Membrane protein retention in the yeast Golgi apparatus: dipeptidyl aminopeptidase A is retained by a cytoplasmic signal containing aromatic residues

doi:10.1083/jcb.121.6.1197

This Article

	Full Text (PDF, 2700K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Nothwehr, S. F.
	Articles by Stevens, T. H.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Nothwehr, S. F.
	Articles by Stevens, T. H.


Social Bookmarking

	What's this?

ARTICLES

Membrane protein retention in the yeast Golgi apparatus: dipeptidyl aminopeptidase A is retained by a cytoplasmic signal containing aromatic residues

SF Nothwehr, CJ Roberts and TH Stevens
Institute of Molecular Biology, University of Oregon, Eugene 97403.

The mechanism by which yeast dipeptidyl aminopeptidase (DPAP) A, type II integral membrane protein, is retained in the late Golgi apparatus has been investigated. Prior work demonstrated that the 118-amino acid cytoplasmic domain is both necessary and sufficient for Golgi retention and that mutant or overexpressed DPAP A no longer retained in the Golgi was delivered directly to the vacuolar membrane (Roberts, C. J., S. F. Nothwehr, and T. H. Stevens. 1992. J. Cell Biol. 119:69-83). Replacement of the DPAP A transmembrane domain with a synthetic hydrophobic sequence did not affect either Golgi retention of DPAP A or vacuolar delivery of the retention-defective form of DPAP A. These results indicate that the DPAP A transmembrane domain is not involved in either Golgi retention or targeting of this membrane protein. A detailed mutational analysis of the cytoplasmic domain of DPAP A indicated that the most important elements for retention were within the eight residue stretch 85-92. A 10-amino acid region from DPAP A (81- 90) was sufficient for Golgi retention of alkaline phosphatase, a type II vacuolar membrane protein. Detailed mutational analysis within this 10-amino acid sufficient region demonstrated that a Phe-X-Phe-X-Asp motif was absolutely required for efficient retention. The efficiency of Golgi retention via the DPAP A signal could be diminished by overexpression of wild type but not retention-defective versions of Kex2p, another late Golgi membrane protein, suggesting that multiple Golgi membrane proteins may be retained by a common machinery. These results imply a role for a cytoplasmic signal involving aromatic residues in retention of late Golgi membrane proteins in the yeast Saccharomyces cerevisiae.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Dunkel, M., Latz, A., Schumacher, K., Muller, T., Becker, D., Hedrich, R. (2008). Targeting of Vacuolar Membrane Localized Members of the TPK Channel Family. Mol Plant 1: 938-949 [Abstract] [Full Text]
Chidambaram, S., Zimmermann, J., von Mollard, G. F. (2008). ENTH domain proteins are cargo adaptors for multiple SNARE proteins at the TGN endosome. J. Cell Sci. 121: 329-338 [Abstract] [Full Text]
Copic, A., Starr, T. L., Schekman, R. (2007). Ent3p and Ent5p Exhibit Cargo-specific Functions in Trafficking Proteins between the Trans-Golgi Network and the Endosomes in Yeast. Mol. Biol. Cell 18: 1803-1815 [Abstract] [Full Text]
Liu, K., Hua, Z., Nepute, J. A., Graham, T. R. (2007). Yeast P4-ATPases Drs2p and Dnf1p Are Essential Cargos of the NPFXD/Sla1p Endocytic Pathway. Mol. Biol. Cell 18: 487-500 [Abstract] [Full Text]
Foote, C., Nothwehr, S. F. (2006). The clathrin adaptor complex 1 directly binds to a sorting signal in Ste13p to reduce the rate of its trafficking to the late endosome of yeast. JCB 173: 615-626 [Abstract] [Full Text]
Iwaki, T., Hosomi, A., Tokudomi, S., Kusunoki, Y., Fujita, Y., Giga-Hama, Y., Tanaka, N., Takegawa, K. (2006). Vacuolar protein sorting receptor in Schizosaccharomyces pombe.. Microbiology 152: 1523-1532 [Abstract] [Full Text]
Oliviusson, P., Heinzerling, O., Hillmer, S., Hinz, G., Tse, Y. C., Jiang, L., Robinson, D. G. (2006). Plant Retromer, Localized to the Prevacuolar Compartment and Microvesicles in Arabidopsis, May Interact with Vacuolar Sorting Receptors. Plant Cell 18: 1239-1252 [Abstract] [Full Text]
Cai, H., Zhang, Y., Pypaert, M., Walker, L., Ferro-Novick, S. (2005). Mutants in trs120 disrupt traffic from the early endosome to the late Golgi. JCB 171: 823-833 [Abstract] [Full Text]
Krsmanovic, T., Pawelec, A., Sydor, T., Kolling, R. (2005). Control of Ste6 Recycling by Ubiquitination in the Early Endocytic Pathway in Yeast. Mol. Biol. Cell 16: 2809-2821 [Abstract] [Full Text]
Johnston, H. D., Foote, C., Santeford, A., Nothwehr, S. F. (2005). Golgi-to-Late Endosome Trafficking of the Yeast Pheromone Processing Enzyme Ste13p Is Regulated by a Phosphorylation Site in its Cytosolic Domain. Mol. Biol. Cell 16: 1456-1468 [Abstract] [Full Text]
Abazeed, M. E., Blanchette, J. M., Fuller, R. S. (2005). Cell-free Transport from the trans-Golgi Network to Late Endosome Requires Factors Involved in Formation and Consumption of Clathrin-coated Vesicles. J. Biol. Chem. 280: 4442-4450 [Abstract] [Full Text]
Blanchette, J. M., Abazeed, M. E., Fuller, R. S. (2004). Cell-free Reconstitution of Transport from the trans-Golgi Network to the Late Endosome/Prevacuolar Compartment. J. Biol. Chem. 279: 48767-48773 [Abstract] [Full Text]
Bruinsma, P., Spelbrink, R. G., Nothwehr, S. F. (2004). Retrograde Transport of the Mannosyltransferase Och1p to the Early Golgi Requires a Component of the COG Transport Complex. J. Biol. Chem. 279: 39814-39823 [Abstract] [Full Text]
Sipos, G., Brickner, J. H., Brace, E.J., Chen, L., Rambourg, A., Kepes, F., Fuller, R. S. (2004). Soi3p/Rav1p Functions at the Early Endosome to Regulate Endocytic Trafficking to the Vacuole and Localization of Trans-Golgi Network Transmembrane Proteins. Mol. Biol. Cell 15: 3196-3209 [Abstract] [Full Text]
Chidambaram, S., Mullers, N., Wiederhold, K., Haucke, V., von Mollard, G. F. (2004). Specific Interaction between SNAREs and Epsin N-terminal Homology (ENTH) Domains of Epsin-related Proteins in trans-Golgi Network to Endosome Transport. J. Biol. Chem. 279: 4175-4179 [Abstract] [Full Text]
Zhou, C.-Z., Li de La Sierra-Gallay, I., Quevillon-Cheruel, S., Collinet, B., Minard, P., Blondeau, K., Henckes, G., Aufrere, R., Leulliot, N., Graille, M., Sorel, I., Savarin, P., de la Torre, F., Poupon, A., Janin, J., van Tilbeurgh, H. (2003). Crystal Structure of the Yeast Phox Homology (PX) Domain Protein Grd19p Complexed to Phosphatidylinositol-3-phosphate. J. Biol. Chem. 278: 50371-50376 [Abstract] [Full Text]
Watanabe, S., Imai, M., Ohara, Y., Odagiri, T. (2003). Influenza B Virus BM2 Protein Is Transported through the trans-Golgi Network as an Integral Membrane Protein. J. Virol. 77: 10630-10637 [Abstract] [Full Text]
Kweon, Y., Rothe, A., Conibear, E., Stevens, T. H. (2003). Ykt6p Is a Multifunctional Yeast R-SNARE That Is Required for Multiple Membrane Transport Pathways to the Vacuole. Mol. Biol. Cell 14: 1868-1881 [Abstract] [Full Text]
Ha, S.-A., Torabinejad, J., DeWald, D. B., Wenk, M. R., Lucast, L., De Camilli, P., Newitt, R. A., Aebersold, R., Nothwehr, S. F. (2003). The Synaptojanin-like Protein Inp53/Sjl3 Functions with Clathrin in a Yeast TGN-to-Endosome Pathway Distinct from the GGA Protein-dependent Pathway. Mol. Biol. Cell 14: 1319-1333 [Abstract] [Full Text]
Deloche, O., Schekman, R. W. (2002). Vps10p Cycles between the TGN and the Late Endosome via the Plasma Membrane in Clathrin Mutants. Mol. Biol. Cell 13: 4296-4307 [Abstract] [Full Text]
Brickner, J. H., Blanchette, J. M., Sipos, G., Fuller, R. S. (2001). The Tlg SNARE complex is required for TGN homotypic fusion. JCB 155: 969-978 [Abstract] [Full Text]
Kawasaki-Nishi, S., Bowers, K., Nishi, T., Forgac, M., Stevens, T. H. (2001). The Amino-terminal Domain of the Vacuolar Proton-translocating ATPase a Subunit Controls Targeting and in Vivo Dissociation, and the Carboxyl-terminal Domain Affects Coupling of Proton Transport and ATP Hydrolysis. J. Biol. Chem. 276: 47411-47420 [Abstract] [Full Text]
Ha, S.-A., Bunch, J. T., Hama, H., DeWald, D. B., Nothwehr, S. F. (2001). A Novel Mechanism for Localizing Membrane Proteins to Yeast Trans-Golgi Network Requires Function of Synaptojanin-like Protein. Mol. Biol. Cell 12: 3175-3190 [Abstract] [Full Text]
Bensen, E. S., Yeung, B. G., Payne, G. S. (2001). Ric1p and the Ypt6p GTPase Function in a Common Pathway Required for Localization of Trans-Golgi Network Membrane Proteins. Mol. Biol. Cell 12: 13-26 [Abstract] [Full Text]
Bowers, K., Levi, B. P., Patel, F. I., Stevens, T. H. (2000). The Sodium/Proton Exchanger Nhx1p Is Required for Endosomal Protein Trafficking in the Yeast Saccharomyces cerevisiae. Mol. Biol. Cell 11: 4277-4294 [Abstract] [Full Text]
Nothwehr, S. F., Ha, S.-A., Bruinsma, P. (2000). Sorting of Yeast Membrane Proteins into an Endosome-to-Golgi Pathway Involves Direct Interaction of Their Cytosolic Domains with Vps35p. JCB 151: 297-310 [Abstract] [Full Text]
Panek, H., Conibear, E, Bryan, J., Colvin, R., Goshorn, C., Robinson, L. (2000). Identification of Rgp1p, a novel Golgi recycling factor, as a protein required for efficient localization of yeast casein kinase 1 to the plasma membrane. J. Cell Sci. 113: 4545-4555 [Abstract]
Conibear, E., Stevens, T. H. (2000). Vps52p, Vps53p, and Vps54p Form a Novel Multisubunit Complex Required for Protein Sorting at the Yeast Late Golgi. Mol. Biol. Cell 11: 305-323 [Abstract] [Full Text]
Urbanowski, J. L., Piper, R. C. (1999). The Iron Transporter Fth1p Forms a Complex with the Fet5 Iron Oxidase and Resides on the Vacuolar Membrane. J. Biol. Chem. 274: 38061-38070 [Abstract] [Full Text]
Spelbrink, R. G., Nothwehr, S. F. (1999). The Yeast GRD20 Gene Is Required for Protein Sorting in the trans-Golgi Network/Endosomal System and for Polarization of the Actin Cytoskeleton. Mol. Biol. Cell 10: 4263-4281 [Abstract] [Full Text]
Zheng, H., von Mollard, G. F., Kovaleva, V., Stevens, T. H., Raikhel, N. V. (1999). The Plant Vesicle-associated SNARE AtVTI1a Likely Mediates Vesicle Transport from the Trans-Golgi Network to the Prevacuolar Compartment. Mol. Biol. Cell 10: 2251-2264 [Abstract] [Full Text]
von Mollard, G. F., Stevens, T. H. (1999). The Saccharomyces cerevisiae v-SNARE Vti1p Is Required for Multiple Membrane Transport Pathways to the Vacuole. Mol. Biol. Cell 10: 1719-1732 [Abstract] [Full Text]
Nothwehr, S. F., Bruinsma, P., Strawn, L. A. (1999). Distinct Domains within Vps35p Mediate the Retrieval of Two Different Cargo Proteins from the Yeast Prevacuolar/Endosomal Compartment. Mol. Biol. Cell 10: 875-890 [Abstract] [Full Text]
Jiang, L., Rogers, J. C. (1998). Integral Membrane Protein Sorting to Vacuoles in Plant Cells: Evidence for Two Pathways. JCB 143: 1183-1199 [Abstract] [Full Text]
Bryant, N. J., Piper, R. C., Weisman, L. S., Stevens, T. H. (1998). Retrograde Traffic Out of the Yeast Vacuole to the TGN Occurs via the Prevacuolar/Endosomal Compartment. JCB 142: 651-663 [Abstract] [Full Text]
Vowels, J. J., Payne, G. S. (1998). A Role for the Lumenal Domain in Golgi Localization of the Saccharomyces cerevisiae Guanosine Diphosphatase. Mol. Biol. Cell 9: 1351-1365 [Abstract] [Full Text]
Voos, W., Stevens, T. H. (1998). Retrieval of Resident Late-Golgi Membrane Proteins from the Prevacuolar Compartment of Saccharomyces cerevisiae Is Dependent on the Function of Grd19p. JCB 140: 577-590 [Abstract] [Full Text]
Lupashin, V. V., Pokrovskaya, I. D., McNew, J. A., Waters, M. G. (1997). Characterization of a Novel Yeast SNARE Protein Implicated in Golgi Retrograde Traffic. Mol. Biol. Cell 8: 2659-2676 [Abstract] [Full Text]
Brickner, J. H., Fuller, R. S. (1997). SOI1 Encodes a Novel, Conserved Protein That Promotes TGN-Endosomal Cycling of Kex2p and Other Membrane Proteins by Modulating the Function of Two TGN Localization Signals. JCB 139: 23-36 [Abstract] [Full Text]
Luo, W.-j., Chang, A. (1997). Novel Genes Involved in Endosomal Traffic in Yeast Revealed by Suppression of a Targeting-defective Plasma Membrane ATPase Mutant. JCB 138: 731-746 [Abstract] [Full Text]
Piper, R. C., Bryant, N. J., Stevens, T. H. (1997). The Membrane Protein Alkaline Phosphatase Is Delivered to the Vacuole by a Route That Is Distinct from the VPS-dependent Pathway. JCB 138: 531-545 [Abstract] [Full Text]
Berninsone, P., Eckhardt, M., Gerardy-Schahn, R., Hirschberg, C. B. (1997). Functional Expression of the Murine Golgi CMP-Sialic Acid Transporter in Saccharomyces cerevisiae. J. Biol. Chem. 272: 12616-12619 [Abstract] [Full Text]
Bryant, N. J., Stevens, T. H. (1997). Two Separate Signals Act Independently to Localize a Yeast Late Golgi Membrane Protein through a Combination of Retrieval and Retention. JCB 136: 287-297 [Abstract] [Full Text]
Nothwehr, S., Hindes, A. (1997). The yeast VPS5/GRD2 gene encodes a sorting nexin-1-like protein required for localizing membrane proteins to the late Golgi. J. Cell Sci. 110: 1063-1072 [Abstract]
Knight, S A, Labbe, S, Kwon, L F, Kosman, D J, Thiele, D J (1996). A widespread transposable element masks expression of a yeast copper transport gene.. Genes Dev. 10: 1917-1929 [Abstract]
Schwientek, T., Narimatsu, H., Ernst, J. F. (1996). Golgi Localization and in Vivo Activity of a Mammalian Glycosyltransferase (Human beta1,4-Galactosyltransferase) in Yeast. J. Biol. Chem. 271: 3398-3405 [Abstract] [Full Text]
Schwientek, T., Lorenz, C., Ernst, J. F. (1995). Golgi Localization in Yeast Is Mediated by the Membrane Anchor Region of Rat Liver Sialyltransferase. J. Biol. Chem. 270: 5483-5489 [Abstract] [Full Text]
Morano, K., Klionsky, D. (1994). Differential effects of compartment deacidification on the targeting of membrane and soluble proteins to the vacuole in yeast. J. Cell Sci. 107: 2813-2824 [Abstract]
Dilcher, M., Kohler, B., von Mollard, G. F. (2001). Genetic Interactions with the Yeast Q-SNARE VTI1 Reveal Novel Functions for the R-SNARE YKT6. J. Biol. Chem. 276: 34537-34544 [Abstract] [Full Text]
Poon, P. P., Nothwehr, S. F., Singer, R. A., Johnston, G. C. (2001). The Gcs1 and Age2 ArfGAP proteins provide overlapping essential function for transport from the yeast trans-Golgi network. JCB 155: 1239-1250 [Abstract] [Full Text]