Parsons, A. B., Gao, L., Tabuchi, M., Zhou, H., Boone, C., Hall, M. N. & Emr, S. D. (2004). Genome-wide lethality screen identifies new P14,5P(2) effectors that regulate the actin cytoskeleton. EMBO J 23, 3747-3757.
4. Barral, Y., Parra, M., Bidlingmaier, S. & Snyder, M. (1999). Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast. Genes Dev 13, 176-187.
5. Bertelsen, L. S., Paesold, G., Marcus, S. L., Finlay, B. B., Eckmann, L. & Barrett, K. E. (2004). Modulation of chloride secretory responses and barrier function of intestinal epithelial cells by the Salmonella effector protein SigD. Am J Cell Physiol 287, 939-948.
6. Blomberg, N., Baraldi, E., Nilges, M. & Saraste, M. (1999). The PH superfold: a structural scaffold for multiple functions. Trends Biochem Sci 24, 441-445.
7. Cabezas, A., Patin, K. & Stenmark, H. (2006). Cloning and subcellular localization of a human phosphatidylinositol 3-phosphate 5-kinase, PIKfyve/Fab1. Gene 371, 34-41.
8. Chen, L. M., Hobbie, S. & Galán, J. E. (1996). Requirement of Cdc42 for Salmonella typhimurium-induced cytoskeletal reorganization and nuclear responses in cultured cells. Science 274, 2115-2118
9. Cid, V. J., Adamiková, L., Sánchez, M., Molina, M. & Nombela, C. (2001a). Cell cycle control of septin ring dynamics in the budding yeast. Microbiology 147, 1437-1450.
10. Cid, V. J., Shulewitz, M. J., McDonald, K. L. & Thorner, J. (2001b). Dynamic localization of the Swe1 regulator Hsl7 during the Saccharomyces cerevisiae cell cycle. Mol Biol Cell 12, 1645-1669.
11. Cook J. G., Bardwell, L. & Thorner, J. (1997). Inhibitory and activating functions for MAPK Kss1 in the S. cerevisiae filamentous-growth signalling pathway. Nature 390, 85-88.
12. De Nobel, H., Ruiz, C., Martin, H., Morris, W., Brut, S., Molina, M. & Klis, F. M. (2000). Cell wall perturbation in yeast results in dual phosphorylation of the Slt2/Mpk1 MAP kinase and in an Slt2-mediated increase in FKS2-lacZ expression, glucanase resistance and thermotolerance. Microbiology 146, 2121-2132.
13. Dukes, J. D., Lee, H., Hagen, R., Reaves, B. J., Layton, A. N., Galyov, E. E. & Whitley, P. (2006). The secreted Salmonella dublin phosphoinositide phosphatase, SopB, localizes to PtdIns(3)P-containing endosomes and perturbs normal endosome to lysosome trafficking. Biochem J 395, 239-247.
14. Feng, Y., Wente, S. R. & Majerus, P. W. (2001). Overexpression of the inositol phosphatase SopB in human 293 cells stimulates cellular chloride influx and inhibits nuclear mRNA export. Proc Natl Acad Sci U S A 98, 875-879.
15. Fu, Y. & Galan, J. E. (1999). A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401, 293-297.
16. Gary, J. D., Wurmser, A. E., Bonangelino, C. J., Weisman, L. S. & Emr, S. D. (1998). Fab1p is essential for PtdIns(3)P 5-kinase activity and the maintenance of vacuolar size and membrane homeostasis. J Cell Biol 143, 65-79.
17. Gladfelter, A. S., Pringle, J. R. & Lew, D. J. (2001). The septin cortex at the yeast mother-bud neck. Curr Opin Microbiol 4, 681-689.
18. Gladfelter, A. S., Bose, L., Zyla, T. R., Bardes, E. S. & Lew, D. J. (2002). Septin ring assembly involves cycles of GTP loading and hydrolysis by Cdc42p. J Cell Biol 156, 315-326.
19. Guan, K. L. & Dixon, J. E. (1991). Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal Biochem 192, 262-267.
20. Harder, K. W., Owen, P., Wong, L. K., Aebersold, R., Clark-Lewis, I. & Jirik, F. R. (1994). Characterization and kinetic analysis of the intracellular domain of human protein tyrosine phosphatase beta (HPTP beta) using synthetic phosphopeptides. Biochem J 298, 395-401.
21. Hardt W. D., Chen, L. M., Schuebel, K. E., Bustelo, X. R. & Galán, J. E. (1998). S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 29, 815-826.
22. Harrison, J. C., Bardes, E. S., Ohya, Y. & Lew, D. J. (2001). A role for the Pkc1p/Mpk1p kinase cascade in the morphogenesis checkpoint. Nat Cell Biol 3, 417-420.
23. Hernández, L. D., Hueffer, K., Wenk, M. R. & Galin, J. E. (2004). Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science 304, 1805-1807.
24. Hong, K. M. & Miller, V. L. (1998). Identification of a novel Salmonella invasion locus homologous to Shigella ipgDE. J Bacteriol 180, 1793-1802.
25. Johnson, D. I. & Pringle, J. R. (1990). Molecular characterization of CDC42, a Saccharomyces cerevisiae gene involved in the development of cell polarity. J Cell Biol 111, 143-152.
26. Knodler, L. A., Finlay, B. B. & Steele-Mortimer, O. (2005). The Salmonella effector protein SopB protects epithelial cells from apoptosis by sustained activation of Akt. J Biol Chem 280, 9058-9064.
27. Lee, B. N. & Ellon, E. A. (1999). The MAPKKK Ste11 regulates vegetative growth through a kinase cascade of shared signalling components. Proc Natl Acad Sci U S A 96, 12679-12684.
28. Lee, K. S., Hines, L. K. & Levin, D. E. (1993). A pair of functionally redundant yeast genes (PPZ1 and PPZ2) encoding type 1-related protein phosphatases function within the PKC1-mediated pathway. Mol Cell Biol 13, 5843-5853.
29. Lesser, C. F. & Miller, S. I. (2001). Expression of microbial virulence proteins in Saccharomyces cerevisiae models mammalian infection. EMBO J 20, 1840-1849.
30. Liu, H., Krizek, J. & Bretscher, A. (1992). Construction of a GAL1-regulated yeast cDNA expression library and its application to the identification of genes whose overexpression causes lethality in yeast. Genetics 132, 665-673.
31. Marcus, S. L., Wank M. R., Steele-Mortimer, O. & Finlay, B. B. (2001). A synaptojanin-homologous region of Salmonella typhimurium SigD is essential for inositol phosphatase activity and Akt activation. FEBS Lett 13, 201-207.
32. Marcus, S. L., Knodler, L. A. & Finlay, B. B. (2002). Salmonella enterica serovar Typhimurium effector SigD/SopB is membrane-associated and ubiquitinated inside host cells. Cell Microbiol 4, 435-446.
33. Martín, H., Arroyo, J., Sánchez, M., Molina, M. & Nombela, C. (1993). Activity of the yeast MAP kinase homologue Slt2 is critically required for cell integrity at 37°C. Mol Gen Genet 241, 177-184.
34. Martín, H., Rodríguez-Pachón, J. M., Ruiz, C., Nombela, C. & Molina, M. (2000). Regulatory mechanisms for modulation of signalling through the cell integrity Slt2-mediated pathway in Saccharomyces cerevisiae. J Biol Chem 275, 1511-1519.
35. McMillan, J. N., Longtine, M. S., Sia, R. A., Theesfeld, C. L., Bardes, E. S., Pringle, J. R. & Lew, D. J. (1999). The morphogenesis checkpoint in Saccharomyces cerevisiae: cell cycle control of Swe1p degradation by Hsl1p and Hsl7p. Mol Cell Biol 19, 6929-6939.
36. Mitchell, D. A., Marshall, T. K. & Deschenes, R. J. (1993). Vectors for the inducible overexpression of glutathione S-transferase fusion proteins in yeast. Yeast 9, 715-722.
37. Mösch, H. U., Roberts, R. L. & Fink G. R. (1996). Ras2 signals via the Cdc42/Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 93, 5352-5356.
38. Murli, S., Watson, R. O. & Galin, J. E. (2001). Role of tyrosine kinases and the tyrosine phosphatase SptP in the interaction of Salmonella with host cells. Cell Microbiol 3, 795-810.
39. Niebuhr, K., Jouihri, N., Allaoui, A., Gounon, P., Sansonetti, P. J. & Parsot, C. (2000). IpgD, a protein secreted by the type III secretion machinery of Shigella flexneri, is chaperoned by IpgE and implicated in entry focus formation. Mol Microbiol 38, 8-19.
40. Norris, F. A., Wilson, M. P., Wallis, T. S., Galyov, E. E. & Majerus, P. W. (1998). SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc Natl Acad Sci U S A 95, 14057-14059.
41. Pardon, P., Popoff, M. Y., Coynault, C., Marly, J. & Miras, I. (1986). Virulence-associated plasmids of Salmonella serotype Typhimurium in experimental murine infection. Ann Inst Pasteur Microbiol 173B, 47-60.
42. Patel, J. C. & Galán, J. E. (2005). Manipulation of the host actin cytoskeleton by Salmonella - all in the name of entry. Curr Opin Microbiol 8, 10-15.
43. Pruyne, D. & Bretscher, A. (2000). Polarization of cell growth in yeast. J Cell Sci 113, 571-585.
44. Rabin, S. D. & Hauser, A. R. (2003). Pseudomonas aeruginosa ExoU, a toxin transported by the type III secretion system, kills Saccharomyces cerevisiae. Infect Immun 71, 4144-4150.
45. Rodríguez-Escudero, I., Hardwidge, P. R., Nombela, C., Cid, V. J., Finlay, B. B. & Molina, M. (2005a). Enteropathogenic Escherichia coli type III effectors alter cytoskeletal function and signalling in Saccharomyces cerevisiae. Microbiology 151, 2933-2945.
46. Roiríguez-Escudero, I., Roelants, F. M., Thorner, J., Nombela, C., Molina, M. & Cid, V. J. (2005b). Reconstitution of the mammalian PI3K/ PTEN/Akt pathway in yeast. Biochem J 390, 613-623.
47. Rodríguez-Pachón, J. M., Martín, H., North, G., Rotger, R., Nombela, C. & Molina, M. (2002). A novel connection between the yeast Cdc42 GTPase and the Slt2-mediated cell integrity pathway identified through the effect of secreted Salmonella GTPase modulators. J Biol Chem 26, 27094-27102.
48. Ruiz, C., Escribano, V., Morgado, E., Molina, M. & Mazon, M. J. (2003). Cell-type-dependent repression of yeast a-specific genes requires Itc1p, a subunit of the Isw2p-Itc1p chromatin remodelling complex. Microbiology 149, 341-351.
49. Sato, H., Frank, D. W., Hillard, C. J. & 9 other authors (2003). The mechanism of action of the Pseudomonas aeruginosa-encoded type III cytotoxin, ExoU. EMBO J 22, 2959-2969.
50. Shinjo, K., Koland, J. G., Hart, M. J., Narasimhan, V., Johnson, D. I., Evans, T. & Cerione, R. A. (1990). Molecular cloning of the gene for the human placental GTP-binding protein Gp(G25K): identification of this GTP-binding protein as the human homolog of the yeast cell-division-cycle protein CDC42. Proc Natl Acad Sci U S A 87, 9853-9857.
51. Shulewitz, M. J., Inouye, C. J. & Thorner, J. W. (1999). Hsl7 localizes to a septin ring and serves as an adapter in a regulatory pathway that relieves tyrosine phosphorylation of Cdc28 protein kinase in Saccharomyces cerevisiae. Mol Cell Biol 19, 7123-7137.
52. Sia, R. A., Herald, H. A. & Lew, D. J. (1996). Cdc28 tyrosine phosphorylation and the morphogenesis checkpoint in budding yeast. Mol Biol Cell 7, 1657-1666.
53. Sia, R. A., Bardes, E. S. & Lew, D. J. (1998). Control of Swe1p degradation by the morphogenesis checkpoint. EMBO J 17, 6678-6688.
54. Skrzypek E., Myers-Morales, T., Whiteheart, S. W. & Straley, S. C. (2003). Application of a Saccharomyces cerevisiae model to study requirements for trafficking of Yersinia pestis YopM in eukaryotic cells. Infect Immun 71, 937-947.
55. Smith, G. R., Givan, S. A., Cullen, P. & Sprague, G. F., Jr (2002). GTPase-activating proteins for Cdc42. Eukaryot Cell 1, 469-480.
56. Steele-Mortimer, O., Knodler, L. A., Marcus, S. L., Scheid, M. P., Goh, B., Pfeifer, C. G., Duronio, V. & Finlay, B. B. (2000). Activation of Akt/protein kinase B in epithelial cells by the Salmonella typhimurium effector SigD. J Biol Chem 275, 37718-37724.
57. Terebiznik M. R., Vieira, O. V., Marcus, S. L., Slade, A., Yip, C. M., Trimble, W. S., Meyer, T., Finlay, B. B. & Grinstein, S. (2002). Elimination of host cell PtdIns(4,5)P(2) by bacterial SigD promotes membrane fission during invasion by Salmonella. Nat Cell Biol 4, 766-773.
58. Trosky, J. E., Mukherjee, S., Burdette, D. L., Roberts, M., McCarter, L., Siegel R. M. & Orth, K. (2004). Inhibition of MAPK signalling pathways by VopA from Vibrio parahaemolyticus. J Biol Chem 279, 51953-51957.
59. Valdivia, R. H. (2004). Modeling the function of bacterial virulence factors in Saccharomyces cerevisiae. Eukaryot Cell 3, 827-834.
60. Von Pawel-Rammingen, U., Telepnev, M. V., Schmidt, G., Aktories, K., Wolf-Watz, H. & Rosqvist, R. (2000). GAP activity of the Yersinia YopE cytotoxin specifically targets the Rho pathway: a mechanism for disruption of actin microfilament structure. Mol Microbiol 36, 737-748.
61. Yoon, S., Liu, Z., Eyobo, Y. & Orth, K. (2003). Yersinia effector YopJ inhibits yeast MAPK signalling pathways by an evolutionarily conserved mechanism. J Biol Chem 278, 2131-2135.
62. Yu, J. W., Mendrola, J. M., Audhya, A., Singh, S., Keleti, D., DeWald, D. B., Murray, D., Emr, S. D. & Lemmon, M. A. (2004). Genome-wide analysis of membrane targeting by S. cerevisiae pleckstrin homology domains. Mol Cell 13, 677-688.
63. Zaharik, M. L., Gruenheid, S., Perrin, A. J. & Finlay, B. B. (2002). Delivery of dangerous goods: Type III secretion in enteric pathogens. Int J Med Microbiol 291, 593-603.
64. Zhou, Z., Gartner, A., Cade, R., Ammerer, G. & Errede, B. (1993). Pheromone-induced signal transduction in Saccharomyces cerevisiae requires the sequential function of three protein kinases. Mol Cell Biol 13, 2069-2080.
65. Zhou, D., Chen, L. M., Hernández, L., Shears, S. B. & Galán, J. E. (2001). A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol Microbiol 39, 248-259.