Abstract
The Saccharomyces cerevisiae protein SEC14p is required for Golgi function and cell viability in vivo. This requirement is obviated by mutations that specifically inactivate the CDP-choline pathway for phosphatidylcholine biosynthesis. The biochemical basis for the in vivo relationship between SEC14p function and the CDP-choline pathway has remained obscure. We now report that SEC14p effects an in vivo depression of CDP-choline pathway activity by inhibiting choline-phosphate cytidylyltransferase (CCTase; EC 2.7.7.15), the rate-determining enzyme of the CDP-choline pathway. Moreover, this SEC14p-mediated inhibition of CCTase was recapitulated in vitro and was saturable. Finally, whereas the SEC14p-dependent inhibition of CCTase in vitro was markedly reduced under assay conditions that were expected to increase levels of phosphatidylinositol-bound SEC14p, assay conditions expected to increase levels of phosphatidylcholine-bound SEC14p resulted in significant potentiation of CCTase inhibition. The collective data suggest that the phosphatidylcholine-bound form of SEC14p effects an essential repression of CDP-choline pathway activity in Golgi membranes by inhibiting CCTase and that the phospholipid-binding/exchange activity of SEC14p represents a mechanism by which the regulatory activity of SEC14p is itself controlled.
MeSH Terms
Carbon Radioisotopes
Carrier Proteins/biosynthesis,isolation & purification,metabolism
Choline/metabolism
Choline-Phosphate Cytidylyltransferase
Cloning, Molecular
Cytidine Diphosphate Choline/metabolism
Cytosol/metabolism
Escherichia coli
Genotype
Golgi Apparatus/metabolism
Intracellular Membranes/metabolism
Kinetics
Ligands
Membrane Proteins
Models, Biological
Nucleotidyltransferases/antagonists & inhibitors
Phosphatidylinositols/metabolism
Phospholipid Transfer Proteins
Phospholipids/isolation & purification,metabolism
Recombinant Proteins/biosynthesis,isolation & purification,metabolism
Saccharomyces cerevisiae/genetics,metabolism
Saccharomyces cerevisiae Proteins
Chemicals
Carbon Radioisotopes
Carrier Proteins
Ligands
Membrane Proteins
Phosphatidylinositols
Phospholipid Transfer Proteins
Phospholipids
Recombinant Proteins
SEC24 protein, S cerevisiae
Saccharomyces cerevisiae Proteins
Cytidine Diphosphate Choline
Nucleotidyltransferases
Choline-Phosphate Cytidylyltransferase
Choline
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Skinner H B
Department of Cell Biology, University of Alabama, Birmingham 35294-0005.
McGee T P
McMaster C R
Fry M R
Bell R M
Bankaitis V A
References (22)
22 references, click to expand
-
A phosphatidylinositol transfer protein controls the phosphatidylcholine content of yeast Golgi membranes.
J Cell Biol. 1994 Feb;124(3):273-87
PMID: 8294512
-
Cloning and characterization of the yeast CKI gene encoding choline kinase and its expression in Escherichia coli.
J Biol Chem. 1989 Feb 5;264(4):2053-9
PMID: 2536698
-
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):4775-84
PMID: 8223486
-
SACCHAROMYCES CEREVISIAE Recessive Suppressor That Circumvents Phosphatidylserine Deficiency.
Genetics. 1984 Nov;108(3):533-43
PMID: 17246236
-
Yeast mutant with thermolabile CDP-choline synthesis. Isolation and characterization of a cholinephosphate cytidyltransferase mutant.
Eur J Biochem. 1983 Mar 1;131(1):223-9
PMID: 6299731
-
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):1271-81
PMID: 2466847
-
Phospholipid transfer proteins: a biological debut.
Trends Cell Biol. 1991 Jul;1(1):30-4
PMID: 14731807
-
Molecular cloning and characterization of the gene encoding cholinephosphate cytidylyltransferase in Saccharomyces cerevisiae.
Eur J Biochem. 1987 Dec 15;169(3):477-86
PMID: 2826147
-
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):3909-17
PMID: 3029130
-
Functional redundancy of CDP-ethanolamine and CDP-choline pathway enzymes in phospholipid biosynthesis: ethanolamine-dependent effects on steady-state membrane phospholipid composition in Saccharomyces cerevisiae.
J Bacteriol. 1994 Nov;176(22):6861-8
PMID: 7961445
-
Lipid transfer proteins.
Chem Phys Lipids. 1990 Nov;56(1):1-20
PMID: 2091833
-
An essential role for a phospholipid transfer protein in yeast Golgi function.
Nature. 1990 Oct 11;347(6293):561-2
PMID: 2215682
-
The GTPase superfamily: conserved structure and molecular mechanism.
Nature. 1991 Jan 10;349(6305):117-27
PMID: 1898771
-
Phospholipid transfer proteins.
Annu Rev Biochem. 1991;60:73-99
PMID: 1883207
-
Secretion in yeast. Purification and in vitro translocation of chemical amounts of prepro-alpha-factor.
J Biol Chem. 1991 Jul 25;266(21):13811-4
PMID: 1856213
-
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
PMID: 1997207
-
Isolation and sequence of cDNA clones encoding rat phosphatidylinositol transfer protein.
J Biol Chem. 1989 Oct 5;264(28):16557-64
PMID: 2777797
-
The gene encoding the phosphatidylinositol transfer protein is essential for cell growth.
J Biol Chem. 1990 Mar 15;265(8):4711-7
PMID: 2407740
-
Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway.
Cell. 1980 Aug;21(1):205-15
PMID: 6996832
-
Coordinate regulation of phospholipid biosynthesis in Saccharomyces cerevisiae: pleiotropically constitutive opi1 mutant.
J Bacteriol. 1985 Jun;162(3):1135-41
PMID: 3888957
-
The synthesis of cytidine diphosphate choline, cytidine diphosphate ethanolamine, and related compounds.
J Biol Chem. 1956 Sep;222(1):185-91
PMID: 13366992
-
Transformation of intact yeast cells treated with alkali cations.
J Bacteriol. 1983 Jan;153(1):163-8
PMID: 6336730