The yeast phosphatidylinositol kinase homolog TOR2 activates RHO1 and RHO2 via the exchange factor ROM2

Cell

Volumn 88, Issue 4, 1997, Pages 531-542

  Schmidt, Anja ^a   Bickle, Marc ^a   Beck, Thomas ^a   Hall, Michael N ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; PHOSPHATIDYLINOSITOL KINASE;

ARTICLE; CELL GROWTH; CYTOSKELETON; GENE DELETION; GENE MUTATION; GENE OVEREXPRESSION; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

EID: 0030906569     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81893-0     Document Type: Article

References (69)

1. Adams, A.E.M., and Pringle, J.R. (1984). Relationship of actin and tubulin distribution to bud growth in wildtype and morphogeneticmutant Saccharomyces cerevisiae. J. Cell Biol. 98, 934-945.
2. Adams, A.E.M., Johnson, D.I., Longnecker, R.M., Sloat, B.F., and Pringle, J.R. (1990). CDC42 and CDC43, two additional genes involved in budding and the establishment of cell polarity in the yeast Saccharomyces cerevisiae. J. Cell Biol. 111, 131-142.
3. Barbet, N.C., Schneider, U., Helliwell, S.B., Stansfield, I., Tuite, M.F., and Hall, M.N. (1996). TOR controls translation initiation and early G1 progression in yeast. Mol. Biol. Cell 7, 25-42.
4. Barfod, E.T., Zheng, Y., Kuang, W.-J., Hart, M.J., Evans, T., Cerione, R.A., and Ashkenazi, A. (1993). Cloning and expression of a human CDC42 GTPase-activating protein reveals a functional SH3-binding domain. J. Biol. Chem. 268, 26059-26062.
5. Benedetti, H., Raths, S., Crausaz, F., and Riezman, H. (1994). The END3 gene encodes a protein that is required for the internalization step of endocytosis and for actin cytoskeleton organization in yeast. Mol. Biol. Cell 5, 1023-1037.
6. Beretta, L, Gingras, A.-C., Svitkin, Y.V., Hall, M.N., and Sonenberg, N. (1996). Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent initiation of translation. EMBO J. 15, 658-664.
7. Cafferkey, R., Young, T.R., McLaughlin, M.M., Bergsma, D.J., Koltin, Y., Sathe, G.M., Faucette, L, Eng, W.K., Johnson, R.K., and Livi, G.P. (1993). Dominant missense mutations in a novel yeast protein related to mammalian phosphatidylinositol 3-kinase and VPS34 abrogate rapamycin toxicity. Mol. Cell. Biol. 13, 6012-6023.
8. Chen, G.C., Zheng, L, and Chan, C.S.M. (1996). The LIM domain-containing Dbm1 GTPase-activating protein is required for normal cellular morphogenesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 1376-1390.
9. Devereux, J., Haeberli, P., and Smithies, O. (1984). A comprehensive set of sequence analysis programs for the VAX. Nucl. Acids Res. 12, 387-395.
10. Di Como, C.J. and Arndt, K.T. (1996). Nutrients, via the TOR proteins, stimulate the association of Tap42 with type 2A phosphatases. Genes Dev. 10, 1904-1916.
11. Downward, J. (1995). A target for PI 3 kinase. Nature 376, 353-354.
12. Drgonova, J., Drgon, T., Tanaka, K, Kollar, R., Chen, G.C. Ford, R.A., Chan, C.S., Takai, Y., and Cabib, E. (1996). Rho1p, a yeast protein at the interface between cell polarization and morphogenesis. Science 272, 277-279.
13. Drubin, D.G. (1991). Development of cell polarity in budding yeast. Cell 65, 1093-1096.
14. Dunn, T.M., and Shortle, D. (1990). Null alleles of SAC7 suppress temperature-sensitive actin mutations in Saccharomyces cerevisiae. Mol. Cell. Biol. 10, 2308-2314.
15. Errede, B., and Levin, D.E., (1993). A conserved kinase cascade for MAP kinase activation in yeast. Curr. Opin. Cell Biol. 2, 254-260.
16. Guthrie, C., and Fink, G.R., eds. (1991). Methods in Enzymology: Guide to Yeast Genetics and Molecular Biology, Volume 194 (New York: Academic Press).
17. Gyuris, J., Golemis, E., Chertkov, H., and Brent, R. (1993). Cdi1, a human G1 and S phase protein phosphatase that associates with Cdk2. Cell 75, 791-803.
18. Hall, A. (1994). Small GTP-binding proteins and the regulation of the actin cytoskeleton. Annu. Rev. Cell Biol. 10, 31-54.
19. Hall, C., Monfries, C., Smith, P., Lim, H.H., Kozma, R., Ahmed, S., Vanniasingham, V., Leung, T., and Lim, L. (1990). Novel human brain cDNA encoding a 34,000 M protein n-chimaerin, related to both the regulatory domain of protein kinase C and BCR, the product of the breakpoint cluster region gene. J. Mol. Biol. 211, 11-16.
20. Hall, M.N. (1996). The TOR signalling pathway and growth control in yeast. Biochem. Soc. Trans. 24, 234-239.
21. Hartley, K.O., Gell, D., Smith, G.C.M., Zhang, H., Divecha, N., Connelley, M.A., Admon, A., Lees-Miller, S.P., Andersen, C.W., and Jackson, S.P. (1995). DNA-dependent protein kinase catalytic subunit: a relative of phosphatidylinositol 3-kinase and the ataxia telangiectasia gene product. Cell 82, 849-856.
22. Heisterkamp, N., Stam, K., Groffen, J., de Klein, A., and Grosveld, G. (1985). Structural organization of the bcr gene and its role in the Ph' translocation. Nature 315, 758-761.
23. Heitman, J., Movva, N.R., and Hall, M.N. (1991). Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253, 905-909.
24. Helliwell, S.B., Wagner, P., Kunz, J., Deuter-Reinhard, M., Henriquez, R., and Hall, M.N. (1994). TOR1 and TOR2 are structurally and functionally similar but not identical phosphatidylinositol kinase homologs in yeast. Mol. Biol. Cell 5, 105-118.
25. Hunter, T. (1995). When is a lipid kinase not a lipid kinase? When it is a protein kinase. Cell 83, 1-4.
26. Igual, J.C, Johnson, A.L., and Johnston, LH. (1996). Coordinated regulation of gene expression by the cell cycle transcription factor SWI4 and the protein kinase C MAP kinase pathway for yeast cell wall integrity. EMBO J. 15, 5001-5013.
27. Imai, J., Toh-e, A., and Matsui, Y. (1996). Genetic analysis of the Saccharomyces cerevisiae RHO3 gene, encoding a Rho-type small GTPase, provides evidence for a role in bud formation. Genetics 142, 359-369.
28. Ito, H., Fukuda, Y., Murata, K., and Kimura, A. (1983).Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168.
29. Johnson, D.I., and 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.
30. Kamada, Y., Qadota, H., Python, C.P., Anraku, Y., Ohya, Y., and Levin, D.E. (1996). Activation of yeast protein kinase C by Rho1 GTPase. J. Biol. Chem. 271, 9193-9196.
31. Keith, C.T., and Schreiber, S.L. (1995). PIK-related kinases: DNA repair, recombination, and cell cycle checkpoints. Science 270, 50-51.
32. Kilmartin, J.V., and Adams, A.E. (1984). Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccharomyces. J. Cell Biol. 98, 922-933.
33. Kohn, A.D., Takeuchi, F., and Roth, R.A. (1996). Akt, a pleckstrin homology domain containing kinase, is activated primarily by phos-phorylation. J. Biol. Chem. 271, 21920-21926.
34. Kron, S.J., and Gow, N.A.R. (1995). Budding yeast morphogenesis: signalling, cytoskeleton and cell cycle. Curr. Opin. Cell Biol. 7, 845-855.
35. Kunz, J., Henriquez, R., Schneider, U., Deuter-Reinhard, M., Movva, N.R., and Hall, M.N. (1993). Target of rapamycin in yeast, TOR2, is an essential phosphatidylinositol kinase homolog required for G1 progression. Cell 73, 585-596.
36. Lancaster, C.A., Taylor-Harris, P.M., Self, A.J., Brill, S.,van Erp, H.E., and Hall, A. (1994). Characterization of rho GAP. J. Biol. Chem. 269, 1137-1142.
37. Lemmon, M.A., Ferguson, K.M., and Schlessinger, J. (1996). PH domains: diverse sequences with a common fold recruit signaling molecules to the cell surface. Cell 85, 621-624.
38. Levin, D.E., and Bartlett-Heubusch, E., (1992). Mutants in the S.cerevisiae PKC1 gene display a cell cycle-specific osmotic stability defect. J. Cell Biol. 116, 1221-1229.
39. Machesky, L.M., and Hall, A. (1996). Rho: a connection between membrane receptor signalling and the cytoskeleton. Trends Cell Biol. 6, 304-310.
40. Madaule, P., Axel, R., and Myers, A.M. (1987). Characterization of two members of the rho gene family from the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 84, 779-783.
41. Masuda, T., Tanaka, K., Nonaka, H., Maeda, A., Musha, T., and Takai, Y. (1994). Molecular cloning and characterization of yeast rho GDP dissociation inhibitor. J. Biol. Chem. 269, 19713-19718.
42. Matsui, Y., and Toh-e, A. (1992). Isolation and characterization of two novel ras superfamily genes in Saccharomyces cerevisiae. Gene 114, 43-49.
43. Matsui, Y., and Toh-e, A. (1992b). Yeast RHO3 and RHO4 ras superfamily genes are necessary for bud growth, and their defect is suppressed by a high dose of bud formation genes CDC42 and BEM1. Mol. Cell. Biol. 12, 5690-5699.
44. Mazzoni,C., Zarov, P., Rambourg, A., and Mann, C. (1993). The SLT2 (MPK1) MAP kinase homolog is involved in polarized cell growth in Saccharomyces cerevisiae. J. Cell Biol. 123, 1821-1833.
45. Mosch, H.-U., Roberts, R.L, and 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. USA 93, 5352-5356.
46. Müller, L., Xu, G., Well, R., Hollenberg, C.P., and Piepersberg, W. (1994). LRG1 is expressed during sporulation in Saccharomyces cerevisiae and contains motifs similar to LIM and rho/racGAP domains. Nucl. Acids Res. 22, 3151-3154.
47. Nonaka, H., Tanaka, K., Hirano, H., Fujiwara, T., Kohno, H., Umikawa, M., Mino, A., and Takai, Y. (1995). A downstream target of RHO1 small GTP-binding protein is PKC1, a homolog of protein kinase C, which leads to activation of the MAP kinase cascade in Saccharomyces cerevisiae. EMBO J. 14, 5931-5938.
48. Ozaki, K., Tanaka, K., Imamura, H., Hihara, T., Kameyama, T., Nonaka, H., Hirano, H., Matsuura, Y., and Takai, Y. (1996). ROM1p and ROM2p are small GDP/GTP exchange proteins (GEPs) for the Rho1p small GTP binding proteins in Saccharomyces cerevisiae. EMBO J. 15, 2196-2207.
49. Park, H.-O., Chant, J., and Herskowitz, I. (1993). BUD2 encodes a GTPase-activating protein for Bud1/Rsr1 necessary for proper budsite selection in yeast. Nature 365, 269-274.
50. Peterson, J., Zheng, Y., Benderl, L., Myers, A., Cerione, R., and Bender, A. (1994). Interactions between the bud emergence proteins Bem1p and Bem2p and Rho-type GTPases in yeast. J. Cell Biol. 127, 1395-1406.
51. Qadota, H., Anraku,Y., Botstein, D., and Ohya, Y. (1994). Conditional lethality of a yeast strain expressing human RhoA in place of RHO1. Proc. Natl. Acad. Sci. USA 97, 9317-9321.
52. Qadota, H., Python C.P. Inoue, S.B., Arisawa, M., Anraku,Y., Zheng, Y., Watanabe, T., Levin, D.E., and Ohya, Y. (1996). Identification of yeast Rho1p GTPase as a regulatory subunit of 1,3-β-glucan synthase. Science 272, 279-281.
53. Reif, K., Nobes, C.D., Thomas, G., Hall, A., and Cantrell, D. (1996). Phosphatidylinositol 3-kinase signals activate a selective subset of Rac/Rho-dependent effector pathways. Curr. Biol. 6, 1445-1455.
54. Ridley, A.J. (1996) Rho: theme and variations. Curr. Biol. 6, 1256-1263.
55. Roemer, T., Paravicini, G., Payton, M.A., and Bussey, H. (1994). Characterization of the yeast (1→6)-β-glucan biosynthetic components, Kre6p and Skn1 p, and genetic interactions between the PKC1 pathway and extracellular matric assembly. J. Cell Biol. 127, 567-579.
56. Sambrook, J, Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, Second Edition (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press).
57. Schmidt, A., Kunz, J., and Hall, M.N. (1996). TOR2 is required for organization of the actin cytoskeleton in yeast. Proc. Natl. Acad. Sci. USA 93, 13780-13785.
58. Shaw, G. (1996) The pleckstrin homology domain: an intriguing multifunctional protein module. BioEssays 18, 35-46.
59. Stevenson, B.J., Ferguson, B., De Virgilio, C., Bi, E., Pringle, J.R., Ammerer, G., and Sprague, G.F., Jr. (1995). Mutation in RGA1, which encodes a putative GTPase-activating protein for the polarity-establishment protein CDC42p, activates the pheromone-response pathway in the yeast Saccharomyces cerevisiae. Genes Dev. 9, 2949-2963
60. Tanaka, K., Lin, B.K., Wood, D.R., and Tamanoi, F. (1991). IRA1, an upstream negative regulator of RAS in yeast, is a RAS GTPase-activating protein. Proc. Natl. Acad. Sci. USA 8, 468-472.
61. von Manteuffel, S.R., Gingras, A.-C., Ming, X.-F., Sonenberg, N., and Thomas, G. (1996). 4E-BP1 phosphorylation is mediated by the FRAP-p70s6k pathway and is independent of mitogen-activated protein kinase. Proc. Natl. Acad. Sci. USA 93, 4076-4080.
62. Wach, A., Brachat, A., Pöhlmann, R., and Philippsen, P. (1994). New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793-1808.
63. Yamamoto, T., Kaibuchi, K., Mizuno, T., Hiroyoshi, M., Shirataki, H., and Takai, Y. (1990). Purification and characterization from bovine brain cytosol of proteins that regulate the GDP/GTP exchange reaction of smg p21s, ras p21-like GTP-binding proteins. J. Biol. Chem. 265, 16626-16634.
64. Yamochi, W., Tanaka, K., Nonaka, H., Maeda, A., Musha, T., and Takai, Y. (1994). Growth site localization of Rho1 small GTP-binding protein and its involvement in bud formation in Saccharomyces cerevisiae. J. Cell Biol. 125, 11077-11093.
65. Zakian, V.A. (1995). ATM-related genes: what do they tell us about functions of the human gene? Cell 82, 685-687.
66. Zheng, X.-F., Fiorentino, D., Chen, J., Crabtree, G.R., and Schreiber, S.L. (1995). TOR kinase domains are required for two distinct functions, only one of which is inhibited by rapamycin. Cell 82, 121-130.
67. Zheng, Y., Hart, M.J., Shinjo, K., Evans, T., Bender, A., and Cerione, R.A. (1993). Biochemical comparisons of the Saccharomyces cerevisiae Bem2 and Bem3 proteins. J. Biol. Chem. 268, 24629-24634.
68. Zheng, Y., Cerione, R., and Bender, A. (1994). Control of the yeast bud-site assembly GTPase CDC42. J. Biol. Chem. 269, 2369-2372.
69. Ziman, M., O'Brien, J.M., Ouellette, LA., Chruch,W.R., and Johnson, D.I. (1991). Mutational analysis of CDC42Sc, a Saccharomyces cerevisiae gene that encodes a putative GTP-binding protein involved in the control of cell polarity. Mol. Cell. Biol. 11, 3537-3544.