Plant Farnesyltransferase Can Restore Yeast Ras Signaling and Mating

REFERENCES

• Anant, J. S., O. C. Ong, H. Xie, S. Clarke, P. J. O’Brien, and B. K. K. Fung. 1992. In vivo differential prenylation of retinal cyclic GMP phosphodiesterase catalytic subunits. J. Biol. Chem. 267:687–690.
   PubMed Web of Science ®Google Scholar
• Anderegg, R. J., R. Betz, S. A. Carr, J. W. Crabb, and W. Duntze. 1988. Structure of the Saccharomyces cerevisiae mating hormone a-factor: identification of S-farnesyl cysteine as a structural component. J. Biol. Chem. 263:18236–18240.
   PubMed Web of Science ®Google Scholar
• Ashby, M. N., P. R. Errada, V. L. Boyartchuk, and J. Rine. 1993. Isolation and DNA sequence of the STE14 gene encoding farnesyl cysteine:carboxyl methyltransferase. Yeast 9:907–913.
   PubMedGoogle Scholar
• Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1995. Current protocols in molecular biology. John Wiley & Sons, Inc., New York, N.Y.
   Google Scholar
• Biermann, B. J., T. A. Morehead, S. E. Tate, J. R. Price, S. K. Randall, and D. N. Crowell. 1994. Novel isoprenylated proteins identified by an expression library screen. J. Biol. Chem. 269:25251–25254.
   PubMedGoogle Scholar
• Boeke, J. D., F. LaCroute, and G. R. Fink. 1984. A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast:5-fluoro-orotic acid resistance. Mol. Gen. Genet. 197:345–346.
   PubMedGoogle Scholar
• Boeke, J. D., J. Trueheart, G. Natsoulis, and G. R. Fink. 1987. 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol. 154:164–175.
   PubMed Web of Science ®Google Scholar
• Boguski, M. S., A. W. Murray, and S. Powers. 1992. Novel repetitive sequence motifs in the α and β subunits of prenyl-protein transferases and homology of the α subunit to the MAD2 gene product of yeast. New Biol. 4:408–411.
   PubMedGoogle Scholar
• Caplan, A. J., J. Tsai, P. J. Casey, and M. G. Douglas. 1992. Farnesylation of YDJ1p is required for function at elevated growth temperatures in Saccharomyces cerevisiae. J. Biol. Chem. 267:18890–18895.
   PubMed Web of Science ®Google Scholar
• Caplin, B. E., L. A. Hettich, and M. S. Marshall. 1994. Substrate characterization of the Saccharomyces cerevisiae protein farnesyltransferase and type-I protein geranylgeranyltransferase. Biochim. Biophys. Acta 1205:39–48.
   PubMedGoogle Scholar
• Casey, P. J., P. A. Solski, C. J. Der, and J. E. Buss. 1989. p21ras is modified by a farnesyl isoprenoid. Proc. Natl. Acad. Sci. USA 86:8323–8327.
   PubMed Web of Science ®Google Scholar
• Chan, R. K., and C. A. Otte. 1982. Isolation and genetic analysis of Saccharomyces cerevisiae mutants supersensitive to G1 arrest by a factor and a factor pheromones. Mol. Cell. Biol. 2:11–20.
   PubMedGoogle Scholar
• Chen, W.-J., D. A. Andres, J. L. Goldstein, D. W. Russel, and M. S. Brown. 1991. cDNA cloning and expression of the peptide-binding β subunit of rat p21 ras farnesyltransferase, the counterpart of the yeast DPR1/RAM1. Cell 66:327–334.
   PubMedGoogle Scholar
• Cutler, S., M. Ghassemian, D. Bonetta, S. Cooney, and P. McCourt. 1996. A protein farnesyl transferase involved in ABA signal transduction in Arabi- dopsis. Science 273:1239–1241.
   PubMed Web of Science ®Google Scholar
• Deschenes, R. J., J. B. Stimmel, S. Clarke, J. Stock, and J. R. Broach. 1989. RAS2 protein of Saccharomyces cerevisiae is methyl-esterified at its carboxyl terminus. J. Biol. Chem. 264:11865–11873.
   PubMed Web of Science ®Google Scholar
• De Smedt, F., A. Boom, X. Pesesse, S. N. Schiffmann, and C. Erneux. 1996. Post-translational modification of human brain type I inositol-1,4,5-trisphos- phate 5-phosphatase by farnesylation. J. Biol. Chem. 271:10419–10424.
   PubMed Web of Science ®Google Scholar
• Emr, S. D., A. Vassarotti, J. Garrett, B. L. Geller, M. Takeda, and M. G. Douglas. 1986. The amino terminus of the yeast F1-ATPase beta-subunit precursor functions as a mitochondrial import signal. J. Cell Biol. 102:523–533.
   PubMedGoogle Scholar
• Fukada, Y., T. Takao, H. Ohguro, T. Yoshizawa, T. Akino, and Y. Shimonishi. 1990. Farnesylated γ-subunit of photoreceptor G protein indispensible for GTP binding. Nature (London) 346:658–660.
   PubMedGoogle Scholar
• Gietz, R. D., and A. Sugino. 1988. New yeast and Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74:527–534.
   PubMed Web of Science ®Google Scholar
• Goldstein, J. L., and M. S. Brown. 1990. Regulation of the mevalonate pathway. Nature (London) 343:425–430.
   PubMed Web of Science ®Google Scholar
• Goodman, L. E., C. M. Perou, A. Fujiyama, and F. Tamanoi. 1988. Structure and expression of yeast DPR1, a gene essential for the processing and intracellular localization of ras proteins. Yeast 4:271–281.
   PubMedGoogle Scholar
• Gutierrez, L., A. I. Magee, C. J. Marshall, and J. F. Hancock. 1989. Post- translational processing of p21ras is two-step and involves carboxyl-methylation and carboxyl-terminal proteolysis. EMBO J. 8:1093–1098.
   PubMed Web of Science ®Google Scholar
• Hancock, J. F., A. I. Magee, J. E. Childs, and C. J. Marshall. 1989. All ras proteins are polyisoprenylated but only some are palmitoylated. Cell 57:1167–1177.
   PubMed Web of Science ®Google Scholar
• He, B., P. Chen, S.-Y. Chen, K. L. Vancura, S. Michaelis, and S. 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
• Inglese, J., W. J. Koch, M. G. Caron, and R. J. Lefkowitz. 1992. Isoprenylation in regulation of signal transduction by G-protein-coupled receptor kinases. Nature (London) 359:147–150.
   PubMedGoogle Scholar
• Inglese, J., W. J. Koch, M. G. Caron, and R. J. Lekowitz. 1992. Isoprenylation of a protein kinase: requirement of farnesylation/α-carboxyl methylation for full enzymatic activity of rhodopsin kinase. J. Biol. Chem. 267:1422–1425.
   PubMedGoogle Scholar
• Ito, H., Y. Fukuda, K. Murata, and A. Kimura. 1983. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153:163–168.
   PubMed Web of Science ®Google Scholar
• Kamiya, Y., A. Sakurai, S. Tamura, N. Takahashi, K. Abe, E. Tsuchiya, S. Fukui, C. Kitada, and M. Fujino. 1978. Structure of the rhodotorucine A, a novel lipopeptide, inducing mating tube formation in Rhodosporidium toruloides. Biochem. Biophys. Res. Commun. 83:1077–1083.
   PubMedGoogle Scholar
• Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680–685.
   PubMed Web of Science ®Google Scholar
• Lai, R. K., D. Perez-Sala, F. J. Canada, and R. R. Rando. 1990. The γ subunit of transducin is farnesylated. Proc. Natl. Acad. Sci. USA 87:7673–7677.
   PubMed Web of Science ®Google Scholar
• Mayer, M. L., B. E. Caplin, and M. S. Marshall. 1992. CDC43 and RAM2 encode the polypeptide subunits of yeast type I protein geranylgeranyltransferase. J. Biol. Chem. 267:20589–20593.
   PubMedGoogle Scholar
• Moores, S. L., M. D. Schaber, S. D. Mosser, E. Rands, M. B. O’Hara, V. M. Garsky, M. S. Marshall, D. L. Pompliano, and J. B. Gibbs. 1991. Sequence dependence of protein isoprenylation. J. Biol. Chem. 266:14603–14610.
   PubMed Web of Science ®Google Scholar
• Morehead, T. A., B. J. Biermann, D. N. Crowell, and S. K. Randall. 1995. Changes in protein isoprenylation during growth of suspension-cultured tobacco cells. Plant Physiol. 109:277–284.
   PubMed Web of Science ®Google Scholar
• Narita, J. Unpublished data.
   Google Scholar
• Omer, C. A., and J. B. Gibbs. 1994. Protein prenylation in eukaryotic microorganisms: genetics, biology and biochemistry. Mol. Microbiol. 11:219–225.
   PubMed Web of Science ®Google Scholar
• O’Reilly, D. R., L. K. Miller, and V. A. Luckow. 1992. Baculovirus expression vectors. A laboratory manual. W. H. Freeman and Company, New York, N.Y.
   Google Scholar
• Otto, J. C., and P. J. Casey. 1996. The hepatitis delta virus large antigen is farnesylated both in vitro and in animal cells. J. Biol. Chem. 271:4569–4572.
   PubMed Web of Science ®Google Scholar
• Pompliano, D. L., M. D. Schaber, S. D. Mosser, C. A. Omer, J. A. Shafer, and J. B. Gibbs. 1993. Isoprenoid diphosphate utilization by recombinant human farnesyl:protein transferase: interactive binding between substrates and a preferred kinetic pathway. Biochemistry 32:8341–8347.
   PubMed Web of Science ®Google Scholar
• Randall, S. K., M. S. Marshall, and D. N. Crowell. 1993. Protein isoprenylation in suspension-cultured tobacco cells. Plant Cell 5:433–442.
   PubMed Web of Science ®Google Scholar
• Reiss, Y., M. S. Brown, and J. L. Goldstein. 1992. Divalent cation and prenyl pyrophosphate specificities of the protein farnesyltransferase from rat brain, a zinc metalloenzyme. J. Biol. Chem. 267:6403–6408.
   PubMedGoogle Scholar
• Reiss, Y., J. L. Goldstein, M. C. Seabra, P. J. Casey, and M. S. Brown. 1990. Inhibition of purified p21 ras farnesyl transferase by Cys-AAX tetrapeptides. Cell 62:81–88.
   PubMed Web of Science ®Google Scholar
• Reiss, Y., M. C. Seabra, S. A. Armstrong, S. A. Slaughter, J. L. Goldstein, and M. S. Brown. 1991. Nonidentical subunits of p21H-ras farnesyltransferase. J. Biol. Chem. 266:10672–10677.
   PubMedGoogle Scholar
• Reiss, Y., S. J. Stradley, L. M. Gierach, M. S. Brown, and J. L. Goldstein. 1991. Sequence requirement for peptide recognition by rat brain p21ras protein farnesyltransferase. Proc. Natl. Acad. Sci. USA 88:732–736.
   PubMed Web of Science ®Google Scholar
• Sakagami, Y., M. Yoshida, A. Isogai, and A. Suzuki. 1981. Peptidal sex hormones inducing conjugation tube formation in compatible mating-type cells of Tremella mesenterica. Science 212:1525–1527.
   PubMed Web of Science ®Google Scholar
• Schafer, W. R., and J. Rine. 1992. Protein prenylation: genes, enzymes, targets and functions. Annu. Rev. Genet. 30:209–237.
   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
• Schena, M., D. Picard, and K. R. Yamamoto. 1991. Vectors for constitutive and inducible gene expression in yeast. Methods Enzymol. 194:389–398.
   PubMedGoogle Scholar
• Schmitt, D., K. Callan, S.-H. Kim, and W. Gruissem. 1996. Molecular and biochemical characterization of tomato farnesyl-protein transferase. Plant Physiol. 112:767–777.
   PubMedGoogle Scholar
• Seabra, M. C., Y. Reiss, P. Casey, M. S. Brown, and J. L. Goldstein. 1991. Protein farnesyltransferase and geranylgeranyltransferase share a common a subunit. Cell 65:429–434.
   PubMed Web of Science ®Google Scholar
• Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19–27.
   PubMed Web of Science ®Google Scholar
• Stotz, A., and P. Linder. 1990. The ADE2 gene from Saccharomyces cerevisiae: sequence and new vectors. Gene 95:91–98.
   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
• Wolda, S. L., and J. A. Glomset. 1988. Evidence for modification of lamin B by a product of mevalonic acid. J. Biol. Chem. 263:5997–6000.
   PubMed Web of Science ®Google Scholar
• Yang, Z., C. L. Cramer, and J. C. Watson. 1993. Protein farnesyltransferase in plants. Molecular cloning and expression of a homolog of the beta subunit from the garden pea. Plant Physiol. 101:667–674.
   PubMedGoogle Scholar
• Yasuda, H., M. A. Lindorfer, K. A. Woodfork, J. E. Fletcher, and J. C. Garrison. 1996. Role of the prenyl group on the G protein g subunit in coupling trimeric G proteins to A1 adenosine receptors. J. Biol. Chem. 271:18588–18595.
   PubMed Web of Science ®Google Scholar
• Ying, W., L. Sepp-Lorenzino, K. Cai, P. Aloise, and P. Coleman. 1994. Photoaffinity-labeling peptide substrates for farnesyl-protein transferase and the intersubunit location of the active site. J. Biol. Chem. 269:470–477.
   PubMedGoogle Scholar
• Zhu, J.-K., R. A. Bressan, and P. M. Hasegawa. 1993. Isoprenylation of the plant molecular chaperone ANJ1 facilitates membrane association and function at high temperature. Proc. Natl. Acad. Sci. USA 90:8557–8561.
   PubMedGoogle Scholar