Expression of the Salmonella spp. virulence factor SifA in yeast alters Rho1 activity on peroxisomes

Molecular Biology of the Cell

Volumn 21, Issue 20, 2010, Pages 3567-3577

  Vinh, Dani B N ^a   Ko, Dennis C ^a   Rachubinski, Richard A ^b   Aitchison, John D ^c   Miller, Samuel I ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

^c INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN SIFA; RHO FACTOR; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; ENDOSOME; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; SALMONELLA; YEAST;

ACTINS; ANIMALS; BACTERIAL PROTEINS; CELL COMPARTMENTATION; CHO CELLS; CRICETINAE; CRICETULUS; ENDOSOMES; GLYCOPROTEINS; GREEN FLUORESCENT PROTEINS; INTRACELLULAR MEMBRANES; MICROSCOPY, FLUORESCENCE; MUTATION; ORGANELLE SHAPE; PEROXISOMES; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; RHO GTP-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SALMONELLA TYPHIMURIUM; VIRULENCE FACTORS;

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

EID: 77958046217     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-06-0482     Document Type: Article

References (65)

1. Abrahams, G. L., Muller, P., and Hensel, M. (2006). Functional dissection of SseF, a type III effector protein involved in positioning the Salmonella-containing vacuole. Traffic 7, 950-965.
2. Alto, N. M., et al. (2006). Identification of a bacterial type III effectors family with G protein mimicry functions. Cell 124, 133-145.
3. Beuzon, C. R., Meresse, S., Unsworth, K. E., Ruiz-Albert, J., Garvis, S., Waterman, S. R., Ryder, T. A., Boucrot, E., and Holden, D. W. (2000). Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J. 19, 3235-3249.
4. Boucrot, E., Beuzon, C. R., Holden, D. W., Gorvel, J. P., and Meresse, S. (2003). Salmonella typhimurium SifA effector protein requires its membrane-anchoring C-terminal hexapeptide for its biological function. J. Biol. Chem. 278(16), 14196-14202.
5. Boucrot, E., Henry, T., Borg, J. P., Gorvel, J. P., and Meresse, S. (2005). The intracellular fate of Salmonella depends on the recruitment of kinesin. Science 308, 1174-1178.
6. Boukh-Viner, T., et al. (2005). Dynamic ergosterol- and ceramide-rich domains in the peroxisomal membrane serve as an organizing platform for peroxisome fusion. J. Cell Biol. 168, 761-773. (Pubitemid 40328160)
7. Bowers, K., and Stevens, T. H. (2005). Protein transport from the late Golgi to the vacuole in the yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta 1774, 438-454.
8. Brumell, J. H., Goosney, D. L., and Finlay, B. B. (2002). SifA, a type III secreted effector of Salmonella typhimurium, directs Salmonella-induced filament (Sif) formation along microtubules. Traffic 3, 407-415.
9. Bulgin, R., Raymond, B., Garnett, J. A., Frankel, G., Crepin, V. F., Berger, C. N., and Arbeloa, A. (2010). Bacterial guanine nucleotide exchange factors SopE-like and WxxxE effectors. Infect. Immun. 78, 1417-1425.
10. Christen, M., Coye, L. H., Hontz, J. S., LaRock, D. L., Pfuetzner, R. A., Megha, and Miller, S. I. (2009). Activation of a bacterial virulence protein by the GTPase RhoA. ScienceSignal 95, 1-6.
11. Curak, J., Rohde, J., and Stagljar, I. (2009). Yeast as a tool to study bacterial effectors. Curr. Opin. Microbiol. 12, 18-23.
12. Eitzen, G. (2003). Actin remodeling to facilitate membrane fusion. Biochim. Biophys. Acta 1641, 175-181.
13. Fagarasanu, A., Fagarasanu, M., and Rachubinski, R. A. (2007). Maintaining peroxisome populations: a story of division and inheritance. Annu. Rev. Cell Dev. Biol. 23, 321-344.
14. Guignot, J., Caron, E., Beuzon, C., Bucci, C., Kagan, J., Roy, C., and Holden, D. W. (2004). Microtubule motors control membrane dynamics of Salmonella-containing vacuoles. J. Cell Sci. 117, 1033-1045.
15. Haraga, A., Ohlson, M. B., and Miller, S. I. (2008). Salmonellae interplay with host cells. Nat. Rev. Microbiol. 6, 53-66.
16. Hoepfner, D., van den Berg, M., Philippsen, P., Tabak, H. F., and Hettema, E. H. (2001). A role for Vps1p, actin, and the Myo2p motor in peroxisome abundance and inheritance in Saccharomyces cerevisiae. J. Cell Biol. 155, 979-990.
17. Huang, Z., Sutton, S. E., Wallenfang, A. J., Orchard, R. C., Wu, X., Feng, Y., Chai, J., and Alto, N. M. (2009). Structural insights into host GTPase isoform selection by a family of bacterial GEF mimics. Nat. Struct. Mol. Biol. 16, 853-860.
18. Huh, W. K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weissman, J. S., and O'Shea, E. K. (2003). Global analysis of protein localization in budding yeast. Nature 425, 686-691.
19. Jackson, L. K., Nawabi, P., Hentea, C., Roark, E. A., and Haldar, K. (2008). The Salmonella virulence protein SifA is a G protein antagonist. Proc. Natl. Acad. Sci. USA 105, 14141-14146.
20. Kaksonen, M., Sun, Y., and Drubin, D. G. (2003). A Pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 115, 475-487.
21. Kaksonen, M., Toret, C. P., and Drubin, D. G. (2005). A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123, 305-320.
22. Koch, A., Schneider, G., Luers, G. H., and Schrader, M. (2004). Peroxisome elongation and constriction but not fission can occur independently of dynamin-like protein 1. J. Cell Sci. 117, 3995-4006.
23. Kuhle, V., Jackel, D., and Hensel, M. (2004). Effector proteins encoded by Salmonella pathogenicity island 2 interfere with the microtubule cytoskeleton after translocation into host cells. Traffic 5, 356-370.
24. Kuhle, V., Abrahams, G. L., and Hensel, M. (2006). Intracellular Salmonella enterica redirect exocytic transport processes in a Salmonella pathogenicity island 2-dependent manner. Traffic 7, 716-730.
25. Lesser, C. F., and Miller, S. I. (2001). Expression of microbial virulence proteins in Saccharomyces cerevisiae models mammalian infection. EMBO J. 20(8), 1840-1841.
26. Li, X., Baumgart, E., Dong, G. X., Morrell, J. C., Jimenez-Sanchez, G., Valle, D., Smith, K. D., and Gould, S. J. (2002). PEX11alpha is required for peroxisome proliferation in response to 4-phenylbutyrate but is dispensable for peroxisome proliferator-activated receptor alpha-mediated peroxisome proliferation. Mol. Cell. Biol. 22(23), 8226-8240.
27. Lorra, C., and Huttner, W. B. (1999). The mesh hypothesis of Golgi dynamics. Nat. Cell Biol. 1, E113-115.
28. Marelli, M., et al. (2004). Quantitative mass spectrometry reveals a role for the GTPase Rho1p in actin organization on the peroxisome membrane. J. Cell Biol. 167(6), 1099-1112. (Pubitemid 40066625)
29. McMahon, H. T., and Gallop, J. L. (2005). Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438, 590-596.
30. Meresse, S., Unsworth, K. E., Habermann, A., Griffiths, G., Fang, F., Martinez-Lorenzo, M. J., Waterman, S. R., Gorvel, J.-P., and Holden, D. W. (2001). Remodelling of the actin cytoskeleton is essential for replication of intravacuolar Salmonella. Cell Microbiol. 3, 567-577.
31. Miao, E. A., Brittnacher, M., Haraga, A., Jeng, R. L., Welch, M. D., and Miller, S. I. (2003). Salmonella effectors translocated across the vacuolar membrane interact with the actin cytoskeleton. Mol. Microbiol. 48, 401-415.
32. Motley, A. M., and Hettema, E. H. (2007). Yeast peroxisomes multiply by growth and division. J. Cell Biol. 178, 399-410.
33. Mumberg, D., Muller, R., and Funk, M. (1995). Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156, 119-122.
34. Newpher, T. M., Smith, R. P., Lemmon, V., and Lemmon, S. K. (2005). In vivo dynamics of clathrin and its adaptor-dependent recruitment to the actinbased endocytic machinery in yeast. Dev. Cell 9, 87-98.
35. Nickerson, D. P., Brett, C. L., and Merz, A. J. (2009). Vps-C complexes: gatekeepers of endolysosomal traffic. Curr. Opin. Cell Biol. 21, 543-551.
36. Ohlson, M. B., Huang, Z., Alto, N. M., Blanc, M. P., Dixon, J. E., Chai, J., and Miller, S. I. (2008). Structure and function of Salmonella SifA indicate that its interactions with SKIP, SseJ, and RhoA family GTPases induce endosomal tubulation. Cell Host Microbe 4, 434-446.
37. Platta, H. W., and Erdmann, R. (2007). Peroxisomal dynamics. Trends Cell Biol. 17, 474-484.
38. Poh, J., Odendall, C., Spanos, A., Boyle, C., Liu, M., Freemont, P., and Holden, D. W. (2008). SteC is a Salmonella kinase required for SPI-2-dependent F-actin remodelling. Cell Microbiol. 10(1), 20-30.
39. Portillo, G-D, F., Zwick, M. B., Leung, K. Y., and Finlay, B. B. (1993). Salmonella induces the formation of filamentous structures containing lysosomal membrane glycoproteins in epithelial cells. Proc. Natl. Acad. Sci. USA 90, 10544-10548.
40. Praefcke, G.J.K., and McMahon, H. T. (2004). The dynamin superfamily: universal membrane tubulation and fission molecules? Nat. Rev. Mol. Cell Biol. 5, 133-147.
41. Ramsden, A. E., Holden, D. W., and Mota, L. J. (2007a). Membrane dynamics and spatial distribution of Salmonella-containing vacuoles. Trends Microbiol. 15, 516-524.
42. Ramsden, A. E., Mota, L. J., Munter, S., Shorte, S. L., and Holden, D. W. (2007b). The SPI-2 type III secretion system restricts motility of Salmonella-containing vacuoles. Cell Microbiol. 9, 2517-2529.
43. Reinicke, A. T., Hutchinson, J. L., Magee, A. I., Mastroeni, P., Trowsdale, J., and Kelly, A. P. (2005). A Salmonella typhimurium effector protein SifA is modified by host cell prenylation and S-acylation machinery. J. Biol. Chem. 280, 14620-14627.
44. Ridley, A. J. (2006). Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol. 16, 522-529.
45. Rottensteiner, H., Stein, K., Sonnenhol, E., and Erdmann, R. (2003). Conserved function of Pex11p and the novel Pex25p and Pex27p in peroxisome biogenesis. Mol. Biol. Cell 14, 4316-4328.
46. Ruiz-Albert, J., Yu, X. J., Beuzon, C. R., Blakey, A. N., Galyov, E. E., and Holden, D. W. (2002). Complementary activities of SseJ and SifA regulate dynamics of the Salmonella typhimurium vacuolar membrane. Mol. Microb. 44, 645-661.
47. Saleem, R. A., Knoblach, B., Mast, F. D., Smith, J. J., Boyle, J., Dobson, C. M., Long-O'Donnell, R., Rachubinski, R. A., and Aitchison, J. D. (2008). Genomewide analysis of signaling networks regulating fatty acid-induced gene expression and organelle biogenesis. J. Cell Biol. 181, 281-292.
48. Schrader, M., and Fahimi, H. D. (2006). Growth and division of peroxisomes. Int. Rev. Cytol. 255, 237-290.
49. Siggers, K. A., and Lesser, C. F. (2008). The yeast Saccharomyces cerevisiae: a versatile model system for the identification and characterization of bacterial virulence proteins. Cell Host Microbe 4, 8-15.
50. Smith, J. J., Marelli, M., Christmas, R. H., Vizeacoumar, F. J., Dilworth, D. J., Ideker, T., Galitski, T., Dimitrov, K., Rachubinski, R. A., and Aitchison, J. D. (2002). Transcriptome profiling to identify genes involved in peroxisome assembly and function. J. Cell Biol. 158(2), 259-271.
51. Smith, J. J., and Aitchison, J. D. (2009). Regulation of peroxisome dynamics. Curr. Opin. Cell Biol. 21, 119-126.
52. Steele-Mortimer, O. (2008). The Salmonella-containing vacuole-moving with the times. Curr. Opin. Microbiol. 11, 38-45.
53. Stein, M. A., Leung, K. Y., Zwick, M., Garcia-del Portillo, F., and Finlay, B. B. (1996). Identification of a Salmonella virulence gene required for formation of filamentous structures containing lysosomal membrane glycoproteins within epithelial cells. Mol. Microbiol. 20, 151-164.
54. Tam, Y. Y., Torres-Guzman, J. C., Vizeacoumar, F. J., Smith, J. J., Marelli, M., Aitchison, J. D., and Rachubinski, R. A. (2003). Pex11-related proteins in peroxisome dynamics: a role for the novel peroxin Pex27p in controlling peroxisome size and number in Saccharomyces cerevisiae. Mol. Biol. Cell 14, 4089-4102.
55. Thoms, S., and Erdmann, R. (2005). Dynamin-related proteins an Pex11 proteins in peroxisome division and proliferation. FEBS J. 272, 5169-5181.
56. Thoms, S., Debelyy, M. O., Nau, K., Meyer, H. E., and Erdmann, R. (2008). Lpx1p is a peroxisomal lipase required for normal peroxisome morphology. FEBS J. 275, 504-514.
57. Valdivia, R. H. (2004).) Modeling the function of bacterial virulence factors in Saccharomyces cerevisiae. Eukaryot. Cell 3, 827-834.
58. Vater, C. A., Raymond, C. K., Ekena, K., Howald-Stevenson, I., and Stevens, T. H. (1992). The VPS1 protein, a homolog of dynamin required for vacuolar protein sorting in Saccharomyces cerevisiae, is a GTPase with two functionally separable domains. J. Cell Biol. 119(4), 773-786.
59. Vida, T. A., and Emr, S. D. (1995). A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol. 128(5), 779-792.
60. Vizeacoumar, F. J., Torres-Guzman, J. C., Tam, Y.Y.C., Aitchison, J. D., and Rachubinski, R. A. (2003). YHR150w and YDR479c encode peroxisomal integral membrane proteins involved in the regulation of peroxisome number, size, and distribution in Saccharomyces cerevisiae. J. Cell Biol. 161, 321-332.
61. 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.
62. Wach, A., Brachat, A., Alberti-Segui, C., Rebischung, C., and Philippsen, P. (1997). Heterologous HIS3 marker and GFP reporter modules for PCR-targeting in Saccharomyces cerevisiae. Yeast 13, 1065-1075.
63. Winzeler, E. A., et al. (1999). Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285, 901-906.
64. Yan, M., Rayapuram, N., and Subramani, S. (2005). The control of peroxisome number and size during division and proliferation. Curr. Opin. Cell Biol. 17, 376-383.
65. Yu, X., and Cai, M. (2004). The yeast dynamin-related GTPase Vps1p functions in the organization of the actin cytoskeleton via interaction with Sla1p. J. Cell Sci. 117, 3839-3853.