Abstract
Phospholipid metabolism plays an important role in cellular regulation by generating second messengers for signal transduction. Many stimuli activate a phospholipase D, which catalyzes the hydrolysis of phosphatidylcholine, producing phosphatidic acid and choline. Here we report that the yeast SP014 gene, which is essential for meiosis [Honigberg, S. M., Conicella, C. & Esposito, R. E. (1992) Genetics 130, 703-716], encodes a phospholipase D. SP014 RNA and protein activity are induced during late meiotic prophase, and the enzyme has properties similar to mammalian phosphatidylinositol 4,5-bisphosphate-regulated phospholipase D. Characterization of an unusual allele of SP014 defines regions of the protein important for enzyme catalysis and regulation. These results implicate phospholipase D signaling in regulating cellular differentiation.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Boman A. L., Kahn R. A. Arf proteins: the membrane traffic police? Trends Biochem Sci. 1995 Apr;20(4):147–150. doi: 10.1016/s0968-0004(00)88991-4. [DOI] [PubMed] [Google Scholar]
- Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
- Brill S. J., Sternglanz R. Transcription-dependent DNA supercoiling in yeast DNA topoisomerase mutants. Cell. 1988 Jul 29;54(3):403–411. doi: 10.1016/0092-8674(88)90203-6. [DOI] [PubMed] [Google Scholar]
- Brown H. A., Gutowski S., Moomaw C. R., Slaughter C., Sternweis P. C. ADP-ribosylation factor, a small GTP-dependent regulatory protein, stimulates phospholipase D activity. Cell. 1993 Dec 17;75(6):1137–1144. doi: 10.1016/0092-8674(93)90323-i. [DOI] [PubMed] [Google Scholar]
- Clarke L., Carbon J. Isolation of a yeast centromere and construction of functional small circular chromosomes. Nature. 1980 Oct 9;287(5782):504–509. doi: 10.1038/287504a0. [DOI] [PubMed] [Google Scholar]
- Divecha N., Irvine R. F. Phospholipid signaling. Cell. 1995 Jan 27;80(2):269–278. doi: 10.1016/0092-8674(95)90409-3. [DOI] [PubMed] [Google Scholar]
- Dujon B., Alexandraki D., André B., Ansorge W., Baladron V., Ballesta J. P., Banrevi A., Bolle P. A., Bolotin-Fukuhara M., Bossier P. Complete DNA sequence of yeast chromosome XI. Nature. 1994 Jun 2;369(6479):371–378. doi: 10.1038/369371a0. [DOI] [PubMed] [Google Scholar]
- Ella K. M., Dolan J. W., Meier K. E. Characterization of a regulated form of phospholipase D in the yeast Saccharomyces cerevisiae. Biochem J. 1995 May 1;307(Pt 3):799–805. doi: 10.1042/bj3070799. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Elledge S. J., Davis R. W. A family of versatile centromeric vectors designed for use in the sectoring-shuffle mutagenesis assay in Saccharomyces cerevisiae. Gene. 1988 Oct 30;70(2):303–312. doi: 10.1016/0378-1119(88)90202-8. [DOI] [PubMed] [Google Scholar]
- Engebrecht J., Roeder G. S. Yeast mer1 mutants display reduced levels of meiotic recombination. Genetics. 1989 Feb;121(2):237–247. doi: 10.1093/genetics/121.2.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Exton J. H. Phosphatidylcholine breakdown and signal transduction. Biochim Biophys Acta. 1994 Apr 14;1212(1):26–42. doi: 10.1016/0005-2760(94)90186-4. [DOI] [PubMed] [Google Scholar]
- Friesen H., Lunz R., Doyle S., Segall J. Mutation of the SPS1-encoded protein kinase of Saccharomyces cerevisiae leads to defects in transcription and morphology during spore formation. Genes Dev. 1994 Sep 15;8(18):2162–2175. doi: 10.1101/gad.8.18.2162. [DOI] [PubMed] [Google Scholar]
- Hill J. E., Myers A. M., Koerner T. J., Tzagoloff A. Yeast/E. coli shuttle vectors with multiple unique restriction sites. Yeast. 1986 Sep;2(3):163–167. doi: 10.1002/yea.320020304. [DOI] [PubMed] [Google Scholar]
- Honigberg S. M., Conicella C., Espositio R. E. Commitment to meiosis in Saccharomyces cerevisiae: involvement of the SPO14 gene. Genetics. 1992 Apr;130(4):703–716. doi: 10.1093/genetics/130.4.703. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kobayashi M., Kanfer J. N. Phosphatidylethanol formation via transphosphatidylation by rat brain synaptosomal phospholipase D. J Neurochem. 1987 May;48(5):1597–1603. doi: 10.1111/j.1471-4159.1987.tb05707.x. [DOI] [PubMed] [Google Scholar]
- Krieg P. A., Melton D. A. In vitro RNA synthesis with SP6 RNA polymerase. Methods Enzymol. 1987;155:397–415. doi: 10.1016/0076-6879(87)55027-3. [DOI] [PubMed] [Google Scholar]
- Krisak L., Strich R., Winters R. S., Hall J. P., Mallory M. J., Kreitzer D., Tuan R. S., Winter E. SMK1, a developmentally regulated MAP kinase, is required for spore wall assembly in Saccharomyces cerevisiae. Genes Dev. 1994 Sep 15;8(18):2151–2161. doi: 10.1101/gad.8.18.2151. [DOI] [PubMed] [Google Scholar]
- Liscovitch M., Cantley L. C. Signal transduction and membrane traffic: the PITP/phosphoinositide connection. Cell. 1995 Jun 2;81(5):659–662. doi: 10.1016/0092-8674(95)90525-1. [DOI] [PubMed] [Google Scholar]
- Löw R., Rausch T. Sensitive, nonradioactive northern blots using alkaline transfer of total RNA and PCR-amplified biotinylated probes. Biotechniques. 1994 Dec;17(6):1026-8, 1030. [PubMed] [Google Scholar]
- Massenburg D., Han J. S., Liyanage M., Patton W. A., Rhee S. G., Moss J., Vaughan M. Activation of rat brain phospholipase D by ADP-ribosylation factors 1,5, and 6: separation of ADP-ribosylation factor-dependent and oleate-dependent enzymes. Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11718–11722. doi: 10.1073/pnas.91.24.11718. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mitchell A. P. Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiol Rev. 1994 Mar;58(1):56–70. doi: 10.1128/mr.58.1.56-70.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moolenaar W. H., Kruijer W., Tilly B. C., Verlaan I., Bierman A. J., de Laat S. W. Growth factor-like action of phosphatidic acid. Nature. 1986 Sep 11;323(6084):171–173. doi: 10.1038/323171a0. [DOI] [PubMed] [Google Scholar]
- Moolenaar W. H. Lysophosphatidic acid, a multifunctional phospholipid messenger. J Biol Chem. 1995 Jun 2;270(22):12949–12952. doi: 10.1074/jbc.270.22.12949. [DOI] [PubMed] [Google Scholar]
- Morris A. J., Rudge S. A., Mahlum C. E., Jenco J. M. Regulation of phosphoinositide-3-kinase by G protein beta gamma subunits in a rat osteosarcoma cell line. Mol Pharmacol. 1995 Sep;48(3):532–539. [PubMed] [Google Scholar]
- Murray A. W. Creative blocks: cell-cycle checkpoints and feedback controls. Nature. 1992 Oct 15;359(6396):599–604. doi: 10.1038/359599a0. [DOI] [PubMed] [Google Scholar]
- Nishizuka Y. Protein kinase C and lipid signaling for sustained cellular responses. FASEB J. 1995 Apr;9(7):484–496. [PubMed] [Google Scholar]
- Okamura S., Yamashita S. Purification and characterization of phosphatidylcholine phospholipase D from pig lung. J Biol Chem. 1994 Dec 9;269(49):31207–31213. [PubMed] [Google Scholar]
- Peltz S. W., He F., Welch E., Jacobson A. Nonsense-mediated mRNA decay in yeast. Prog Nucleic Acid Res Mol Biol. 1994;47:271–298. doi: 10.1016/s0079-6603(08)60254-8. [DOI] [PubMed] [Google Scholar]
- Rothstein R. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 1991;194:281–301. doi: 10.1016/0076-6879(91)94022-5. [DOI] [PubMed] [Google Scholar]
- Seifert H. S., Chen E. Y., So M., Heffron F. Shuttle mutagenesis: a method of transposon mutagenesis for Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1986 Feb;83(3):735–739. doi: 10.1073/pnas.83.3.735. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Simmonds A. C., Halsey M. J. General and local anaesthetics perturb the fusion of phospholipid vesicles. Biochim Biophys Acta. 1985 Mar 14;813(2):331–337. doi: 10.1016/0005-2736(85)90249-4. [DOI] [PubMed] [Google Scholar]
- Singer W. D., Brown H. A., Bokoch G. M., Sternweis P. C. Resolved phospholipase D activity is modulated by cytosolic factors other than Arf. J Biol Chem. 1995 Jun 23;270(25):14944–14950. doi: 10.1074/jbc.270.25.14944. [DOI] [PubMed] [Google Scholar]
- Wang X., Xu L., Zheng L. Cloning and expression of phosphatidylcholine-hydrolyzing phospholipase D from Ricinus communis L. J Biol Chem. 1994 Aug 12;269(32):20312–20317. [PubMed] [Google Scholar]
- Yu C. L., Tsai M. H., Stacey D. W. Cellular ras activity and phospholipid metabolism. Cell. 1988 Jan 15;52(1):63–71. doi: 10.1016/0092-8674(88)90531-4. [DOI] [PubMed] [Google Scholar]