Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1994 Feb 1;124(3):273–287. doi: 10.1083/jcb.124.3.273

A phosphatidylinositol transfer protein controls the phosphatidylcholine content of yeast Golgi membranes

PMCID: PMC2119930  PMID: 8294512

Abstract

SEC14p is required for protein transport from the yeast Golgi complex. We describe a quantitative analysis of yeast bulk membrane and Golgi membrane phospholipid composition under conditions where Golgi secretory function has been uncoupled from its usual SEC14p requirement. The data demonstrate that SEC14p specifically functions to maintain a reduced phosphatidylcholine content in Golgi membranes and indicate that overproduction of SEC14p markedly reduces the apparent rate of phosphatidylcholine biosynthesis via the CDP-choline pathway in vivo. We suggest that SEC14p serves as a sensor of Golgi membrane phospholipid composition through which the activity of the CDP-choline pathway in Golgi membranes is regulated such that a phosphatidylcholine content that is compatible with the essential secretory function of these membranes is maintained.

Full Text

The Full Text of this article is available as a PDF (2.0 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aitken J. F., van Heusden G. P., Temkin M., Dowhan W. The gene encoding the phosphatidylinositol transfer protein is essential for cell growth. J Biol Chem. 1990 Mar 15;265(8):4711–4717. [PubMed] [Google Scholar]
  2. Atkinson K. D. SACCHAROMYCES CEREVISIAE Recessive Suppressor That Circumvents Phosphatidylserine Deficiency. Genetics. 1984 Nov;108(3):533–543. doi: 10.1093/genetics/108.3.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Atkinson K., Fogel S., Henry S. A. Yeast mutant defective in phosphatidylserine synthesis. J Biol Chem. 1980 Jul 25;255(14):6653–6661. [PubMed] [Google Scholar]
  4. Bankaitis V. A., Aitken J. R., Cleves A. E., Dowhan W. An essential role for a phospholipid transfer protein in yeast Golgi function. Nature. 1990 Oct 11;347(6293):561–562. doi: 10.1038/347561a0. [DOI] [PubMed] [Google Scholar]
  5. Bankaitis V. A., Malehorn D. E., Emr S. D., Greene R. The Saccharomyces cerevisiae SEC14 gene encodes a cytosolic factor that is required for transport of secretory proteins from the yeast Golgi complex. J Cell Biol. 1989 Apr;108(4):1271–1281. doi: 10.1083/jcb.108.4.1271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bowman B. J., Slayman C. W. The effects of vanadate on the plasma membrane ATPase of Neurospora crassa. J Biol Chem. 1979 Apr 25;254(8):2928–2934. [PubMed] [Google Scholar]
  7. Böhni P. C., Deshaies R. J., Schekman R. W. SEC11 is required for signal peptide processing and yeast cell growth. J Cell Biol. 1988 Apr;106(4):1035–1042. doi: 10.1083/jcb.106.4.1035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Carman G. M., Henry S. A. Phospholipid biosynthesis in yeast. Annu Rev Biochem. 1989;58:635–669. doi: 10.1146/annurev.bi.58.070189.003223. [DOI] [PubMed] [Google Scholar]
  9. Cleves A. E., McGee T. P., Whitters E. A., Champion K. M., Aitken J. R., Dowhan W., Goebl M., Bankaitis V. A. Mutations in the CDP-choline pathway for phospholipid biosynthesis bypass the requirement for an essential phospholipid transfer protein. Cell. 1991 Feb 22;64(4):789–800. doi: 10.1016/0092-8674(91)90508-v. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cleves A. E., Novick P. J., Bankaitis V. A. Mutations in the SAC1 gene suppress defects in yeast Golgi and yeast actin function. J Cell Biol. 1989 Dec;109(6 Pt 1):2939–2950. doi: 10.1083/jcb.109.6.2939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cleves A., McGee T., Bankaitis V. Phospholipid transfer proteins: a biological debut. Trends Cell Biol. 1991 Jul;1(1):30–34. doi: 10.1016/0962-8924(91)90067-j. [DOI] [PubMed] [Google Scholar]
  12. Franzusoff A., Redding K., Crosby J., Fuller R. S., Schekman R. Localization of components involved in protein transport and processing through the yeast Golgi apparatus. J Cell Biol. 1991 Jan;112(1):27–37. doi: 10.1083/jcb.112.1.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Franzusoff A., Schekman R. Functional compartments of the yeast Golgi apparatus are defined by the sec7 mutation. EMBO J. 1989 Sep;8(9):2695–2702. doi: 10.1002/j.1460-2075.1989.tb08410.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gietz R. D., Sugino A. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene. 1988 Dec 30;74(2):527–534. doi: 10.1016/0378-1119(88)90185-0. [DOI] [PubMed] [Google Scholar]
  15. Greenberg M. L., Reiner B., Henry S. A. Regulatory mutations of inositol biosynthesis in yeast: isolation of inositol-excreting mutants. Genetics. 1982 Jan;100(1):19–33. doi: 10.1093/genetics/100.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hjelmstad R. H., Bell R. M. Mutants of Saccharomyces cerevisiae defective in sn-1,2-diacylglycerol cholinephosphotransferase. Isolation, characterization, and cloning of the CPT1 gene. J Biol Chem. 1987 Mar 15;262(8):3909–3917. [PubMed] [Google Scholar]
  17. Hjelmstad R. H., Bell R. M. The sn-1,2-diacylglycerol ethanolaminephosphotransferase activity of Saccharomyces cerevisiae. Isolation of mutants and cloning of the EPT1 gene. J Biol Chem. 1988 Dec 25;263(36):19748–19757. [PubMed] [Google Scholar]
  18. Klig L. S., Homann M. J., Carman G. M., Henry S. A. Coordinate regulation of phospholipid biosynthesis in Saccharomyces cerevisiae: pleiotropically constitutive opi1 mutant. J Bacteriol. 1985 Jun;162(3):1135–1141. doi: 10.1128/jb.162.3.1135-1141.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kreibich G., Debey P., Sabatini D. D. Selective release of content from microsomal vesicles without membrane disassembly. I. Permeability changes induced by low detergent concentrations. J Cell Biol. 1973 Aug;58(2):436–462. doi: 10.1083/jcb.58.2.436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mason T. L., Poyton R. O., Wharton D. C., Schatz G. Cytochrome c oxidase from bakers' yeast. I. Isolation and properties. J Biol Chem. 1973 Feb 25;248(4):1346–1354. [PubMed] [Google Scholar]
  21. Redding K., Holcomb C., Fuller R. S. Immunolocalization of Kex2 protease identifies a putative late Golgi compartment in the yeast Saccharomyces cerevisiae. J Cell Biol. 1991 May;113(3):527–538. doi: 10.1083/jcb.113.3.527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rothman J. E. Phospholipid transfer market. Nature. 1990 Oct 11;347(6293):519–520. doi: 10.1038/347519a0. [DOI] [PubMed] [Google Scholar]
  23. Rueckert D. G., Schmidt K. Lipid transfer proteins. Chem Phys Lipids. 1990 Nov;56(1):1–20. doi: 10.1016/0009-3084(90)90083-4. [DOI] [PubMed] [Google Scholar]
  24. Skinner H. B., Alb J. G., Jr, Whitters E. A., Helmkamp G. M., Jr, Bankaitis V. A. Phospholipid transfer activity is relevant to but not sufficient for the essential function of the yeast SEC14 gene product. EMBO J. 1993 Dec;12(12):4775–4784. doi: 10.1002/j.1460-2075.1993.tb06166.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Steiner M. R., Lester R. L. In vitro studies of phospholipid biosynthesis in Saccharomyces cerevisiae. Biochim Biophys Acta. 1972 Feb 21;260(2):222–243. doi: 10.1016/0005-2760(72)90035-5. [DOI] [PubMed] [Google Scholar]
  26. Vance J. E., Cui Z. Interpreting the effects of blocking PC biosynthesis. Trends Cell Biol. 1992 Mar;2(3):71–72. doi: 10.1016/0962-8924(92)90062-r. [DOI] [PubMed] [Google Scholar]
  27. Vance J. E., Vance D. E. Does rat liver Golgi have the capacity to synthesize phospholipids for lipoprotein secretion? J Biol Chem. 1988 Apr 25;263(12):5898–5909. [PubMed] [Google Scholar]
  28. Whitters E. A., Cleves A. E., McGee T. P., Skinner H. B., Bankaitis V. A. SAC1p is an integral membrane protein that influences the cellular requirement for phospholipid transfer protein function and inositol in yeast. J Cell Biol. 1993 Jul;122(1):79–94. doi: 10.1083/jcb.122.1.79. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Wirtz K. W. Phospholipid transfer proteins. Annu Rev Biochem. 1991;60:73–99. doi: 10.1146/annurev.bi.60.070191.000445. [DOI] [PubMed] [Google Scholar]
  30. Zinser E., Sperka-Gottlieb C. D., Fasch E. V., Kohlwein S. D., Paltauf F., Daum G. Phospholipid synthesis and lipid composition of subcellular membranes in the unicellular eukaryote Saccharomyces cerevisiae. J Bacteriol. 1991 Mar;173(6):2026–2034. doi: 10.1128/jb.173.6.2026-2034.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. van Meer G. Lipid traffic in animal cells. Annu Rev Cell Biol. 1989;5:247–275. doi: 10.1146/annurev.cb.05.110189.001335. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES