Expression of yeast lipid phosphatase Sac1p is regulated by phosphatidylinositol-4-phosphate
Tóm tắt
Phosphoinositides play a central role in regulating processes at intracellular membranes. In yeast, a large number of phospholipid biosynthetic enzymes use a common mechanism for transcriptional regulation. Yet, how the expression of genes encoding lipid kinases and phosphatases is regulated remains unknown. Here we show that the expression of lipid phosphatase Sac1p in the yeast Saccharomyces cerevisiae is regulated in response to changes in phosphatidylinositol-4-phosphate (PI(4)P) concentrations. Unlike genes encoding enzymes involved in phospholipid biosynthesis, expression of the SAC1 gene is independent of inositol levels. We identified a novel 9-bp motif within the 5' untranslated region (5'-UTR) of SAC1 that is responsible for PI(4)P-mediated regulation. Upregulation of SAC1 promoter activity correlates with elevated levels of Sac1 protein levels. Regulation of Sac1p expression via the concentration of its major substrate PI(4)P ensures proper maintenance of compartment-specific pools of PI(4)P.
Tài liệu tham khảo
Di Paolo G, De Camilli P: Phosphoinositides in cell regulation and membrane dynamics. Nature 2006, 443: 651-7. 10.1038/nature05185.
Behnia R, Munro S: Organelle identity and the signposts for membrane traffic. Nature 2005, 438: 597-604. 10.1038/nature04397.
De Matteis MA, Di Campli A, Godi A: The role of the phosphoinositides at the Golgi complex. Biochim Biophys Acta 2005, 1744: 396-405. 10.1016/j.bbamcr.2005.04.013.
Pendaries C, Tronchere H, Plantavid M, Payrastre B: Phosphoinositide signaling disorders in human diseases. FEBS Lett 2003, 546: 25-31. 10.1016/S0014-5793(03)00437-X.
Carman GM, Henry SA: Phospholipid biosynthesis in the yeast Saccharomyces cerevisiae and interrelationship with other metabolic processes. Prog Lipid Res 1999, 38: 361-99. 10.1016/S0163-7827(99)00010-7.
Jesch SA, Zhao X, Wells MT, Henry SA: Genome-wide analysis reveals inositol, not choline, as the major effector of Ino2p-Ino4p and unfolded protein response target gene expression in yeast. J Biol Chem 2005, 280: 9106-18. 10.1074/jbc.M411770200.
Loewen CJ, Gaspar ML, Jesch SA, Delon C, Ktistakis NT, Henry SA, Levine TP: Phospholipid metabolism regulated by a transcription factor sensing phosphatidic acid. Science 2004, 304: 1644-7. 10.1126/science.1096083.
Tahirovic S, Schorr M, Mayinger P: Regulation of intracellular phosphatidylinositol-4-phosphate by the Sac1 lipid phosphatase. Traffic 2005, 6: 116-30. 10.1111/j.1600-0854.2004.00255.x.
Roy A, Levine TP: Multiple pools of phosphatidylinositol 4-phosphate detected using the pleckstrin homology domain of Osh2p. J Biol Chem 2004, 279: 44683-9. 10.1074/jbc.M401583200.
Foti M, Audhya A, Emr SD: Sac1 lipid phosphatase and stt4 phosphatidylinositol 4-kinase regulate a pool of phosphatidylinositol 4-phosphate that functions in the control of the actin cytoskeleton and vacuole morphology. Mol Biol Cell 2001, 12: 2396-411.
Faulhammer F, Konrad G, Brankatschk B, Tahirovic S, Knodler A, Mayinger P: Cell growth-dependent coordination of lipid signaling and glycosylation is mediated by interactions between Sac1p and Dpm1p. J Cell Biol 2005, 168: 185-91. 10.1083/jcb.200407118.
Zhu J, Zhang MQ: SCPD: a promoter database of the yeast Saccharomyces cerevisiae. Bioinformatics 1999, 15: 607-11. 10.1093/bioinformatics/15.7.607.
Hughes WE, Pocklington MJ, Orr E, Paddon CJ: Mutations in the Saccharomyces cerevisiae gene SAC1 cause multiple drug sensitivity. Yeast 1999, 15: 1111-24. 10.1002/(SICI)1097-0061(199908)15:11<1111::AID-YEA440>3.0.CO;2-H.
Cleves AE, Novick PJ, Bankaitis VA: Mutations in the SAC1 gene suppress defects in yeast Golgi and yeast actin function. J Cell Biol 1989, 109: 2939-2950. 10.1083/jcb.109.6.2939.
Kochendorfer KU, Then AR, Kearns BG, Bankaitis VA, Mayinger P: Sac1p plays a crucial role in microsomal ATP transport, which is distinct from its function in Golgi phospholipid metabolism. Embo J 1999, 18: 1506-15. 10.1093/emboj/18.6.1506.
Tahirovic S, Schorr M, Then A, Berger J, Schwarz H, Mayinger P: Role for lipid signaling and the cell integrity MAP kinase cascade in yeast septum biogenesis. Curr Genet 2003, 43: 71-8.
Whitters EA, Cleves AE, McGee TP, Skinner HB, Bankaitis VA: SAC1p is an integral membrane protein that influences the cellular requirement for phospholipid transfer protein function and inositol in yeast. J Cell Biol 1993, 122: 79-94. 10.1083/jcb.122.1.79.
Bachhawat N, Ouyang Q, Henry SA: Functional characterization of an inositol-sensitive upstream activation sequence in yeast. A cis-regulatory element responsible for inositol-choline mediated regulation of phospholipid biosynthesis. J Biol Chem 1995, 270: 25087-95. 10.1074/jbc.270.42.25087.
Greenberg ML, Reiner B, Henry SA: Regulatory mutations of inositol biosynthesis in yeast: isolation of inositol-excreting mutants. Genetics 1982, 100: 19-33.
Ashburner BP, Lopes JM: Regulation of yeast phospholipid biosynthetic gene expression in response to inositol involves two superimposed mechanisms. Proc Natl Acad Sci USA 1995, 92: 9722-6. 10.1073/pnas.92.21.9722.
Kohno O, Normington K, Sambrook J, Gething MJ, Mori K: The promoter region of the yeast KAR2 (BiP) gene contains a regulatory domain that responds to the presence of unfolded proteins in the endoplasmic reticulum. Mol Cell Biol 1993, 13: 877-890.
Guo S, Stolz LE, Lemrow SM, York JD: SAC1-like domains of yeast SAC1, INP52, and INP53 and of human synaptojanin encode polyphosphoinositide phosphatases. J Biol Chem 1999, 274: 12990-5. 10.1074/jbc.274.19.12990.
Audhya A, Foti M, Emr SD: Distinct roles for the yeast phosphatidylinositol 4-kinases, Stt4p and Pik1p, in secretion, cell growth, and organelle membrane dynamics. Mol Biol Cell 2000, 11: 2673-89.
Konrad G, Schlecker T, Faulhammer F, Mayinger P: Retention of the yeast Sac1p phosphatase in the endoplasmic reticulum causes distinct changes in cellular phosphoinositide levels and stimulates microsomal ATP transport. J Biol Chem 2002, 277: 10547-54. 10.1074/jbc.M200090200.
Faulhammer F, S Kanjilal-Kolar, Knodler A, Lo J, Lee Y, Konrad G, Mayinger P: Growth Control of Golgi Phosphoinositides by Reciprocal Localization of Sac1 Lipid Phosphatase and Pik1 4-Kinase. Traffic 2007.
Mori K, Ogawa N, Kawahara T, Yanagi H, Yura T: Palindrome with spacer of one nucleotide is characteristic of the cis-acting unfolded protein response element in Saccharomyces cerevisiae. J Biol Chem 1998, 273: 9912-20. 10.1074/jbc.273.16.9912.
Bunce MW, Bergendahl K, Anderson RA: Nuclear PI(4,5)P(2): a new place for an old signal. Biochim Biophys Acta 2006, 1761: 560-9.
Deleris P, Gayral S, Breton-Douillon M: Nuclear Ptdlns(3,4,5)P3 signaling: an ongoing story. J Cell Biochem 2006, 98: 469-85. 10.1002/jcb.20695.
Homma K, Terui S, Minemura M, Qadota H, Anraku Y, Kanaho Y, Ohya Y: Phosphatidylinositol-4-phosphate 5-kinase localized on the plasma membrane is essential for yeast cell morphogenesis. J Biol Chem 1998, 273: 15779-86. 10.1074/jbc.273.25.15779.
Desrivieres S, Cooke FT, Parker PJ, Hall MN: MSS4, a phosphatidylinositol-4-phosphate 5-kinase required for organization of the actin cytoskeleton in Saccharomyces cerevisiae. J Biol Chem 1998, 273: 15787-93. 10.1074/jbc.273.25.15787.
Flick JS, Thorner J: Genetic and biochemical characterization of a phosphatidylinositol-specific phospholipase C in Saccharomyces cerevisiae. Mol Cell Biol 1993, 13: 5861-76.
York JD, Odom AR, Murphy R, Ives EB, Wente SR: A phospholipase C-dependent inositol polyphosphate kinase pathway required for efficient messenger RNA export. Science 1999, 285: 96-100. 10.1126/science.285.5424.96.
Odom AR, Stahlberg A, Wente SR, York JD: A role for nuclear inositol 1,4,5-trisphosphate kinase in transcriptional control. Science 2000, 287: 2026-9. 10.1126/science.287.5460.2026.
Sikorski RS, Hieter P: A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 1989, 122: 19-27.
Harlow E, Lane D: Antibodies: A laboratory manual. Cold Spring Harbor Laboratory; 1988.
Schorr M, Then A, Tahirovic S, Hug N, Mayinger P: The phosphoinositide phosphatase Sac1p controls trafficking of the yeast Chs3p chitin synthase. Curr Biol 2001, 11: 1421-6. 10.1016/S0960-9822(01)00449-3.