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PMID: 8391537 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Guanosine diphosphatase is required for protein and sphingolipid glycosylation in the Golgi lumen of Saccharomyces cerevisiae.

The Journal of cell biology ·Vol. 122 ·No. 2 ·1993-07-00 ·Pages 307-23

Abeijon C, Yanagisawa K, Mandon EC, Häusler A, Moremen K, Hirschberg CB, Robbins PW

Abstract

Current models for nucleotide sugar use in the Golgi apparatus predict a critical role for the lumenal nucleoside diphosphatase. After transfer of sugars to endogenous macromolecular acceptors, the enzyme converts nucleoside diphosphates to nucleoside monophosphates which in turn exit the Golgi lumen in a coupled antiporter reaction, allowing entry of additional nucleotide sugar from the cytosol. To test this model, we cloned the gene for the S. cerevisiae guanosine diphosphatase and constructed a null mutation. This mutation should reduce the concentrations of GDP-mannose and GMP and increase the concentration of GDP in the Golgi lumen. The alterations should in turn decrease mannosylation of proteins and lipids in this compartment. In fact, we found a partial block in O- and N-glycosylation of proteins such as chitinase and carboxypeptidase Y and underglycosylation of invertase. In addition, mannosylinositolphosphorylceramide levels were drastically reduced.

Related Genes
GDA1
MeSH Terms
Amino Acid Sequence Base Sequence Carboxypeptidases/biosynthesis Cathepsin A Cell Wall/chemistry,ultrastructure Ceramides/biosynthesis Chitinases/metabolism Cloning, Molecular Genes, Fungal Glycoside Hydrolases/metabolism Glycosylation Golgi Apparatus/metabolism Mannose/metabolism Molecular Sequence Data Mutation Proteins/metabolism Pyrophosphatases/genetics,metabolism Saccharomyces cerevisiae/genetics,growth & development,metabolism,ultrastructure Saccharomyces cerevisiae Proteins beta-Fructofuranosidase
Chemicals
Ceramides Proteins Saccharomyces cerevisiae Proteins Glycoside Hydrolases Chitinases beta-Fructofuranosidase Carboxypeptidases Cathepsin A PRC1 protein, S cerevisiae serine carboxypeptidase Pyrophosphatases guanosine-diphosphatase Mannose
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Abeijon C
Department of Biochemistry and Molecular Biology, University of Massachusetts Medical Center, Worcester 01655.
Yanagisawa K
Mandon E C
Häusler A
Moremen K
Hirschberg C B
Robbins P W
References (73)
73 references, click to expand
  1. Dolichyl phosphate-mediated mannosyl transfer through liposomal membranes.
    Proc Natl Acad Sci U S A. 1982 Mar;79(5):1520-4 PMID: 6951194
  2. Yeast KRE genes provide evidence for a pathway of cell wall beta-glucan assembly.
    J Cell Biol. 1990 May;110(5):1833-43 PMID: 2186051
  3. Some kinetic properties of human-milk galactosyl transferase.
    Eur J Biochem. 1974 May 15;44(2):537-60 PMID: 4209349
  4. Yeast/E. coli shuttle vectors with multiple unique restriction sites.
    Yeast. 1986 Sep;2(3):163-7 PMID: 3333305
  5. Isolation, characterization, and properties of Saccharomyces cerevisiae mnn mutants with nonconditional protein glycosylation defects.
    Methods Enzymol. 1990;185:440-70 PMID: 2199792
  6. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  7. Yeast KRE2 defines a new gene family encoding probable secretory proteins, and is required for the correct N-glycosylation of proteins.
    Genetics. 1992 Feb;130(2):273-83 PMID: 1541391
  8. Revision of the oligosaccharide structures of yeast carboxypeptidase Y.
    Proc Natl Acad Sci U S A. 1990 May;87(9):3368-72 PMID: 2185468
  9. Yeast manno-protein biosynthesis: solubilization and selective assay of four mannosyltransferases.
    Proc Natl Acad Sci U S A. 1975 Oct;72(10):3912-6 PMID: 1105568
  10. Glycosyltransferases. Structure, localization, and control of cell type-specific glycosylation.
    J Biol Chem. 1989 Oct 25;264(30):17615-8 PMID: 2681181
  11. Biosynthesis of phosphoinositol-containing sphingolipids from phosphatidylinositol by a membrane preparation from Saccharomyces cerevisiae.
    J Bacteriol. 1980 Jun;142(3):747-54 PMID: 6991492
  12. Topology of eukaryotic type II membrane proteins: importance of N-terminal positively charged residues flanking the hydrophobic domain.
    Cell. 1991 Feb 22;64(4):777-87 PMID: 1997206
  13. Protein glycosylation in yeast.
    Annu Rev Biochem. 1987;56:915-44 PMID: 3304149
  14. Improved tools for biological sequence comparison.
    Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444-8 PMID: 3162770
  15. Structure of Saccharomyces cerevisiae alg3, sec18 mutant oligosaccharides.
    J Biol Chem. 1991 Mar 25;266(9):5547-51 PMID: 2005096
  16. Bifunctional role of glycosphingolipids. Modulators for transmembrane signaling and mediators for cellular interactions.
    J Biol Chem. 1990 Nov 5;265(31):18713-6 PMID: 2229037
  17. Internal amino acid sequence analysis of proteins separated by one- or two-dimensional gel electrophoresis after in situ protease digestion on nitrocellulose.
    Proc Natl Acad Sci U S A. 1987 Oct;84(20):6970-4 PMID: 3313383
  18. Distinct sets of SEC genes govern transport vesicle formation and fusion early in the secretory pathway.
    Cell. 1990 May 18;61(4):723-33 PMID: 2188733
  19. Analysis of glycoproteins from Saccharomyces cerevisiae.
    Methods Enzymol. 1991;194:682-97 PMID: 2005816
  20. A simple method for displaying the hydropathic character of a protein.
    J Mol Biol. 1982 May 5;157(1):105-32 PMID: 7108955
  21. Localization of components involved in protein transport and processing through the yeast Golgi apparatus.
    J Cell Biol. 1991 Jan;112(1):27-37 PMID: 1986005
  22. Orientation and role of nucleosidediphosphatase and 5'-nucleotidase in Golgi vesicles from rat liver.
    Biochemistry. 1982 Sep 14;21(19):4640-5 PMID: 6291586
  23. Early stages in the yeast secretory pathway are required for transport of carboxypeptidase Y to the vacuole.
    Cell. 1982 Sep;30(2):439-48 PMID: 6754086
  24. Dolichol phosphate mannose synthase is required in vivo for glycosyl phosphatidylinositol membrane anchoring, O mannosylation, and N glycosylation of protein in Saccharomyces cerevisiae.
    Mol Cell Biol. 1990 Nov;10(11):5796-805 PMID: 2146492
  25. Phosphatidylinositol phosphate, phosphatidylinositol bisphosphate, and the phosphoinositol sphingolipids are found in the plasma membrane and stimulate the plasma membrane H(+)-ATPase of Saccharomyces cerevisiae.
    Arch Biochem Biophys. 1992 Jan;292(1):70-6 PMID: 1309300
  26. Functional compartments of the yeast Golgi apparatus are defined by the sec7 mutation.
    EMBO J. 1989 Sep;8(9):2695-702 PMID: 2684655
  27. Topography of glycosylation in the rough endoplasmic reticulum and Golgi apparatus.
    Annu Rev Biochem. 1987;56:63-87 PMID: 3304145
  28. Beta-D-fructofuranoside fructohydrolase from yeast.
    Methods Enzymol. 1975;42:504-11 PMID: 237205
  29. Isolation and partial characterization of a major inositol-containing lipid in baker's yeast, mannosyl-diinositol, diphosphoryl-ceramide.
    Proc Natl Acad Sci U S A. 1969 Nov;64(3):1042-8 PMID: 4313330
  30. The yeast GTP-binding YPT1 protein and a mammalian counterpart are associated with the secretion machinery.
    Cell. 1988 Mar 25;52(6):915-24 PMID: 3127057
  31. Identification of a glycolipid precursor of the Trypanosoma brucei variant surface glycoprotein.
    J Biol Chem. 1986 Sep 15;261(26):12147-53 PMID: 3745182
  32. Partial purification of a mannosyltransferase involved in the O-mannosylation of glycoproteins from Saccharomyces cerevisiae.
    Glycobiology. 1991 Sep;1(4):367-73 PMID: 1820198
  33. Characterization of the Saccharomyces Golgi complex through the cell cycle by immunoelectron microscopy.
    Mol Biol Cell. 1992 Jul;3(7):789-803 PMID: 1381247
  34. ADP-ribosylation factor is functionally and physically associated with the Golgi complex.
    Proc Natl Acad Sci U S A. 1990 Feb;87(3):1238-42 PMID: 2105501
  35. Structure, assembly, and secretion of octameric invertase.
    J Biol Chem. 1987 Mar 25;262(9):4387-94 PMID: 3031075
  36. Inositol-requiring mutants of Saccharomyces cerevisiae.
    Genetics. 1975 May;80(1):23-40 PMID: 1093935
  37. The yeast secretory pathway is perturbed by mutations in PMR1, a member of a Ca2+ ATPase family.
    Cell. 1989 Jul 14;58(1):133-45 PMID: 2526682
  38. The role of nucleoside diphosphatase in a uridine nucleotide cycle associated with lactose synthesis in rat mammary-gland Golgi apparatus.
    Biochem J. 1977 Dec 15;168(3):423-33 PMID: 204286
  39. Glycosylation in Saccharomyces cerevisiae: cloning and characterization of an alpha-1,2-mannosyltransferase structural gene.
    Glycobiology. 1992 Feb;2(1):77-84 PMID: 1550992
  40. Glycoprotein biosynthesis in Saccharomyces cerevisiae. Isolation and characterization of the gene encoding a specific processing alpha-mannosidase.
    J Biol Chem. 1991 Aug 15;266(23):15120-7 PMID: 1714453
  41. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  42. Carbohydrate moiety of carboxypeptidase Y and perturbation of its biosynthesis.
    Eur J Biochem. 1978 Nov 15;91(2):567-75 PMID: 365528
  43. A guanosine diphosphatase enriched in Golgi vesicles of Saccharomyces cerevisiae. Purification and characterization.
    J Biol Chem. 1990 Nov 5;265(31):19351-5 PMID: 2172253
  44. One-step gene disruption in yeast.
    Methods Enzymol. 1983;101:202-11 PMID: 6310324
  45. Turnover of inositol and phosphorus containing lipids in Saccharomyces cerevisiae; extracellular accumulation of glycerophosphorylinositol derived from phosphatidylinositol.
    Arch Biochem Biophys. 1972 Aug;151(2):483-95 PMID: 4339932
  46. Topography of glycosylation in yeast: characterization of GDPmannose transport and lumenal guanosine diphosphatase activities in Golgi-like vesicles.
    Proc Natl Acad Sci U S A. 1989 Sep;86(18):6935-9 PMID: 2476806
  47. Two differentially regulated mRNAs with different 5' ends encode secreted with intracellular forms of yeast invertase.
    Cell. 1982 Jan;28(1):145-54 PMID: 7039847
  48. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  49. Chitinase is required for cell separation during growth of Saccharomyces cerevisiae.
    J Biol Chem. 1991 Oct 15;266(29):19758-67 PMID: 1918080
  50. Order of events in the yeast secretory pathway.
    Cell. 1981 Aug;25(2):461-9 PMID: 7026045
  51. Immunolocalization of Kex2 protease identifies a putative late Golgi compartment in the yeast Saccharomyces cerevisiae.
    J Cell Biol. 1991 May;113(3):527-38 PMID: 2016334
  52. Structural requirements of a membrane-spanning domain for protein anchoring and cell surface transport.
    Cell. 1985 Jul;41(3):1007-15 PMID: 3924407
  53. A Critical Evaluation of the Nitrogen Assimilation Tests Commonly Used in the Classification of Yeasts.
    J Bacteriol. 1946 Sep;52(3):293-301 PMID: 16561177
  54. Yeast glycoprotein biosynthesis: MNT1 encodes an alpha-1,2-mannosyltransferase involved in O-glycosylation.
    Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6846-50 PMID: 1495972
  55. Role of microtubules in the organisation of the Golgi apparatus.
    Cell Motil Cytoskeleton. 1990;15(2):67-70 PMID: 2178782
  56. Selective and immediate effects of clathrin heavy chain mutations on Golgi membrane protein retention in Saccharomyces cerevisiae.
    J Cell Biol. 1992 Aug;118(3):531-40 PMID: 1322413
  57. Yeast KEX2 protease and mannosyltransferase I are localized to distinct compartments of the secretory pathway.
    Yeast. 1989 Jan-Feb;5(1):25-33 PMID: 2648696
  58. 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
  59. Isolation of a rat liver Golgi mannosidase II clone by mixed oligonucleotide-primed amplification of cDNA.
    Proc Natl Acad Sci U S A. 1989 Jul;86(14):5276-80 PMID: 2748583
  60. O-glycosylation in Saccharomyces cerevisiae is initiated at the endoplasmic reticulum.
    FEBS Lett. 1983 Jul 25;158(2):335-8 PMID: 6347716
  61. Isolation, characterization, and expression of cDNAs encoding murine alpha-mannosidase II, a Golgi enzyme that controls conversion of high mannose to complex N-glycans.
    J Cell Biol. 1991 Dec;115(6):1521-34 PMID: 1757461
  62. Inositol phosphorylceramide, a novel substance and the chief member of a major group of yeast sphingolipids containing a single inositol phosphate.
    J Biol Chem. 1974 Jun 10;249(11):3395-405 PMID: 4364653
  63. Immuno-isolation of Sec7p-coated transport vesicles from the yeast secretory pathway.
    Nature. 1992 Jan 9;355(6356):173-5 PMID: 1729652
  64. Sec15 protein, an essential component of the exocytotic apparatus, is associated with the plasma membrane and with a soluble 19.5S particle.
    J Cell Biol. 1991 Mar;112(6):1117-31 PMID: 1900300
  65. Biosynthesis of the vacuolar yeast glycoprotein carboxypeptidase Y. Conversion of precursor into the enzyme.
    Eur J Biochem. 1978 Apr 17;85(2):599-608 PMID: 348476
  66. Structure of oligosaccharides on Saccharomyces SUC2 invertase secreted by the methylotrophic yeast Pichia pastoris.
    J Biol Chem. 1991 Dec 5;266(34):22807-17 PMID: 1744075
  67. Functions of sphingolipids and sphingolipid breakdown products in cellular regulation.
    Science. 1989 Jan 27;243(4890):500-7 PMID: 2643164
  68. Biosynthesis of mannosylinositolphosphoceramide in Saccharomyces cerevisiae is dependent on genes controlling the flow of secretory vesicles from the endoplasmic reticulum to the Golgi.
    J Cell Biol. 1991 May;113(3):515-25 PMID: 2016333
  69. Cloning and sequencing of the yeast gene for dolichol phosphate mannose synthase, an essential protein.
    J Biol Chem. 1988 Nov 25;263(33):17499-507 PMID: 3053713
  70. Myo-inositol transport in Saccharomyces cerevisiae.
    J Bacteriol. 1982 May;150(2):441-6 PMID: 7040334
  71. Synthesis of an O-glycosylated cell surface protein induced in yeast by alpha factor.
    Proc Natl Acad Sci U S A. 1986 Sep;83(17):6263-6 PMID: 16593749
  72. Compartmental organization of Golgi-specific protein modification and vacuolar protein sorting events defined in a yeast sec18 (NSF) mutant.
    J Cell Biol. 1991 Jul;114(2):207-18 PMID: 2071670
  73. Transformation of intact yeast cells treated with alkali cations.
    J Bacteriol. 1983 Jan;153(1):163-8 PMID: 6336730
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.122.2.307
Published
1993-07-00
Pages
307-23
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2119650
Subset
IM
Grants
NIGMS NIH HHS · GM 30365 · United States
NIGMS NIH HHS · GM 45188 · United States
Databases
GENBANK
L19560
External Links
PubMed source DOI: 10.1083/jcb.122.2.307 PMC Full Text View journal details
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