DOI: 10.1091/mbc.12.8.2396. 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

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

10.1091/mbc.12.8.2396

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

Synthesis and turnover of phosphoinositides are tightly regulated processes mediated by a set of recently identified kinases and phosphatases. We analyzed the primary role of the phosphoinositide phosphatase Sac1p in Saccharomyces cerevisiae with the use of a temperature-sensitive allele of this gene. Our analysis demonstrates that inactivation of Sac1p leads to a specific increase in the cellular levels of phosphatidylinositol 4-phosphate (PtdIns(4)P), accompanied by changes in vacuole morphology and an accumulation of lipid droplets. We have found that the majority of Sac1p localizes to the endoplasmic reticulum, and this localization is crucial for the efficient turnover of PtdIns(4)P. By generating double mutant strains harboring the sac1tsallele and one of two temperature-sensitive PtdIns 4-kinase genes,stt4tsor pik1ts, we have demonstrated that the bulk of PtdIns(4)P that accumulates insac1 mutant cells is generated by the Stt4 PtdIns 4-kinase, and not Pik1p. Consistent with these findings, inactivation of Sac1p partially rescued defects associated withstt4tsbut notpik1tsmutant cells. To analyze potential overlapping functions between Sac1p and other homologous phosphoinositide phosphatases, sac1tsmutant cells lacking various other synaptojanin-like phosphatases were generated. These double and triple mutants exacerbated the accumulation of intracellular phosphoinositides and caused defects in Golgi function. Together, our results demonstrate that Sac1p primarily turns over Stt4p-generated PtdIns(4)P and that the membrane localization of Sac1p is important for its function in vivo. Regulation of this PtdIns(4)P pool appears to be crucial for the maintenance of vacuole morphology, regulation of lipid storage, Golgi function, and actin cytoskeleton organization.

Bibliography

Foti, M., Audhya, A., & Emr, S. D. (2001). 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. Molecular Biology of the Cell, 12(8), 2396â2411.

Authors 3

Michelangelo Foti (first)
Anjon Audhya (additional)
Scott D. Emr (additional)

References 58 Referenced 204

10.1091/mbc.11.8.2673
10.1016/S0005-2760(98)00134-9 / Biochim. Biophys. Acta by Balla T. (1998)
10.1091/mbc.5.9.1023
10.1093/genetics/154.1.83 / Genetics by Bensen E.S. (2000)
10.1016/S1097-2765(00)80125-2 / Mol. Cell by Burd C.G. (1998)
10.1016/0092-8674(82)90384-1 / Cell by Carlson M. (1982)
10.1083/jcb.109.6.2939 / J. Cell Biol. by Cleves A.E. (1989)
10.1002/(SICI)1521-1878(199805)20:5<423::AID-BIES9>3.0.CO;2-O / Bioessays by Cockcroft S. (1998)
10.1016/S0092-8674(01)80013-1 / Cell by Cowles C.R. (1997)
10.1007/PL00000700 / Cell Mol. Life Sci. by Divecha N. (2000)
10.1016/S0021-9258(18)35954-4 / J. Biol. Chem. by Flanagan C.A. (1992)
10.1146/annurev.biochem.67.1.481 / Annu. Rev. Biochem. by Fruman D.A. (1998)
10.1002/j.1460-2075.1994.tb06519.x / EMBO J. by Garcia-Bustos J.F. (1994)
10.1083/jcb.143.1.65 / J. Cell Biol. by Gary J.D. (1998)
10.1083/jcb.136.4.789 / J. Cell Biol. by Gaynor E.C. (1997)
10.1083/jcb.127.3.653 / J. Cell Biol. by Gaynor E.C. (1994)
10.1093/emboj/19.17.4577 / EMBO J. by Gillooly D.J. (2000)
10.1083/jcb.100.3.965 / J. Cell Biol. by Greenspan P. (1985)
10.1074/jbc.274.19.12990 / J. Biol. Chem. by Guo S. (1999)
10.1074/jbc.274.48.34294 / J. Biol. Chem. by Hama H. (1999)
10.1016/S0022-2836(83)80284-8 / J. Mol. Biol. by Hanahan D. (1983)
10.1042/bj3500337 / Biochem. J. by Hughes W.E. (2000)
10.1002/(SICI)1097-0061(199908)15:11<1111::AID-YEA440>3.0.CO;2-H / Yeast by Hughes W.E. (1999)
10.1074/jbc.275.2.801 / J. Biol. Chem. by Hughes W.E. (2000)
10.1034/j.1600-0854.2000.010301.x / Traffic by Huijbregts R.P.H. (2000)
10.1128/JB.153.1.163-168.1983 / J. Bacteriol. by Ito H. (1983)
10.1093/emboj/18.6.1506 / EMBO J. by Kochendorfer K.U. (1999)
10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U / Yeast by Longtine M.S. (1998)
10.1083/jcb.138.4.731 / J. Cell Biol. by Luo W.-J. (1997)
10.1074/jbc.274.16.10669 / J. Biol. Chem. by Majerus P.W. (1999)
10.1146/annurev.cellbio.14.1.231 / Annu. Rev. Cell Dev. Biol. by Martin T.F. (1998)
10.1016/S0092-8674(00)81577-9 / Cell by Matsuoka K. (1998)
10.1083/jcb.131.6.1377 / J. Cell Biol. by Mayinger P. (1995)
10.1002/yea.320080202 / Yeast by Muhlrad D. (1992)
10.1074/jbc.M003923200 / J. Biol. Chem. by Nemoto Y. (2000)
10.1093/genetics/121.4.659 / Genetics by Novick P. (1989)
10.1016/S0092-8674(00)81707-9 / Cell by Odorizzi G. (1998)
10.1128/MCB.20.24.9376-9390.2000 / Mol. Cell. Biol. by Ooms L.M. (2000)
10.1091/mbc.7.6.985
10.1091/mbc.10.7.2235
10.1128/MCB.8.11.4936 / Mol. Cell. Biol. by Robinson J.S. (1988)
10.1128/MCB.18.9.5308 / Mol. Cell. Biol. by Sato T.K. (1998)
10.1126/science.8385367 / Science by Schu P.V. (1993)
10.1091/mbc.9.10.2873 / Mol. Cell. Biol. by Seron K. (1998)
10.1093/genetics/122.1.19 / Genetics by Sikorski R.S. (1989)
{'key': 'B49', 'first-page': '350', 'volume': '74', 'author': 'Srinivasan S.', 'year': '1997', 'journal-title': 'Eur. J. Cell Biol.'} / Eur. J. Cell Biol. by Srinivasan S. (1997)
10.1083/jcb.129.2.321 / J. Cell Biol. by Stack J.H. (1995)
10.1074/jbc.271.39.24048 / J. Biol. Chem. by Stenmark H. (1996)
10.1074/jbc.274.19.12979 / J. Biol. Chem. by Stock S.D. (1999)
10.1093/genetics/148.4.1715 / Genetics by Stolz L.E. (1998)
10.1074/jbc.273.19.11852 / J. Biol. Chem. by Stolz L.E. (1998)
10.1074/jbc.273.21.13189 / J. Biol. Chem. by Trotter P.J. (1998)
10.1083/jcb.128.5.779 / J. Cell Biol. by Vida T.A. (1995)
10.1038/70319 / Nat. Cell Biol. by Walch-Solimena C. (1999)
10.1083/jcb.122.1.79 / J. Cell Biol. by Whitters E.A. (1993)
10.1074/jbc.272.20.13236 / J. Biol. Chem. by Wong K. (1997)
10.1016/0378-1119(95)00214-Q / Gene by Yoshida S. (1995)
10.1016/S0005-2736(00)00294-7 / Biochim. Biophys. Acta by Zweytick D. (2000)

Dates

Type	When
Created	12 years, 1 month ago (July 2, 2013, 8:18 p.m.)
Deposited	3 years, 6 months ago (Feb. 26, 2022, 9:45 p.m.)
Indexed	56 minutes ago (Aug. 30, 2025, 12:21 a.m.)
Issued	24 years ago (Aug. 1, 2001)
Published	24 years ago (Aug. 1, 2001)
Published Print	24 years ago (Aug. 1, 2001)

Funders 0

None

BibTeX

@article{Foti_2001, title={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}, volume={12}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.12.8.2396}, DOI={10.1091/mbc.12.8.2396}, number={8}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Foti, Michelangelo and Audhya, Anjon and Emr, Scott D.}, editor={Drubin, David}, year={2001}, month=aug, pages={2396–2411} }

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      "first-page": "69",
      "DOI": "10.1016/S0005-2760(98)00134-9",
      "volume": "1436",
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    {
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      "DOI": "10.1016/S1097-2765(00)80125-2",
      "volume": "2",
      "author": "Burd C.G.",
      "year": "1998",
      "journal-title": "Mol. Cell"
    },
    {
      "key": "B6",
      "doi-asserted-by": "crossref",
      "first-page": "145",
      "DOI": "10.1016/0092-8674(82)90384-1",
      "volume": "28",
      "author": "Carlson M.",
      "year": "1982",
      "journal-title": "Cell"
    },
    {
      "key": "B7",
      "doi-asserted-by": "crossref",
      "first-page": "2939",
      "DOI": "10.1083/jcb.109.6.2939",
      "volume": "109",
      "author": "Cleves A.E.",
      "year": "1989",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B8",
      "doi-asserted-by": "crossref",
      "first-page": "423",
      "DOI": "10.1002/(SICI)1521-1878(199805)20:5<423::AID-BIES9>3.0.CO;2-O",
      "volume": "20",
      "author": "Cockcroft S.",
      "year": "1998",
      "journal-title": "Bioessays"
    },
    {
      "key": "B9",
      "doi-asserted-by": "crossref",
      "first-page": "109",
      "DOI": "10.1016/S0092-8674(01)80013-1",
      "volume": "91",
      "author": "Cowles C.R.",
      "year": "1997",
      "journal-title": "Cell"
    },
    {
      "key": "B10",
      "doi-asserted-by": "crossref",
      "first-page": "379",
      "DOI": "10.1007/PL00000700",
      "volume": "57",
      "author": "Divecha N.",
      "year": "2000",
      "journal-title": "Cell Mol. Life Sci."
    },
    {
      "key": "B11",
      "doi-asserted-by": "crossref",
      "first-page": "24117",
      "DOI": "10.1016/S0021-9258(18)35954-4",
      "volume": "267",
      "author": "Flanagan C.A.",
      "year": "1992",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B12",
      "doi-asserted-by": "crossref",
      "first-page": "481",
      "DOI": "10.1146/annurev.biochem.67.1.481",
      "volume": "67",
      "author": "Fruman D.A.",
      "year": "1998",
      "journal-title": "Annu. Rev. Biochem."
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    {
      "key": "B13",
      "doi-asserted-by": "crossref",
      "first-page": "2352",
      "DOI": "10.1002/j.1460-2075.1994.tb06519.x",
      "volume": "13",
      "author": "Garcia-Bustos J.F.",
      "year": "1994",
      "journal-title": "EMBO J."
    },
    {
      "key": "B14",
      "doi-asserted-by": "crossref",
      "first-page": "65",
      "DOI": "10.1083/jcb.143.1.65",
      "volume": "143",
      "author": "Gary J.D.",
      "year": "1998",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B15",
      "doi-asserted-by": "crossref",
      "first-page": "789",
      "DOI": "10.1083/jcb.136.4.789",
      "volume": "136",
      "author": "Gaynor E.C.",
      "year": "1997",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B16",
      "doi-asserted-by": "crossref",
      "first-page": "653",
      "DOI": "10.1083/jcb.127.3.653",
      "volume": "127",
      "author": "Gaynor E.C.",
      "year": "1994",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B17",
      "doi-asserted-by": "crossref",
      "first-page": "4577",
      "DOI": "10.1093/emboj/19.17.4577",
      "volume": "19",
      "author": "Gillooly D.J.",
      "year": "2000",
      "journal-title": "EMBO J."
    },
    {
      "key": "B18",
      "doi-asserted-by": "crossref",
      "first-page": "965",
      "DOI": "10.1083/jcb.100.3.965",
      "volume": "100",
      "author": "Greenspan P.",
      "year": "1985",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B19",
      "doi-asserted-by": "crossref",
      "first-page": "12990",
      "DOI": "10.1074/jbc.274.19.12990",
      "volume": "274",
      "author": "Guo S.",
      "year": "1999",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B20",
      "doi-asserted-by": "crossref",
      "first-page": "34294",
      "DOI": "10.1074/jbc.274.48.34294",
      "volume": "274",
      "author": "Hama H.",
      "year": "1999",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B21",
      "doi-asserted-by": "crossref",
      "first-page": "557",
      "DOI": "10.1016/S0022-2836(83)80284-8",
      "volume": "166",
      "author": "Hanahan D.",
      "year": "1983",
      "journal-title": "J. Mol. Biol."
    },
    {
      "key": "B22",
      "doi-asserted-by": "crossref",
      "first-page": "337",
      "DOI": "10.1042/bj3500337",
      "volume": "350",
      "author": "Hughes W.E.",
      "year": "2000",
      "journal-title": "Biochem. J."
    },
    {
      "key": "B23",
      "doi-asserted-by": "crossref",
      "first-page": "1111",
      "DOI": "10.1002/(SICI)1097-0061(199908)15:11<1111::AID-YEA440>3.0.CO;2-H",
      "volume": "15",
      "author": "Hughes W.E.",
      "year": "1999",
      "journal-title": "Yeast"
    },
    {
      "key": "B24",
      "doi-asserted-by": "crossref",
      "first-page": "801",
      "DOI": "10.1074/jbc.275.2.801",
      "volume": "275",
      "author": "Hughes W.E.",
      "year": "2000",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B25",
      "doi-asserted-by": "crossref",
      "first-page": "195",
      "DOI": "10.1034/j.1600-0854.2000.010301.x",
      "volume": "1",
      "author": "Huijbregts R.P.H.",
      "year": "2000",
      "journal-title": "Traffic"
    },
    {
      "key": "B26",
      "doi-asserted-by": "crossref",
      "first-page": "163",
      "DOI": "10.1128/JB.153.1.163-168.1983",
      "volume": "153",
      "author": "Ito H.",
      "year": "1983",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "B27",
      "doi-asserted-by": "crossref",
      "first-page": "1506",
      "DOI": "10.1093/emboj/18.6.1506",
      "volume": "18",
      "author": "Kochendorfer K.U.",
      "year": "1999",
      "journal-title": "EMBO J."
    },
    {
      "key": "B28",
      "doi-asserted-by": "crossref",
      "first-page": "953",
      "DOI": "10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U",
      "volume": "14",
      "author": "Longtine M.S.",
      "year": "1998",
      "journal-title": "Yeast"
    },
    {
      "key": "B29",
      "doi-asserted-by": "crossref",
      "first-page": "731",
      "DOI": "10.1083/jcb.138.4.731",
      "volume": "138",
      "author": "Luo W.-J.",
      "year": "1997",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B30",
      "doi-asserted-by": "crossref",
      "first-page": "10669",
      "DOI": "10.1074/jbc.274.16.10669",
      "volume": "274",
      "author": "Majerus P.W.",
      "year": "1999",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B31",
      "doi-asserted-by": "crossref",
      "first-page": "231",
      "DOI": "10.1146/annurev.cellbio.14.1.231",
      "volume": "14",
      "author": "Martin T.F.",
      "year": "1998",
      "journal-title": "Annu. Rev. Cell Dev. Biol."
    },
    {
      "key": "B32",
      "doi-asserted-by": "crossref",
      "first-page": "263",
      "DOI": "10.1016/S0092-8674(00)81577-9",
      "volume": "93",
      "author": "Matsuoka K.",
      "year": "1998",
      "journal-title": "Cell"
    },
    {
      "key": "B33",
      "doi-asserted-by": "crossref",
      "first-page": "1377",
      "DOI": "10.1083/jcb.131.6.1377",
      "volume": "131",
      "author": "Mayinger P.",
      "year": "1995",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "B34",
      "doi-asserted-by": "crossref",
      "first-page": "79",
      "DOI": "10.1002/yea.320080202",
      "volume": "8",
      "author": "Muhlrad D.",
      "year": "1992",
      "journal-title": "Yeast"
    },
    {
      "key": "B35",
      "doi-asserted-by": "crossref",
      "first-page": "34293",
      "DOI": "10.1074/jbc.M003923200",
      "volume": "275",
      "author": "Nemoto Y.",
      "year": "2000",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B36",
      "doi-asserted-by": "crossref",
      "first-page": "659",
      "DOI": "10.1093/genetics/121.4.659",
      "volume": "121",
      "author": "Novick P.",
      "year": "1989",
      "journal-title": "Genetics"
    },
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