Dual Lipid Modification of the Yeast Gγ Subunit Ste18p Determines Membrane Localization of Gβγ

REFERENCES

• Bhattacharya, S., L. Chen, J. R. Broach, and J. Powers 1995. Ras membrane targeting is essential for glucose signaling but not for viability in yeast. Proc. Natl. Acad. Sci. USA 92:2984–2988.
   PubMedGoogle Scholar
• Cadwallader, K. A., H. Paterson, S. G. Macdonald, and J. Hancock 1994. N-terminally myristoylated Ras proteins require palmitoylation or a polybasic domain for plasma membrane localization. Mol. Cell. Biol. 14:4722–4730.
   PubMedGoogle Scholar
• Chen, J. Q., M. Devivo, J. Dingus, A. Harry, J. R. Li, J. L. Sui, D. J. Carty, J. L. Blank, J. H. Exton, R. H. Stoffel, J. Inglese, R. J. Lefkowitz, D. E. Logothetis, J. D. Hildebrandt, and J. Iyengar 1995. A region of adenylyl cyclase 2 critical for regulation by G protein βγ subunits. Science 268:1166–1169.
   PubMed Web of Science ®Google Scholar
• Deschenes, R. J., and J. Broach 1987. Fatty acylation is important but not essential for Saccharomyces cerevisiae RAS function. Mol. Cell. Biol. 7:2344–2351.
   PubMedGoogle Scholar
• DeWaard, M., H. Y. Liu, D. Walker, V. E. S. Scott, C. A. Gurnett, and J. Campbell 1997. Direct binding of G-protein βγ complex to voltage-dependent calcium channels. Nature 385:446–450.
   PubMed Web of Science ®Google Scholar
• Dudler, T., and J. Gelb 1996. Palmitoylation of Ha-Ras facilitates membrane binding, activation of downstream effectors, and meiotic maturation in Xenopus oocytes. J. Biol. Chem. 271:11541–11547.
   PubMedGoogle Scholar
• Dunphy, J. T., W. K. Greentree, C. L. Manahan, and J. Linder 1996. G-protein palmitoyltransferase activity is enriched in plasma membranes. J. Biol. Chem. 271:7154–7159.
   PubMed Web of Science ®Google Scholar
• Farh, L., D. A. Mitchell, and J. Deschenes 1995. Farnesylation and proteolysis are sequential, but distinct steps in the CaaX box modification pathway. Arch. Biochem. Biophys. 318:113–121.
   PubMedGoogle Scholar
• Farnsworth, C. C., M. C. Seabra, L. H. Ericsson, M. H. Gelb, and J. Glomset 1994. Rab geranylgeranyl transferase catalyzes the geranylgeranylation of adjacent cysteines in the small GTPases Rab1A, Rab3A, and Rab5A. Proc. Natl. Acad. Sci. USA 91:11963–11967.
   PubMed Web of Science ®Google Scholar
• Ferro-Novick, S., and J. Novick 1993. The role of GTP-binding proteins in transport along the exocytic pathway. Annu. Rev. Cell Biol. 9:575–599.
   PubMedGoogle Scholar
• Finegold, A. A., W. R. Schafer, J. Rine, M. Whiteway, and J. Tamanoi 1990. Common modifications of trimeric G proteins and ras protein: involvement of polyisoprenylation. Science 249:165–169.
   PubMedGoogle Scholar
• Fujiyama, A., K. Matsumoto, and J. Tamanoi 1987. A novel yeast mutant defective in the processing of ras proteins: assessment of the effect of the mutation on processing steps. EMBO J. 6:223–228.
   PubMed Web of Science ®Google Scholar
• Fukuda, Y., T. Takao, H. Ohguro, T. Yoshizawa, T. Akino, and J. Shimonishi 1990. Farnesylated γ subunit of photoreceptor G protein indispensable for GTP binding. Nature 346:658–660.
   PubMedGoogle Scholar
• Gonzalo, S., and J. Linder 1998. SNAP-25 palmitoylation and plasma membrane targeting require a functional secretory pathway. Mol. Biol. Cell 9:585–597.
   PubMed Web of Science ®Google Scholar
• Grishin, A. V., J. L. Weiner, and J. Blumer 1994. Biochemical and genetic analysis of dominant-negative mutations affecting a yeast G-protein γ subunit. Mol. Cell. Biol. 14:4571–4578.
   PubMedGoogle Scholar
• Hancock, J. F., A. I. Magee, J. E. Childs, and J. Marshall 1989. All ras proteins are polyisoprenylated but only some are palmitoylated. Cell 57:1167–1177.
   PubMed Web of Science ®Google Scholar
• Hartwell, L. H. 1967. Macromolecule synthesis in temperature-sensitive mutants of yeast. J. Bacteriol. 93:1662–1670.
   PubMed Web of Science ®Google Scholar
• Hasson, M. S., D. Blinder, J. Thorner, and J. Jenness 1994. Mutational activation of the STE5 gene product bypasses the requirement for G protein β and γ subunits in the yeast pheromone response pathway. Mol. Cell. Biol. 14:1054–1065.
   PubMedGoogle Scholar
• He, B., P. Chen, S. Y. Chen, K. L. Vancura, S. Michaelis, and J. Powers 1991. RAM2, an essential gene of yeast, and RAM1 encode the two polypeptide components of the farnesyltransferase that prenylates a-factor and Ras proteins. Proc. Natl. Acad. Sci. USA 88:11373–11377.
   PubMed Web of Science ®Google Scholar
• Hirschman, J. E., G. S. DeZutter, W. F. Simonds, and J. Jenness 1997. The Gβγ complex of the yeast pheromone response pathway: subcellular fractionation and protein-protein interactions. J. Biol. Chem. 272:240–248.
   PubMedGoogle Scholar
• Inanobe, A., K. I. Morishige, N. Takahashi, H. Ito, M. Yamada, T. Takumi, H. Nishina, K. Takahashi, Y. Kanaho, T. Katada, and J. Kurachi 1995. Gβγ directly binds to the carboxyl terminus of the G protein-gated muscarinic K+ channel, GIRK1. Biochem. Biophys. Res. Commun. 212:1022–1028.
   PubMedGoogle Scholar
• Iniguez-Lluhi, J. A., M. I. Simon, J. D. Robishaw, and J. Gilman 1992. G protein βγ subunits synthesized in Sf9 cells. Functional characterization and the significance of prenylation of γ. J. Biol. Chem. 267:23409–23417.
   PubMed Web of Science ®Google Scholar
• Jenness, D. D., Y. Li, C. Tipper, and J. Spatrick 1997. Elimination of defective α-factor pheromone receptors. Mol. Cell. Biol. 17:6236–6245.
   PubMedGoogle Scholar
• Krapivinsky, G., L. Krapivinsky, K. Wickman, and J. Clapham 1995. Gβγ binds directly to the G protein-gated K+ channel, IKACh. J. Biol. Chem. 270:29059–29062.
   PubMedGoogle Scholar
• Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685.
   PubMed Web of Science ®Google Scholar
• Leeuw, T., C. Wu, J. D. Schrag, M. Whiteway, D. Y. Thomas, and J. Leberer 1998. Interaction of a G-protein β-subunit with a conserved sequence in Ste20/PAK family protein kinases. Nature 391:191–195.
   PubMed Web of Science ®Google Scholar
• Linder, M. E., C. Kleuss, and J. Mumby 1995. Palmitoylation of G-protein α subunits. Methods Enzymol. 250:314–330.
   PubMedGoogle Scholar
• Magee, A. I., L. Gutierrez, I. A. McKay, C. J. Marshall, and J. Hall 1987. Dynamic fatty acylation of p21N-ras. EMBO J. 6:3353–3357.
   PubMed Web of Science ®Google Scholar
• Manahan, C. L., and M. E. Linder. Personal communication.
   Google Scholar
• Muntz, K. H., P. C. Sternweis, A. G. Gilman, and J. Mumby 1992. Influence of γ subunit prenylation on association of guanine nucleotide-binding regulatory proteins with membranes. Mol. Biol. Cell 3:49–61.
   PubMedGoogle Scholar
• Nern, A., and J. Arkowitz 1998. A GTP-exchange factor required for cell orientation. Nature 391:195–198.
   PubMedGoogle Scholar
• Ohya, Y., H. Qadota, Y. Anraku, J. R. Pringle, and J. Botstein 1993. Suppression of yeast geranylgeranyl transferase I defect by alternative prenylation of two target GTPases, Rho1p and Cdc42p. Mol. Biol. Cell 4:1017–1025.
   PubMedGoogle Scholar
• Pfeffer, S. R., A. B. Dirac-Svejstrup, and J. Soldati 1995. Rab GDP dissociation inhibitor: putting Rab GTPases in the right place. J. Biol. Chem. 270:17057–17059.
   PubMedGoogle Scholar
• Powers, S., S. Michaelis, D. Broek, S. Santa Anna, J. Field, I. Herskowitz, and J. Wigler 1986. RAM, a gene of yeast required for a functional modification of RAS proteins and for production of mating pheromone a-factor. Cell 47:413–422.
   PubMedGoogle Scholar
• Pryciak, P. M., and J. Huntress 1998. Membrane recruitment of the kinase cascade scaffold protein Ste5 by the Gβγ complex underlies activation of the yeast pheromone response pathway. Genes Dev. 12:2684–2697.
   PubMed Web of Science ®Google Scholar
• Ray, K., C. Kunsch, L. M. Bonner, and J. Robishaw 1995. Isolation of cDNA clones encoding eight different human G protein γ subunits, including three novel forms designated the γ4, γ10, and γ11 subunits. J. Biol. Chem. 270:21765–21771.
   PubMed Web of Science ®Google Scholar
• Rehm, A., and J. Ploegh 1997. Assembly and intracellular targeting of the βγ subunits of heterotrimeric G proteins. J. Cell Biol. 137:305–317.
   PubMedGoogle Scholar
• Resh, M. D. 1996. Regulation of cellular signalling by fatty acid acylation and prenylation of signal transduction proteins. Cell Signal. 8:403–412.
   PubMed Web of Science ®Google Scholar
• Schafer, W. R., C. E. Trueblood, C. C. Yang, M. P. Mayer, S. Rosenberg, C. D. Poulter, S. H. Kim, and J. Rine 1990. Enzymatic coupling of cholesterol intermediates to a mating pheromone precursor and to the ras protein. Science 249:1133–1139.
   PubMed Web of Science ®Google Scholar
• Schandel, K. A., and J. Jenness 1994. Direct evidence for ligand-induced internalization of the yeast α-factor pheromone receptor. Mol. Cell. Biol. 14:7245–7255.
   PubMed Web of Science ®Google Scholar
• Shahinian, S., and J. Silvius 1995. Doubly-lipid-modified protein sequence motifs exhibit long-lived anchorage to lipid bilayer membranes. Biochemistry 34:3813–3822.
   PubMed Web of Science ®Google Scholar
• Simonds, W. F., B. J. E. Butrynski, N. Gautam, C. G. Unson, and J. Spiegel 1991. G-protein βγ dimers. Membrane targeting requires subunit coexpression and intact gamma C-A-A-X domain. J. Biol. Chem. 266:5363–5366.
   PubMedGoogle Scholar
• Song, J. P., and J. Dohlman 1996. Partial constitutive activation of pheromone responses by a palmitoylation-site mutant of a G protein α subunit in yeast. Biochemistry 35:14806–14817.
   PubMedGoogle Scholar
• Stone, D. E., G. M. Cole, M. D. Lopes, M. Goebl, and J. Reed 1991. N-Myristoylation is required for function of the pheromone-responsive Gα protein of yeast: conditional activation of the pheromone response by a temperature-sensitive N-myristoyl transferase. Genes Dev. 5:1969–1981.
   PubMedGoogle Scholar
• Trueblood, C. E., Y. Ohya, and J. Rine 1993. Genetic evidence for in vivo cross-specificity of the CaaX-box protein prenyltransferases farnesyltransferase and geranylgeranyltransferase-I in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:4260–4275.
   PubMed Web of Science ®Google Scholar
• Vancura, A., A. Sessler, B. Leichus, and J. Kuret 1994. Prenylation motif is required for plasma membrane localization and biochemical function of casein kinase I in budding yeast. J. Biol. Chem. 269:19271–19278.
   PubMedGoogle Scholar
• Wedegaertner, P. B., P. T. Wilson, and J. Bourne 1995. Lipid modifications of trimeric G proteins. J. Biol. Chem. 270:503–506.
   PubMed Web of Science ®Google Scholar
• Whiteway, M. S., and J. Thomas 1994. Site-directed mutations altering the CAAX box of Ste18, the yeast pheromone-response pathway G gamma subunit. Genetics 137:967–976.
   PubMedGoogle Scholar
• Zhang, F. L., and J. Casey 1996. Protein prenylation: molecular mechanisms and functional consequences. Annu. Rev. Biochem. 65:241–269.
   PubMed Web of Science ®Google Scholar