The amino-terminal non-catalytic region of Salmonella typhimurium SigD affects actin organization in yeast and mammalian cells

Cellular Microbiology

Volumn 7, Issue 10, 2005, Pages 1432-1446

  Alemán, Ainel ^a   Rodríguez Escudero, Isabel ^a   Mallo, Gustavo V ^b   Cid, Victor J ^a   Molina, María ^a   Rotger, Rafael ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; AMINO ACID; BACTERIAL PROTEIN; PHOSPHATASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN SIGD; UNCLASSIFIED DRUG;

ALLELE; AMINO TERMINAL SEQUENCE; ARTICLE; BIOLOGICAL MODEL; BUDDING; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CELL ADHESION; CELL MEMBRANE; CONTROLLED STUDY; DATA ANALYSIS; ENZYME ACTIVITY; FUNGUS GROWTH; GENE DELETION; GENE MUTATION; GROWTH INHIBITION; HELA CELL; HUMAN; HUMAN CELL; MAMMAL CELL; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SACCHAROMYCES CEREVISIAE; SALMONELLA TYPHIMURIUM; YEAST CELL;

ACTINS; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CELL ADHESION; CELLS; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HUMANS; MICROSCOPY, FLUORESCENCE; MUTATION; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SALMONELLA TYPHIMURIUM; SEQUENCE DELETION;

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

EID: 25144480412     PISSN: 14625814     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2005.00568.x     Document Type: Article

References (47)

1. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (1993) Current Protocols in Molecular Biology. New York: Greene Publishing Associates and Wiley Interscience.
2. Brumell, J.H., Steele-Mortimer, O., and Finlay, B.B. (1999) Bacterial invasion: Force feeding by Salmonella. Curr Biol 9: 277-280.
3. Doyle, T., and Botstein, D. (1996) Movement of yeast cortical actin cytoskeleton visualized in vivo. Proc Natl Acad Sci USA 93: 3886-3891.
4. Drecktrah, D., Knodler, L.A., and Steele-Mortimer, O. (2004) Modulation and utilization of host cell phosphoinositides by Salmonella spp. Infect Immun 72: 4331-4335.
5. Feng, Y., Wente, S.R., and 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 USA 98: 875-879.
6. Galán, J.E., and Curtiss, R., III (1989) Virulence and vaccine potential of phoP mutants of Salmonella typhimurium. Microb Pathog 6: 433-443.
7. Galán, J.E., and Zhou, D. (2000) Striking a balance: modulation of the actin cytoskeleton by Salmonella. Proc Natl Acad Sci USA 97: 8754-8761.
8. Galyov, E.E., Wood, M.W., Rosqvist, R., Mullan, P.B., Watson, P.R., Hedges, S., and Wallis, T.S. (1997) A secreted effector protein of Salmonella dublin is translocated into eukaryotic cells and mediates inflammation and fluid secretion in infected ileal mucosa. Mol Microbiol 25: 903-912.
9. García del Portillo, F. (2001) Salmonella intracellular proliferation: where, when and how? Microbes Infect 3: 1305-1311.
10. Guan, K.L., and 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.
11. Harder, K.W., Owen, P., Wong, L.K., Aebersold, R., Clark-Lewis, I., and 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.
12. Hernandez, L.D., Hueffer, K., Wenk, M.R., and Galan, J.E. (2004) Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science 304: 1805-1807.
13. Higashide, W., Dai, S., Hombs, V.P., and Zhou, D. (2002) Involvement of SipA in modulating actin dynamics during Salmonella invasion into cultured epithelial cells. Cell Microbiol 4: 357-365.
14. Hong, K.M., and Miller, V.L. (1998) Identification of a novel Salmonella invasion locus homologous to Shigella lpgde. J Bacteriol 180: 1793-1802.
15. Ito, H., Fukada, Y., Murata, K., and Kimura, A. (1983) Transformation of intact yeast with alkali cations. J Bacteriol 153: 163-168.
16. Jiménez, J., Cid, V.J., Cenamor, R., Yuste, M., Molero, G., Nombela, C., and Sánchez, M. (1998) Morphogenesis beyond cytokinetic arrest in Saccharomyces cerevisiae. J Cell Biol 143: 1617-1634.
17. Kimbrough, T.G., and Miller, S.L. (2002) Assembly of the type III secretion needle complex of Salmonella typhimurium. Microbes Infect 4: 75-82.
18. Lesser, C.F., and Miller, S.I. (2001) Expression of microbial virulence proteins in Saccharomyces cerevisiae models mammalian infection. EMBO J 20: 1840-1849.
19. Lin, S.L., Le, T.X., and Cowen, D.S. (2003) SptP, a Salmonella typhimurium type III-secreted protein, inhibits the mitogen-activated protein kinase pathway by inhibiting Raf activation. Cell Microbiol 5: 267-275.
20. McGhie, E.J., Haywarg, R.D., and Koronakis, V. (2001) Cooperation between actin-binding proteins of invasive Salmonella: SipA potentiates SipC nucleation and bundling of actin. EMBO J 20: 2131-2139.
21. Marcus, S.L., Wenk, M.R., Steele-Mortimer, O., and 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.
22. Marcus, S.L., Knodler, L.A., and Finlay, B.B. (2002) Salmonella enterica serovar typhimurium effector SigD/SopB is membrane-associated and ubiquitinated inside host cells. Cell Microbiol 4: 435-446.
23. Mitchell, D.A., Marshall, T.K., and Deschenes, R.J. (1993) Vectors for the inducible overexpression of glutathione S-transferase fusion proteins in yeast. Yeast 9: 715-722.
24. Nejedlik, L., Pierfelice, T., and Geiser, J.R. (2004) Actin distribution is disrupted upon expression of Yersinia YopO/YpkA in yeast. Yeast 21: 759-768.
25. Niebuhr, K., Jouihri, N., Allaoui, A., Gounon, P., Sansonetti, P.J., and 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.
26. 2 into PtdIns 5-P by the S. flexneri effector IpgD reorganizes host cell morphology. EMBO J 21: 5069-5078.
27. Norris, F.A., Wilson, M.P., Wallis, T.S., Galyov, E.E., and Majerus, P.W. (1998) SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc Natl Acad Sci USA 95: 14057-14059.
28. Ohl, M.E., and Miller, S.L. (2001) Salmonella: a model for bacterial pathogenesis. Annu Rev Med 52: 259-274.
29. Pardon, P., Popoff, M.Y., Coynault, C., Marly, J., and Miras, I. (1986) Virulence-associated plasmids of Salmonella serotype Typhimurium in experimental murine infection. Ann Inst Pasteur Microbiol 173B: 47-60.
30. Patel, J.C., and Galan, J.E. (2005) Manipulation of the host actin cytoskeleton by Salmonella-All in the name of entry. Curr Opin Microbiol 8: 10-15.
31. Pizarro-Cerda, J., and Cossart, P. (2004) Subversion of phosphoinositide metabolism by intracellular bacterial pathogens. Nat Cell Biol 6: 1026-1033.
32. Pruyne, D., and Bretscher, A. (2000) Polarization of cell growth in yeast. J Cell Sci 113: 571-585.
33. Raffatellu, M., Wilson, R.P., Chessa, D., Andrews-Polymenis, H., Tran, Q.T., Lawhon, S., et al. (2005) SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica sero-type typhimurium invasion of epithelial cells. Infect Immun 73: 146-154.
34. Rodriguez-Escudero, I., Roelants, F.M., Thorner, J., Nombela, C., Molina, M., and Cid, V.J. (2005) Reconstitution of the mammalian PI3K-PTEN-Akt pathway in yeast. Biochem J (in press).
35. Rodríguez-Pachón, J.M., Martin, H., North, G., Rotger, R., Nombela, C., and 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.
36. Skrzypek, E., Myers-Morales, T., Whiteheart, S.W., and 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.
37. Steele-Mortimer, O., Knodler, L.A., Marcus, S.L., Scheid, M.P., Goh, B., Pfeifer, C.G., et al. (2000) Activation of Akt/protein kinase B in epithelial cells by the Salmonella typhimurium effector SigD. J Biol Chem 275: 37718-37724.
38. Stefan, C.J., Audhya, A., and Emr, S.D. (2002) The yeast synaptojanin-like proteins control the cellular distribution of phosphatidylinositol 4,5-bisphosphate. Mol Biol Cell 13: 542-557.
39. Terebiznik, M.R., Vieira, O.V., Marcus, S.L., Slade, A., Yip, C.M., Trimble, W.S., et al. (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.
40. Teruel, M.N., Blanpied, T.A., Shen, K., Augustine, G.J., and Meyer, T. (1999) A versatile microporation technique for the transfection of cultured CNS neurons. J Neurosci Meth 93: 37-48.
41. Valdivia, R.H. (2004) Modelling the function of bacterial virulence factors in Saccharomyces cerevisiae. Eukaryot Cell 3: 827-834.
42. Von Pawel-Rammingen, U., Telepnev, M.V., Schmidt, G., Aktories, K., Wolf-Watz, H., and 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.
43. Yoon, S., Liu, Z., Eyobo, Y., and Orth, K. (2003) Yersinia effector YopJ inhibits yeast MAPK signalling pathways by an evolutionarily conserved mechanism. J Biol Chem 278: 2131-2135.
44. Zaharik, M.L., Gruenheid, S., Perrin, A.J., and Finlay, B.B. (2002) Delivery of dangerous goods: Type III secretion in enteric pathogens. Int J Med Microbiol 291: 593-603.
45. Zhou, D., and Galin, J. (2001) Salmonella entry into host cells: the work in concert of type III secreted effector proteins. Microbes Infect 3: 1293-1298.
46. Zhou, D., Mooseker, M.S., and Galin, J.E. (1999) An invasion-associated Salmonella protein modulates the actin-bundling activity of plastin. Proc Natl Acad Sci USA 96: 10176-10181.
47. Zhou, D., Chen, L.M., Hernández, L., Shears, S.B., and 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.