Search tips
Search criteria 


Logo of jcellbiolHomeThe Rockefeller University PressEditorsContactInstructions for AuthorsThis issue
J Cell Biol. 1988 March 1; 106(3): 641–648.
PMCID: PMC2115093

Secretory vesicles externalize the major plasma membrane ATPase in yeast


Yeast cell surface growth is accomplished by constitutive secretion and plasma membrane assembly, culminating in the fusion of vesicles with the bud membrane. Coordination of secretion and membrane assembly has been investigated by examining the biogenesis of plasma membrane ATPase (PM ATPase) in secretion-defective (sec) strains of Saccharomyces cerevisiae. PM ATPase is synthesized as a approximately 106-kD polypeptide that is not detectably modified by asparagine-linked glycosylation or proteolysis during transit to the plasma membrane. Export of the PM ATPase requires the secretory pathway. In sec1, a mutant defective in the last step of secretion, large amounts of Golgi- derived vesicles are accumulated. Biochemical characterization of this organelle has demonstrated that PM ATPase and the secretory enzyme, acid phosphatase, are transported in a single vesicle species.

Full Text

The Full Text of this article is available as a PDF (1.2M).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Atkinson KD, Ramirez RM. Secretion can proceed uncoupled from net plasma membrane expansion in inositol-starved Saccharomyces cerevisiae. J Bacteriol. 1984 Oct;160(1):80–86. [PMC free article] [PubMed]
  • Bernstein M, Hoffmann W, Ammerer G, Schekman R. Characterization of a gene product (Sec53p) required for protein assembly in the yeast endoplasmic reticulum. J Cell Biol. 1985 Dec;101(6):2374–2382. [PMC free article] [PubMed]
  • Bordallo C, Schwencke J, Suarez Rendueles M. Localization of the thermosensitive X-prolyl dipeptidyl aminopeptidase in the vacuolar membrane of Saccharomyces cerevisiae. FEBS Lett. 1984 Jul 23;173(1):199–203. [PubMed]
  • Bulawa CE, Slater M, Cabib E, Au-Young J, Sburlati A, Adair WL, Jr, Robbins PW. The S. cerevisiae structural gene for chitin synthase is not required for chitin synthesis in vivo. Cell. 1986 Jul 18;46(2):213–225. [PubMed]
  • Deshaies RJ, Schekman R. A yeast mutant defective at an early stage in import of secretory protein precursors into the endoplasmic reticulum. J Cell Biol. 1987 Aug;105(2):633–645. [PMC free article] [PubMed]
  • Elango N, Correa JU, Cabib E. Secretory character of yeast chitinase. J Biol Chem. 1982 Feb 10;257(3):1398–1400. [PubMed]
  • Esmon B, Novick P, Schekman R. Compartmentalized assembly of oligosaccharides on exported glycoproteins in yeast. Cell. 1981 Aug;25(2):451–460. [PubMed]
  • Feldman RI, Bernstein M, Schekman R. Product of SEC53 is required for folding and glycosylation of secretory proteins in the lumen of the yeast endoplasmic reticulum. J Biol Chem. 1987 Jul 5;262(19):9332–9339. [PubMed]
  • Ferro-Novick S, Novick P, Field C, Schekman R. Yeast secretory mutants that block the formation of active cell surface enzymes. J Cell Biol. 1984 Jan;98(1):35–43. [PMC free article] [PubMed]
  • Field C, Schekman R. Localized secretion of acid phosphatase reflects the pattern of cell surface growth in Saccharomyces cerevisiae. J Cell Biol. 1980 Jul;86(1):123–128. [PMC free article] [PubMed]
  • Fuller SD, Bravo R, Simons K. An enzymatic assay reveals that proteins destined for the apical or basolateral domains of an epithelial cell line share the same late Golgi compartments. EMBO J. 1985 Feb;4(2):297–307. [PubMed]
  • Gumbiner B, Kelly RB. Two distinct intracellular pathways transport secretory and membrane glycoproteins to the surface of pituitary tumor cells. Cell. 1982 Jan;28(1):51–59. [PubMed]
  • Holcomb CL, Etcheverry T, Schekman R. Isolation of secretory vesicles from Saccharomyces cerevisiae. Anal Biochem. 1987 Nov 1;166(2):328–334. [PubMed]
  • HUNTER WM, GREENWOOD FC. Preparation of iodine-131 labelled human growth hormone of high specific activity. Nature. 1962 May 5;194:495–496. [PubMed]
  • Julius D, Blair L, Brake A, Sprague G, Thorner J. Yeast alpha factor is processed from a larger precursor polypeptide: the essential role of a membrane-bound dipeptidyl aminopeptidase. Cell. 1983 Mar;32(3):839–852. [PubMed]
  • Kelly RB. Pathways of protein secretion in eukaryotes. Science. 1985 Oct 4;230(4721):25–32. [PubMed]
  • Koland JG, Hammes GG. Steady state kinetic studies of purified yeast plasma membrane proton-translocating ATPase. J Biol Chem. 1986 May 5;261(13):5936–5942. [PubMed]
  • Kubota S, Yoshida Y, Kumaoka H, Furumichi A. Studies on the microsomal electron-transport system of anaerobically grown yeast. V. Purification and characterization of NADPH-cytochrome c reductase. J Biochem. 1977 Jan;81(1):197–205. [PubMed]
  • Lodish HF, Braell WA, Schwartz AL, Strous GJ, Zilberstein A. Synthesis and assembly of membrane and organelle proteins. Int Rev Cytol Suppl. 1981;12:247–307. [PubMed]
  • Moore HP, Gumbiner B, Kelly RB. A subclass of proteins and sulfated macromolecules secreted by AtT-20 (mouse pituitary tumor) cells is sorted with adrenocorticotropin into dense secretory granules. J Cell Biol. 1983 Sep;97(3):810–817. [PMC free article] [PubMed]
  • Moore HP, Walker MD, Lee F, Kelly RB. Expressing a human proinsulin cDNA in a mouse ACTH-secreting cell. Intracellular storage, proteolytic processing, and secretion on stimulation. Cell. 1983 Dec;35(2 Pt 1):531–538. [PubMed]
  • Nakajima T, Ballou CE. Yeast manno-protein biosynthesis: solubilization and selective assay of four mannosyltransferases. Proc Natl Acad Sci U S A. 1975 Oct;72(10):3912–3916. [PubMed]
  • Novick P, Schekman R. Secretion and cell-surface growth are blocked in a temperature-sensitive mutant of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1858–1862. [PubMed]
  • Novick P, Schekman R. Export of major cell surface proteins is blocked in yeast secretory mutants. J Cell Biol. 1983 Feb;96(2):541–547. [PMC free article] [PubMed]
  • Novick P, Ferro S, Schekman R. Order of events in the yeast secretory pathway. Cell. 1981 Aug;25(2):461–469. [PubMed]
  • Novick P, Field C, Schekman R. Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell. 1980 Aug;21(1):205–215. [PubMed]
  • Palade G. Intracellular aspects of the process of protein synthesis. Science. 1975 Aug 1;189(4200):347–358. [PubMed]
  • Pfeffer SR, Kelly RB. The subpopulation of brain coated vesicles that carries synaptic vesicle proteins contains two unique polypeptides. Cell. 1985 Apr;40(4):949–957. [PubMed]
  • Rindler MJ, Ivanov IE, Plesken H, Rodriguez-Boulan E, Sabatini DD. Viral glycoproteins destined for apical or basolateral plasma membrane domains traverse the same Golgi apparatus during their intracellular transport in doubly infected Madin-Darby canine kidney cells. J Cell Biol. 1984 Apr;98(4):1304–1319. [PMC free article] [PubMed]
  • Rodriguez Boulan E, Sabatini DD. Asymmetric budding of viruses in epithelial monlayers: a model system for study of epithelial polarity. Proc Natl Acad Sci U S A. 1978 Oct;75(10):5071–5075. [PubMed]
  • Schauer I, Emr S, Gross C, Schekman R. Invertase signal and mature sequence substitutions that delay intercompartmental transport of active enzyme. J Cell Biol. 1985 May;100(5):1664–1675. [PMC free article] [PubMed]
  • Scott JH, Schekman R. Lyticase: endoglucanase and protease activities that act together in yeast cell lysis. J Bacteriol. 1980 May;142(2):414–423. [PMC free article] [PubMed]
  • Serrano R. Plasma membrane ATPase of fungi and plants as a novel type of proton pump. Curr Top Cell Regul. 1984;23:87–126. [PubMed]
  • Serrano R, Kielland-Brandt MC, Fink GR. Yeast plasma membrane ATPase is essential for growth and has homology with (Na+ + K+), K+- and Ca2+-ATPases. Nature. 1986 Feb 20;319(6055):689–693. [PubMed]
  • Simons K, Fuller SD. Cell surface polarity in epithelia. Annu Rev Cell Biol. 1985;1:243–288. [PubMed]
  • Stevens T, Esmon B, Schekman R. Early stages in the yeast secretory pathway are required for transport of carboxypeptidase Y to the vacuole. Cell. 1982 Sep;30(2):439–448. [PubMed]
  • Strous GJ, Lodish HF. Intracellular transport of secretory and membrane proteins in hepatoma cells infected by vesicular stomatitis virus. Cell. 1980 Dec;22(3):709–717. [PubMed]
  • Strous GJ, Willemsen R, van Kerkhof P, Slot JW, Geuze HJ, Lodish HF. Vesicular stomatitis virus glycoprotein, albumin, and transferrin are transported to the cell surface via the same Golgi vesicles. J Cell Biol. 1983 Dec;97(6):1815–1822. [PMC free article] [PubMed]
  • To-E A, Ueda Y, Kakimoto SI, Oshima Y. Isolation and characterization of acid phosphatase mutants in Saccharomyces cerevisiae. J Bacteriol. 1973 Feb;113(2):727–738. [PMC free article] [PubMed]
  • Tschopp J, Esmon PC, Schekman R. Defective plasma membrane assembly in yeast secretory mutants. J Bacteriol. 1984 Dec;160(3):966–970. [PMC free article] [PubMed]
  • Van Rijn HJ, Boer P, Steyn-Parvé EP. Biosynthesis of acid phosphatase of baker's yeast. Factors influencing its production by protoplasts and characterization of the secreted enzyme. Biochim Biophys Acta. 1972 May 12;268(2):431–441. [PubMed]
  • Vincent R, Nadeau D. A micromethod for the quantitation of cellular proteins in Percoll with the Coomassie brilliant blue dye-binding assay. Anal Biochem. 1983 Dec;135(2):355–362. [PubMed]
  • Walworth NC, Novick PJ. Purification and characterization of constitutive secretory vesicles from yeast. J Cell Biol. 1987 Jul;105(1):163–174. [PMC free article] [PubMed]

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