The newly identified yeast GRD genes are required for retention of late-Golgi membrane proteins. (original) (raw)

Mol Cell Biol. 1996 Jun; 16(6): 2700–2707.

Division of Biological Sciences, University of Missouri, Columbia 65211, USA.

Abstract

Processing of A-ALP, a late-Golgi membrane protein constructed by fusing the cytosolic domain of dipeptidyl aminopeptidase A to the transmembrane and lumenal domains of alkaline phosphatase (ALP), serves as a convenient assay for loss of retention of late-Golgi membrane proteins in Saccharomyces cerevisiae. In this study, a large group of novel grd (for Golgi retention defective) yeast mutants, representing 18 complementation groups, were identified on the basis of their mislocalization of A-ALP to the vacuole, where it was proteolytically processed and thus became enzymatically activated. All of the grd mutants exhibited significant mislocalization of A-ALP, as measured by determining the kinetics of A-ALP processing and by analyzing its

Full Text

The Full Text of this article is available as a PDF (618K).

Selected References

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

Ammerer G, Hunter CP, Rothman JH, Saari GC, Valls LA, Stevens TH. PEP4 gene of Saccharomyces cerevisiae encodes proteinase A, a vacuolar enzyme required for processing of vacuolar precursors. Mol Cell Biol. 1986 Jul;6(7):2490–2499. [PMC free article] [PubMed] [Google Scholar]
Bachhawat AK, Suhan J, Jones EW. The yeast homolog of H < beta > 58, a mouse gene essential for embryogenesis, performs a role in the delivery of proteins to the vacuole. Genes Dev. 1994 Jun 15;8(12):1379–1387. [PubMed] [Google Scholar]
Bosshart H, Humphrey J, Deignan E, Davidson J, Drazba J, Yuan L, Oorschot V, Peters PJ, Bonifacino JS. The cytoplasmic domain mediates localization of furin to the trans-Golgi network en route to the endosomal/lysosomal system. J Cell Biol. 1994 Sep;126(5):1157–1172. [PMC free article] [PubMed] [Google Scholar]
Canfield WM, Johnson KF, Ye RD, Gregory W, Kornfeld S. Localization of the signal for rapid internalization of the bovine cation-independent mannose 6-phosphate/insulin-like growth factor-II receptor to amino acids 24-29 of the cytoplasmic tail. J Biol Chem. 1991 Mar 25;266(9):5682–5688. [PubMed] [Google Scholar]
Cereghino JL, Marcusson EG, Emr SD. The cytoplasmic tail domain of the vacuolar protein sorting receptor Vps10p and a subset of VPS gene products regulate receptor stability, function, and localization. Mol Biol Cell. 1995 Sep;6(9):1089–1102. [PMC free article] [PubMed] [Google Scholar]
Chapman RE, Munro S. The functioning of the yeast Golgi apparatus requires an ER protein encoded by ANP1, a member of a new family of genes affecting the secretory pathway. EMBO J. 1994 Oct 17;13(20):4896–4907. [PMC free article] [PubMed] [Google Scholar]
Conibear E, Stevens TH. Vacuolar biogenesis in yeast: sorting out the sorting proteins. Cell. 1995 Nov 17;83(4):513–516. [PubMed] [Google Scholar]
Cooper A, Bussey H. Yeast Kex1p is a Golgi-associated membrane protein: deletions in a cytoplasmic targeting domain result in mislocalization to the vacuolar membrane. J Cell Biol. 1992 Dec;119(6):1459–1468. [PMC free article] [PubMed] [Google Scholar]
Damke H, Baba T, Warnock DE, Schmid SL. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol. 1994 Nov;127(4):915–934. [PMC free article] [PubMed] [Google Scholar]
Davis NG, Horecka JL, Sprague GF., Jr Cis- and trans-acting functions required for endocytosis of the yeast pheromone receptors. J Cell Biol. 1993 Jul;122(1):53–65. [PMC free article] [PubMed] [Google Scholar]
Fuller RS, Brake AJ, Thorner J. Intracellular targeting and structural conservation of a prohormone-processing endoprotease. Science. 1989 Oct 27;246(4929):482–486. [PubMed] [Google Scholar]
Fuller RS, Sterne RE, Thorner J. Enzymes required for yeast prohormone processing. Annu Rev Physiol. 1988;50:345–362. [PubMed] [Google Scholar]
Graham TR, Seeger M, Payne GS, MacKay VL, Emr SD. Clathrin-dependent localization of alpha 1,3 mannosyltransferase to the Golgi complex of Saccharomyces cerevisiae. J Cell Biol. 1994 Nov;127(3):667–678. [PMC free article] [PubMed] [Google Scholar]
Graham TR, Emr SD. 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):207–218. [PMC free article] [PubMed] [Google Scholar]
Graham TR, Krasnov VA. Sorting of yeast alpha 1,3 mannosyltransferase is mediated by a lumenal domain interaction, and a transmembrane domain signal that can confer clathrin-dependent Golgi localization to a secreted protein. Mol Biol Cell. 1995 Jul;6(7):809–824. [PMC free article] [PubMed] [Google Scholar]
Horazdovsky BF, DeWald DB, Emr SD. Protein transport to the yeast vacuole. Curr Opin Cell Biol. 1995 Aug;7(4):544–551. [PubMed] [Google Scholar]
Kornfeld S. Structure and function of the mannose 6-phosphate/insulinlike growth factor II receptors. Annu Rev Biochem. 1992;61:307–330. [PubMed] [Google Scholar]
Lawrence CW. Classical mutagenesis techniques. Methods Enzymol. 1991;194:273–281. [PubMed] [Google Scholar]
Lewis MJ, Pelham HR. Ligand-induced redistribution of a human KDEL receptor from the Golgi complex to the endoplasmic reticulum. Cell. 1992 Jan 24;68(2):353–364. [PubMed] [Google Scholar]
Lewis MJ, Sweet DJ, Pelham HR. The ERD2 gene determines the specificity of the luminal ER protein retention system. Cell. 1990 Jun 29;61(7):1359–1363. [PubMed] [Google Scholar]
Machamer CE. Targeting and retention of Golgi membrane proteins. Curr Opin Cell Biol. 1993 Aug;5(4):606–612. [PMC free article] [PubMed] [Google Scholar]
Marcusson EG, Horazdovsky BF, Cereghino JL, Gharakhanian E, Emr SD. The sorting receptor for yeast vacuolar carboxypeptidase Y is encoded by the VPS10 gene. Cell. 1994 May 20;77(4):579–586. [PubMed] [Google Scholar]
Marusich MF. Efficient hybridoma production using previously frozen splenocytes. J Immunol Methods. 1988 Nov 10;114(1-2):155–159. [PubMed] [Google Scholar]
Mitchell JK, Fonzi WA, Wilkerson J, Opheim DJ. A particulate form of alkaline phosphatase in the yeast, Saccharomyces cerevisiae. Biochim Biophys Acta. 1981 Feb 13;657(2):482–494. [PubMed] [Google Scholar]
Nilsson T, Slusarewicz P, Hoe MH, Warren G. Kin recognition. A model for the retention of Golgi enzymes. FEBS Lett. 1993 Sep 6;330(1):1–4. [PubMed] [Google Scholar]
Nothwehr SF, Conibear E, Stevens TH. Golgi and vacuolar membrane proteins reach the vacuole in vps1 mutant yeast cells via the plasma membrane. J Cell Biol. 1995 Apr;129(1):35–46. [PMC free article] [PubMed] [Google Scholar]
Nothwehr SF, Roberts CJ, Stevens TH. Membrane protein retention in the yeast Golgi apparatus: dipeptidyl aminopeptidase A is retained by a cytoplasmic signal containing aromatic residues. J Cell Biol. 1993 Jun;121(6):1197–1209. [PMC free article] [PubMed] [Google Scholar]
Nothwehr SF, Stevens TH. Sorting of membrane proteins in the yeast secretory pathway. J Biol Chem. 1994 Apr 8;269(14):10185–10188. [PubMed] [Google Scholar]
Payne GS, Schekman R. Clathrin: a role in the intracellular retention of a Golgi membrane protein. Science. 1989 Sep 22;245(4924):1358–1365. [PubMed] [Google Scholar]
Pearse BM, Robinson MS. Clathrin, adaptors, and sorting. Annu Rev Cell Biol. 1990;6:151–171. [PubMed] [Google Scholar]
Pelham HR. The retention signal for soluble proteins of the endoplasmic reticulum. Trends Biochem Sci. 1990 Dec;15(12):483–486. [PubMed] [Google Scholar]
Pelham HR, Munro S. Sorting of membrane proteins in the secretory pathway. Cell. 1993 Nov 19;75(4):603–605. [PMC free article] [PubMed] [Google Scholar]
Piper RC, Cooper AA, Yang H, Stevens TH. VPS27 controls vacuolar and endocytic traffic through a prevacuolar compartment in Saccharomyces cerevisiae. J Cell Biol. 1995 Nov;131(3):603–617. [PMC free article] [PubMed] [Google Scholar]
Piper RC, Whitters EA, Stevens TH. Yeast Vps45p is a Sec1p-like protein required for the consumption of vacuole-targeted, post-Golgi transport vesicles. Eur J Cell Biol. 1994 Dec;65(2):305–318. [PubMed] [Google Scholar]
Raymond CK, Howald-Stevenson I, Vater CA, Stevens TH. Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol Biol Cell. 1992 Dec;3(12):1389–1402. [PMC free article] [PubMed] [Google Scholar]
Raymond CK, Roberts CJ, Moore KE, Howald I, Stevens TH. Biogenesis of the vacuole in Saccharomyces cerevisiae. Int Rev Cytol. 1992;139:59–120. [PubMed] [Google Scholar]
Redding K, Holcomb C, Fuller RS. Immunolocalization of Kex2 protease identifies a putative late Golgi compartment in the yeast Saccharomyces cerevisiae. J Cell Biol. 1991 May;113(3):527–538. [PMC free article] [PubMed] [Google Scholar]
Roberts CJ, Nothwehr SF, Stevens TH. Membrane protein sorting in the yeast secretory pathway: evidence that the vacuole may be the default compartment. J Cell Biol. 1992 Oct;119(1):69–83. [PMC free article] [PubMed] [Google Scholar]
Roberts CJ, Raymond CK, Yamashiro CT, Stevens TH. Methods for studying the yeast vacuole. Methods Enzymol. 1991;194:644–661. [PubMed] [Google Scholar]
Rothman JE. Mechanisms of intracellular protein transport. Nature. 1994 Nov 3;372(6501):55–63. [PubMed] [Google Scholar]
Seeger M, Payne GS. Selective and immediate effects of clathrin heavy chain mutations on Golgi membrane protein retention in Saccharomyces cerevisiae. J Cell Biol. 1992 Aug;118(3):531–540. [PMC free article] [PubMed] [Google Scholar]
Semenza JC, Hardwick KG, Dean N, Pelham HR. ERD2, a yeast gene required for the receptor-mediated retrieval of luminal ER proteins from the secretory pathway. Cell. 1990 Jun 29;61(7):1349–1357. [PubMed] [Google Scholar]
Sikorski RS, Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. [PMC free article] [PubMed] [Google Scholar]
Stanley KK, Howell KE. TGN38/41: a molecule on the move. Trends Cell Biol. 1993 Aug;3(8):252–255. [PubMed] [Google Scholar]
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] [Google Scholar]
Toh-E A, Nakamura H, Oshima Y. A gene controlling the synthesis of non specific alkaline phosphatase in Saccharomyces cerevisiae. Biochim Biophys Acta. 1976 Mar 25;428(1):182–192. [PubMed] [Google Scholar]
Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. [PMC free article] [PubMed] [Google Scholar]
Townsley FM, Wilson DW, Pelham HR. Mutational analysis of the human KDEL receptor: distinct structural requirements for Golgi retention, ligand binding and retrograde transport. EMBO J. 1993 Jul;12(7):2821–2829. [PMC free article] [PubMed] [Google Scholar]
Trowbridge IS. Endocytosis and signals for internalization. Curr Opin Cell Biol. 1991 Aug;3(4):634–641. [PubMed] [Google Scholar]
Weisz OA, Swift AM, Machamer CE. Oligomerization of a membrane protein correlates with its retention in the Golgi complex. J Cell Biol. 1993 Sep;122(6):1185–1196. [PMC free article] [PubMed] [Google Scholar]
Wilcox CA, Redding K, Wright R, Fuller RS. Mutation of a tyrosine localization signal in the cytosolic tail of yeast Kex2 protease disrupts Golgi retention and results in default transport to the vacuole. Mol Biol Cell. 1992 Dec;3(12):1353–1371. [PMC free article] [PubMed] [Google Scholar]
Wilsbach K, Payne GS. Vps1p, a member of the dynamin GTPase family, is necessary for Golgi membrane protein retention in Saccharomyces cerevisiae. EMBO J. 1993 Aug;12(8):3049–3059. [PMC free article] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis