Genetic and Biochemical Characterization of a Phosphatidylinositol-Specific Phospholipase C in Saccharomyces cerevisiae

REFERENCES

• Bairoch, A., and J. A. Cox. 1990. EF-hand motifs in inositol phospholipid-specific phospholipase C. FEBS Lett. 269:454–456.
   PubMedGoogle Scholar
• Benton, B. Unpublished results.
   Google Scholar
• Berridge, Μ. J. 1993. Inositol trisphosphate and calcium signalling. Nature (London) 361:315–325.
   PubMed Web of Science ®Google Scholar
• Bloomquist, B. T., R. D. Shortridge, S. Schneuwly, Μ. Perdew, C. Montrell, H. Steller, G. Rubin, and W. L. Pak. 1988. Isolation of a putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction. Cell 54:723–733.
   PubMed Web of Science ®Google Scholar
• Brewster, J. L., T. de Valoir, N. D. Dwyer, E. Winter, and Μ. C. Gustin. 1993. An osmosensing signal transduction pathway in yeast. Science 259:1760–1763.
   PubMed Web of Science ®Google Scholar
• Buchman, A. R., W. J. Kimmerly, J. Rine, and R. D. Kornberg. 1988. Two DNA-binding factors recognize specific sequences at silencers, upstream activating sequences, autonomously replicating sequences, and telomers in Saccharomyces cerevisiae. Mol. Cell. Biol. 8:210–224.
   PubMed Web of Science ®Google Scholar
• Chen, E., and K. Struhl. 1988. Saturation mutagenesis of a yeast HIS3 “TATA element”: genetic evidence for a specific TATA- binding protein. Proc. Natl. Acad. Sci. USA 85:2691–2695.
   PubMed Web of Science ®Google Scholar
• Chen, E. Y., and P. H. Seeburg. 1985. Supercoil sequencing: a fast and simple method for sequencing plasmid DNA. DNA 4:165–170.
   PubMedGoogle Scholar
• Chu, G., D. Vollrath, and R. W. Davis. 1986. Separation of large DNA molecules by contour-clamped homogeneous electric fields. Science 234:1582–1585.
   PubMed Web of Science ®Google Scholar
• Cyert, Μ. S., R. Kunisawa, D. Kaim, and J. Thorner. 1991. Yeast has homologs (CNA1 and CNA2 gene products) of mammalian calcineurin, a calmodulin-regulated phosphoprotein phosphatase. Proc. Natl. Acad. Sci. USA 88:7376–7380.
   PubMedGoogle Scholar
• Cyert, Μ. S., and J. Thorner. 1992. Regulatory subunit (CNB1 gene product) of yeast Ca2+∕calmodulin-dependent phosphoprotein phosphatases is required for adaptation to pheromone. Mol. Cell. Biol. 12:3460–3469.
   PubMedGoogle Scholar
• Davis, T. N., Μ. S. Urdea, F. R. Masiarz, and J. Thorner. 1986. Isolation of the yeast calmodulin gene: calmodulin is an essential protein. Cell 47:423–431.
   PubMed Web of Science ®Google Scholar
• Eider, R. T., E. Y. Loh, and R. W. Davis. 1983. RNA from the yeast transposable element Tyl has both ends in the direct repeats, a structure similar to retrovirus RNA. Proc. Natl. Acad. Sci. USA 80:2432–2436.
   PubMedGoogle Scholar
• Emori, Y., Y. Homma, H. Sorimachi, H. Kawasaki, O. Nakanishi, K. Suzuki, and T. Takenawa. 1989. A second type of rat phosphoinositide-specific phospholipase C containing a src- related sequence not essential for phosphoinositide-hydrolyzing activity. J. Biol. Chem. 264:21885–21890.
   PubMedGoogle Scholar
• Evan, G. L, G. K. Lewis, G. Ramsay, and J. Μ. Bishop. 1985. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5:3610–3616.
   PubMed Web of Science ®Google Scholar
• Feinberg, A. P, and B. Vogelstein. 1983. A technique for radiolabeling DNA restriction fragments to high specific activity. Anal. Biochem. 132:266–270.
   Google Scholar
• Flanagan, C. A., and J. Thorner. 1992. Purification and characterization of a soluble phosphatidylinositol 4-kinase from the yeast Saccharomyces cerevisiae. J. Biol. Chem. 267:24117–24125.
   PubMedGoogle Scholar
• Flick, J. S∙, and Μ. Johnston. 1990. Two systems of glucose repression of the GAL1 promoter in Saccharomyces cerevisiae. Mol. Cell. Biol. 10:4757–4769.
   PubMedGoogle Scholar
• Flick, J. S., and M∙ Johnston. 1991. GRRl of Saccharomyces cerevisiae is required for glucose repression and encodes a protein with leucine-rich repeats. Mol. Cell. Biol. 11:5101–5112.
   PubMed Web of Science ®Google Scholar
• Gieselmann, R., and K. Mann. 1992. ASP-56, a new actin- Sequestering protein from pig platelets with homology to CAP, adenylate cyclase-associated protein from yeast. FEBS Lett. 298:149–153.
   PubMedGoogle Scholar
• Gietz, R. D., and R. H. Schiestl. 1991. Applications of high efficiency lithium acetate transformations of intact yeast cells using single-stranded nucleic acids as carrier. Yeast 7:253–263.
   PubMed Web of Science ®Google Scholar
• Goldschidt-Clermont, P. J., J. W. Kim, L. Μ. Machesky, S. G. Rhee, and T. D. Pollard. 1991. Regulation of phospholipase C-γl by profilin and tyrosine phosphorylation. Science 251:1231–1233.
   PubMedGoogle Scholar
• Griggs, D. W., and Μ. Johnston. 1991. Regulated expression of the GAL4 activator gene in yeast provides a sensitive genetic switch for glucose repression. Proc. Natl. Acad. Sci. USA 88:8597–8601.
   PubMedGoogle Scholar
• Harlow, E∙, and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Hawldns, P. T., L. R. Stephens, and J. R. Piggot. 1993. Analysis of inositol metabolites produced by Saccharomyces cerevisiae in response to glucose stimulation. J. Biol. Chem. 268:3374–3383.
   PubMedGoogle Scholar
• Henikoff, S. 1984. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28:351–359.
   PubMed Web of Science ®Google Scholar
• Hill, J. E., A. Μ. Myers, T. J. Koerner, and A. Tzagoloff. 1986. Yeast/E. coli shuttle vectors with multiple unique restriction sites. Yeast 2:163–167.
   PubMed Web of Science ®Google Scholar
• Hofmann, S. L., and P. W. Majerus. 1982. Identification and properties of two distinct phosphatidylinositol-specific phospholipase C enzymes from sheep seminal vesicular glands. J. Biol. Chem. 257:6461–6469.
   PubMedGoogle Scholar
• Iida, H., Y. Yagawa, and Y. Anraku. 1990. Essential role for induced Ca2+ influx followed by [Ca2+]i rise in maintaining viability of yeast cells late in the mating pheromone response pathway. A study of [Ca2+]i in single Saccharomyces cerevisiae cells with imaging of Fura-2. J. Biol. Chem. 265:13391–13399.
   PubMedGoogle Scholar
• Janknecht, R., G. de Martynoff, J. Lou, R. A. Hipskind, A. Nordheim, and H. G. Stunnenberg. 1991. Rapid and efficient purification of native histidine-tagged protein expressed by recombinant vaccinia virus. Proc. Natl. Acad. Sci. USA 88:8972–8976.
   PubMedGoogle Scholar
• Johnston, M., and R. W. Davis. 1984. Sequences that regulate the divergent GAL1-10 promoter in Saccharomyces cerevisiae. Mol. Cell. Biol. 4:1440–1448.
   PubMed Web of Science ®Google Scholar
• Jones, E. W. 1991. Tackling the protease problem in Saccharomyces cerevisiae. Methods Enzymol. 194:428–453.
   PubMed Web of Science ®Google Scholar
• Jones, J. S., and L. Prakash. 1990. Yeast Saccharomyces cerevisiae selectable markers in pUC18 polylinkers. Yeast 6:363–366.
   PubMedGoogle Scholar
• Kaibuchi, K., A. Miyqjima, K.-I. Aria, and K. Matsumoto. 1986. Possible involvement of Λ4S-encoded proteins in glucose- induced inositolphospholipid turnover in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 83:8172–8176.
   PubMed Web of Science ®Google Scholar
• Katan, M., R. W. Kriz, N. Totty, R. PhHp, E. Meldrum, R. A. Aldape, J. L. Knopf, and P. J. Parker. 1988. Determination of the primary structure of PLC-154 demonstrates diversity of phosphoinositide-specific phospholipase C activities. Cell 54:171–177.
   PubMedGoogle Scholar
• Koch, C. A., D. Anderson, Μ. F. Moran, C. Ellis, and T. Pawson. 1991. SH2 and SH3 domains: elements that control interactions of cytoplasmic signalling proteins. Science 252:668–674.
   PubMed Web of Science ®Google Scholar
• Kriz, Re, L. L. Linn, L. Sultzmann, C. ElHs, C. H. Heldin, T. Pawson, and J. Knopf. 1990. Phospholipase C isozymes: structural and functional similarities. CIBA Found. Symp. 150:112–123.
   PubMedGoogle Scholar
• Laemmh, 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
• Lester, R. L., and Μ. R. Steiner. 1968. The occurrence of diphosphoinositide and triphosphoinositide in Saccharomyces cerevisiae. J. Biol. Chem. 243:4889–4893.
   PubMedGoogle Scholar
• Levin, D. E., and E. Barlett-Heubusch. 1992. Mutants in the S. cerevisiae PKCl gene display a cell cycle-specific osmotic stability defect. J. Cell Biol. 116:1221–1229.
   PubMed Web of Science ®Google Scholar
• Levin, D. E., and B. Errede. 1993. A multitude of MAP kinase activation pathways. J. NIH Res. 5:49–52.
   Google Scholar
• Levin, D. E., F. O. Flelds, R. Kunisawa, J. Μ. Bishop, and J. Thorner. 1990. A candidate protein kinase C gene, PKCl, is required for the S. cerevisiae cell cycle. Cell 62:213–224.
   PubMed Web of Science ®Google Scholar
• Meldrum, E., Μ. Katan, and P. Parker. 1989. A novel inositolphospholipid-specific phospholipase C. Eur. J. Biochem. 182:673–677.
   PubMedGoogle Scholar
• Meldrum, E., R. W. Kriz, N. Totty, and P. J. Parker. 1991. A second gene product of the inositol-phospholipid-specific phospholipase C δ subclass. Eur. J. Biochem. 196:159–165.
   PubMedGoogle Scholar
• Mohammadi, M., C. A. Dionne, W. Li, N. Li, T. Spivak, A. Μ. Honegger, Μ. Jaye, and J. Schlessinger. 1992. Point mutation in FGF receptor eliminates phosphatidylinositol hydrolysis without affecting mitogenesis. Nature (London) 358:681–684.
   PubMed Web of Science ®Google Scholar
• Nishizuka, Y. 1992. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 258:607–614.
   PubMed Web of Science ®Google Scholar
• Olson, Μ. V., J. E. Dutchick, G. Μ. Graham, C. Helms, Μ. Franc, Μ. MacCoHin, R. Seheiman, and R. Frank. 1986. Random-clone strategy for geomic restriction mapping in yeast. Proc. Natl. Acad. Sci. USA 85:7826–7830.
   Google Scholar
• Park, D., D.-Y. Jhon, R. Kriz, J. Knopf, and S. G. Rhee. 1992. Cloning, sequencing, expression, and Gq-independent activation of phospholipase C-β2. J. Biol. Chem. 267:16048–16055.
   PubMed Web of Science ®Google Scholar
• Pausch, Μ., D. Kaim, R. Kunisawa, A. Admon, and J. Thorner. 1991. Multiple Ca2+∕calmodulin-dependent protein kinase genes in a unicellular eukaryote. EMBO 10:1511–1522.
   PubMed Web of Science ®Google Scholar
• Payne, W. E., and Μ. Fitzgerald-Hayes. 1993. A mutation in PLCl, a candidate phosphoinositide-specific phospholipase C gene from Saccharomyces cerevisiae, causes aberrant mitotic chromosome segregation. Mol. Cell. Biol. 13:4351–4364.
   PubMedGoogle Scholar
• Pearson, W. R∙, and D. J. Lipman. 1988. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA 85:2444–2448.
   PubMed Web of Science ®Google Scholar
• Peters, K. G., J. Marie, E. Wilson, H. E. Ives, J. Escobedo, Μ. Del Rosario, D. Mirda, and L. T. Williams. 1992. Point mutations of an FGF receptor abolishes phosphatidylinositol turnover and Ca2+ flux but not mitogenesis. Nature (London) 358:678–681.
   PubMed Web of Science ®Google Scholar
• Pringle, J. R., A. E. Μ Adams, D. G. Drubin, and B. K. Haarer. 1991. Immunofluorescence methods for yeast. Methods Enzymol. 194:565–602.
   PubMedGoogle Scholar
• Rhee, S. G., and K. D. Choi. 1992. Multiple forms of phospholipase C isozymes and their activation mechanisms. Adv. Second Messenger Phosphoprotein Res. 26:35–61.
   PubMedGoogle Scholar
• Riles, L. (Department of Genetics, Washington University School of Medicine). Personal communication.
   Google Scholar
• Rogers, S., R. Wells, and M∙ Rechsteiner. 1986. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 234:364–368.
   PubMed Web of Science ®Google Scholar
• Rose, Μ. D., P. Novick, J. H. Thomas, D. Botstein, and G. R. Fink. 1987. A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene 60:237–243.
   PubMed Web of Science ®Google Scholar
• Rose, Μ. D., F. Winston, and P. Hieter. 1990. Methods in yeast genetics: a laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Rothstein, R. J. 1983. One-step gene disruption in yeast. Methods Enzymol. 101:202–211.
   PubMed Web of Science ®Google Scholar
• Ryu, S. H., K. S. Cho, K.-Y. Lee, P.-G. Suh, and S. G. Rhee. 1987. Purification and characterization of two immunologically distinct phosphoinositide-specific phospholipases C from bovine brain. J. Biol. Chem. 262:12511–12518.
   PubMed Web of Science ®Google Scholar
• Ryu, S. H., P.-G. Suh, K. S. Cho, K.-Y. Lee, and S. G. Rhee. 1987. Bovine brain cytosol contains three immunologically distinct forms of inositolphospholipid-specific phospholipase C. Proc. Natl. Acad. Sci. USA 84:6649–6653.
   PubMedGoogle Scholar
• Saiki, R. K., D. H. Gelfand, S. Stoffel, S. J. Scharf, R. Higuchi, G. T. Horn, K. B. MuHis, and H. A. Erlich. 1988. Primer- directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487–491.
   PubMed Web of Science ®Google Scholar
• Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Sehatzmann, H. J. 1973. Dependence on calcium concentration and stoichiometry of the calcium pump in human red cells. J. Physiol. 235:551–569.
   PubMedGoogle Scholar
• Schomerus, C., and H. Kuntzel. 1992. CDC25-dependent induction of inositol 1,4,5-trisphosphate and diacylglycerol in Sac- chromyces cerevisiae by nitrogen. FEBS Lett. 307:249–252.
   PubMed Web of Science ®Google Scholar
• Sikorski, R. S., and P. Heiter. 1989. A system of shuttle vectors and yeast host strains designated for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19–27.
   PubMed Web of Science ®Google Scholar
• Slater, Μ. R., and E. A. Craig. 1987. Transcriptional regulation of an hsp70 heat shock gene in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 7:1906–1916.
   PubMedGoogle Scholar
• Stahl, Μ. L., C. R. Ferenz, K. L. Kelleher, R. W. Kriz, and J. L. Knopf. 1988. Sequence similarity of phospholipase C with the non-catalytic region of src. Nature (London) 331:269–272.
   PubMedGoogle Scholar
• Suh, P.-G., S. H. Ryu, K.-H. Moon, H. W. Suh, and S. G. Rhee. 1988. Inositol phospholipid-specific phospholipase C: complete cDNA and protein sequences and sequence homology to tyrosine kinase-related oncogene products. Proc. Natl. Acad. Sci. USA 85:5419–5423.
   PubMed Web of Science ®Google Scholar
• Suh, P.-G., S. H. Ryu, K. H. Moon, H. W. Suh, and S. G. Rhee. 1988. Cloning and sequence of multiple forms of phospholipase C. Cell 54:161–169.
   PubMed Web of Science ®Google Scholar
• Thomas, B. J∙, and R. J. Rothstein. 1989. Elevated recombination rates in transcriptionally active DNA. Cell 56:619–630.
   PubMed Web of Science ®Google Scholar
• Vojtek, A., B. Haarer, J. Field, J. Gerst, T. D. Pollard, S. Brown, and Μ. Wigler. 1991. Evidence for a functional link between profilin and CAP in the yeast S. cerevisiae. Cell 66:497–505.
   PubMedGoogle Scholar
• Wilson, D. B∙, T. E. Bross, S. L. Hoftnann, and P. W. Majerus. 1984. Hydrolysis of polyphosphoinositides by purified sheep seminal vesicle phospholipase C enzymes. J. Biol. Chem. 259:11718–11724.
   PubMed Web of Science ®Google Scholar
• Wu, D., H. Jiang, A. Katz, and Μ. I. Simon. 1993. Identification of critical regions on phospholipase C-βl required for activation by G-proteins. J. Biol. Chem. 268:3704–3709.
   PubMed Web of Science ®Google Scholar
• Yoko-O, T., Y. Matsui, H. Yagisawa, H. Nojima, I. Uno, and A. Toh-e. 1993. The putative phosphoinositide-specific phospholipase C gene, PLCl, of the yeast Saccharomyces cerevisiae is important for cell growth. Proc. Natl. Acad. Sci. USA 90:1804–1808.
   PubMed Web of Science ®Google Scholar