Endoplasmic reticulum localization of Sec12p is achieved by two mechanisms: Rer1p-dependent retrieval that requires the transmembrane domain and Rer1p-independent retention that involves the cytoplasmic domain

doi:10.1083/jcb.134.2.279

This Article

Full Text (PDF, 3710K)

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 Sato, M.

Articles by Nakano, A.

Search for Related Content

PubMed

PubMed Citation

Articles by Sato, M.

Articles by Nakano, A.

Pubmed/NCBI databases

Gene	GEO Profiles
HomoloGene	Protein
Compound via MeSH
Substance via MeSH

Social Bookmarking

What's this?

ARTICLES

Endoplasmic reticulum localization of Sec12p is achieved by two mechanisms: Rer1p-dependent retrieval that requires the transmembrane domain and Rer1p-independent retention that involves the cytoplasmic domain

M Sato, K Sato and A Nakano
Department of Biological Sciences, Graduate School of Science, University of Tokyo, Japan.

Yeast Sec12p is a type II transmembrane protein in the ER, which is essential for the formation of transport vesicles. From biochemical and morphological lines of evidence, we have proposed that Sec12p is localized to the ER by two mechanisms: static retention in the ER and dynamic retrieval from the early Golgi compartment. We have also shown that Rer1p, a membrane protein in the Golgi, is required for correct localization of Sec12p. In the present study, we have performed a systematic analysis to determine the ER localization signals in Sec12p corresponding to these two mechanisms. Both the transmembrane domain (TMD) and the NH2-terminal cytoplasmic domain of Sec12p show the ability to localize the protein to the ER. The effect of the TMD is potent and sufficient by itself for the ER localization and is strongly dependent on Rer1p. On the other hand, the cytoplasmic domain shows a moderate ER-localization capability which is independent of Rer1p. The rate of mannosyl modification has been measured to distinguish between retention and retrieval. The cytoplasmic domain significantly delays the transport from the ER to the cis-Golgi. In contrast, the TMD shows only a subtle retardation in the transport from the ER to the cis-Golgi but strictly prevents the transport beyond there. From these observations, we conclude that the TMD mainly acts as the retrieval signal and the cytoplasmic domain contains the retention signal. This study not only supports the two-mechanisms hypothesis but also provides powerful tools to dissect the two.
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:

Mitsui, K., Hatakeyama, K., Matsushita, M., Kanazawa, H. (2009). Saccharomyces cerevisiae Na+/H+ Antiporter Nha1p Associates with Lipid Rafts and Requires Sphingolipid for Stable Localization to the Plasma Membrane. J Biochem 145: 709-720 [Abstract] [Full Text]
Murakami-Sekimata, A., Sato, K., Sato, K., Takashima, A., Nakano, A. (2009). O-Mannosylation is required for the solubilization of heterologously expressed human beta-amyloid precursor protein in Saccharomyces cerevisiae.. GENES CELLS 14: 205-215 [Abstract] [Full Text]
Mukhopadhyay, D., Howell, K. S., Riezman, H., Capitani, G. (2008). Identifying Key Residues of Sphinganine-1-phosphate Lyase for Function in Vivo and in Vitro. J. Biol. Chem. 283: 20159-20169 [Abstract] [Full Text]
Loewen, C. J.R., Young, B. P., Tavassoli, S., Levine, T. P. (2007). Inheritance of cortical ER in yeast is required for normal septin organization. JCB 179: 467-483 [Abstract] [Full Text]
Huang, J., Reggiori, F., Klionsky, D. J. (2007). The Transmembrane Domain of Acid Trehalase Mediates Ubiquitin-independent Multivesicular Body Pathway Sorting. Mol. Biol. Cell 18: 2511-2524 [Abstract] [Full Text]
Spasic, D., Raemaekers, T., Dillen, K., Declerck, I., Baert, V., Serneels, L., Fullekrug, J., Annaert, W. (2007). Rer1p competes with APH-1 for binding to nicastrin and regulates {gamma}-secretase complex assembly in the early secretory pathway. JCB 176: 629-640 [Abstract] [Full Text]
Nishiya, T., Kajita, E., Miwa, S., DeFranco, A. L. (2005). TLR3 and TLR7 Are Targeted to the Same Intracellular Compartments by Distinct Regulatory Elements. J. Biol. Chem. 280: 37107-37117 [Abstract] [Full Text]
Hernandez, D. H., Paris, N., Neuhaus, J.-M., Deloche, O. (2005). The Yeast Saccharomyces cerevisiae Is Not an Efficient Tool for in Vivo Studies of Plant Vacuolar Sorting Receptors. Plant Cell 17: 1339-1342 [Full Text]
Kim, J., Hamamoto, S., Ravazzola, M., Orci, L., Schekman, R. (2005). Uncoupled Packaging of Amyloid Precursor Protein and Presenilin 1 into Coat Protein Complex II Vesicles. J. Biol. Chem. 280: 7758-7768 [Abstract] [Full Text]
Sato, K. (2004). COPII Coat Assembly and Selective Export from the Endoplasmic Reticulum. J Biochem 136: 755-760 [Abstract] [Full Text]
Hama, E., Shirotani, K., Iwata, N., Saido, T. C. (2004). Effects of Neprilysin Chimeric Proteins Targeted to Subcellular Compartments on Amyloid {beta} Peptide Clearance in Primary Neurons. J. Biol. Chem. 279: 30259-30264 [Abstract] [Full Text]
Parker, A. K. T., Gergely, F. V., Taylor, C. W. (2004). Targeting of Inositol 1,4,5-Trisphosphate Receptors to the Endoplasmic Reticulum by Multiple Signals within Their Transmembrane Domains. J. Biol. Chem. 279: 23797-23805 [Abstract] [Full Text]
Sato, M., Sato, K., Nakano, A. (2004). Endoplasmic Reticulum Quality Control of Unassembled Iron Transporter Depends on Rer1p-mediated Retrieval from the Golgi. Mol. Biol. Cell 15: 1417-1424 [Abstract] [Full Text]
Sasanami, T., Hanafy, A. M., Toriyama, M., Mori, M. (2003). Variant of Perivitelline Membrane Glycoprotein ZPC of Japanese Quail (Coturnix japonica) Lacking Its Cytoplasmic Tail Exhibits the Retention in the Endoplasmic Reticulum of Chinese Hamster Ovary (CHO-K1) Cells. Biol. Reprod. 69: 1401-1407 [Abstract] [Full Text]
Sato, K., Sato, M., Nakano, A. (2003). Rer1p, a Retrieval Receptor for ER Membrane Proteins, Recognizes Transmembrane Domains in Multiple Modes. Mol. Biol. Cell 14: 3605-3616 [Abstract] [Full Text]
Umebayashi, K., Nakano, A. (2003). Ergosterol is required for targeting of tryptophan permease to the yeast plasma membrane. JCB 161: 1117-1131 [Abstract] [Full Text]
Nakamura-Kubo, M., Nakamura, T., Hirata, A., Shimoda, C. (2003). The Fission Yeast spo14+ Gene Encoding a Functional Homologue of Budding Yeast Sec12 Is Required for the Development of Forespore Membranes. Mol. Biol. Cell 14: 1109-1124 [Abstract] [Full Text]
Supek, F., Madden, D. T., Hamamoto, S., Orci, L., Schekman, R. (2002). Sec16p potentiates the action of COPII proteins to bud transport vesicles. JCB 158: 1029-1038 [Abstract] [Full Text]
Massaad, M. J., Herscovics, A. (2002). Interaction of the endoplasmic reticulum {alpha}1,2-mannosidase Mns1p with Rer1p using the split-ubiquitin system. J. Cell Sci. 114: 4629-4635 [Abstract] [Full Text]
Charloteaux, B., Lins, L., Moereels, H., Brasseur, R. (2002). Analysis of the C-Terminal Membrane Anchor Domains of Hepatitis C Virus Glycoproteins E1 and E2: toward a Topological Model. J. Virol. 76: 1944-1958 [Abstract] [Full Text]
Belden, W. J., Barlowe, C. (2001). Distinct Roles for the Cytoplasmic Tail Sequences of Emp24p and Erv25p in Transport between the Endoplasmic Reticulum and Golgi Complex. J. Biol. Chem. 276: 43040-43048 [Abstract] [Full Text]
Belden, W. J., Barlowe, C. (2001). Deletion of Yeast p24 Genes Activates the Unfolded Protein Response. Mol. Biol. Cell 12: 957-969 [Abstract] [Full Text]
Sato, K., Sato, M., Nakano, A. (2001). Rer1p, a Retrieval Receptor for Endoplasmic Reticulum Membrane Proteins, Is Dynamically Localized to the Golgi Apparatus by Coatomer. JCB 152: 935-944 [Abstract] [Full Text]
Reggiori, F., Black, M. W., Pelham, H. R. B. (2000). Polar Transmembrane Domains Target Proteins to the Interior of the Yeast Vacuole. Mol. Biol. Cell 11: 3737-3749 [Abstract] [Full Text]
Pedrazzini, E., Villa, A., Longhi, R., Bulbarelli, A., Borgese, N. (2000). Mechanism of Residence of Cytochrome B(5), a Tail-Anchored Protein, in the Endoplasmic Reticulum. JCB 148: 899-914 [Abstract] [Full Text]
Watson, R. T., Pessin, J. E. (2000). Functional Cooperation of Two Independent Targeting Domains in Syntaxin 6 Is Required for Its Efficient Localization in the trans-Golgi Network of 3T3L1 Adipocytes. J. Biol. Chem. 275: 1261-1268 [Abstract] [Full Text]
Lewis, M. J., Nichols, B. J., Prescianotto-Baschong, C., Riezman, H., Pelham, H. R. B. (2000). Specific Retrieval of the Exocytic SNARE Snc1p from Early Yeast Endosomes. Mol. Biol. Cell 11: 23-38 [Abstract] [Full Text]
Vos, J. C., Spee, P., Momburg, F., Neefjes, J. (1999). Membrane Topology and Dimerization of the Two Subunits of the Transporter Associated with Antigen Processing Reveal a Three-Domain Structure. J. Immunol. 163: 6679-6685 [Abstract] [Full Text]
Cai, Y., Maeda, Y., Cedzich, A., Torres, V. E., Wu, G., Hayashi, T., Mochizuki, T., Park, J. H., Witzgall, R., Somlo, S. (1999). Identification and Characterization of Polycystin-2, the PKD2 Gene Product. J. Biol. Chem. 274: 28557-28565 [Abstract] [Full Text]
Sherwood, P. W., Carlson, M. (1999). Efficient export of the glucose transporter Hxt1p from the endoplasmic reticulum requires Gsf2p. Proc. Natl. Acad. Sci. USA 96: 7415-7420 [Abstract] [Full Text]
Kato, J.-i., Fujisaki, S., Nakajima, K.-i., Nishimura, Y., Sato, M., Nakano, A. (1999). The Escherichia coli Homologue of Yeast Rer2, a Key Enzyme of Dolichol Synthesis, Is Essential for Carrier Lipid Formation in Bacterial Cell Wall Synthesis. J. Bacteriol. 181: 2733-2738 [Abstract] [Full Text]
Greenfield, J., High, S (1999). The Sec61 complex is located in both the ER and the ER-Golgi intermediate compartment. J. Cell Sci. 112: 1477-1486 [Abstract]
Sato, M., Sato, K., Nishikawa, S.-i., Hirata, A., Kato, J.-i., Nakano, A. (1999). The Yeast RER2 Gene, Identified by Endoplasmic Reticulum Protein Localization Mutations, Encodes cis-Prenyltransferase, a Key Enzyme in Dolichol Synthesis. Mol. Cell. Biol. 19: 471-483 [Abstract] [Full Text]
Letourneur, F., Cosson, P. (1998). Targeting to the Endoplasmic Reticulum in Yeast Cells by Determinants Present in Transmembrane Domains. J. Biol. Chem. 273: 33273-33278 [Abstract] [Full Text]
Nakamura, N., Yamazaki, S., Sato, K., Nakano, A., Sakaguchi, M., Mihara, K. (1998). Identification of Potential Regulatory Elements for the Transport of Emp24p. Mol. Biol. Cell 9: 3493-3503 [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]
Reggiori, F., Conzelmann, A. (1998). Biosynthesis of Inositol Phosphoceramides and Remodeling of Glycosylphosphatidylinositol Anchors in Saccharomyces cerevisiae Are Mediated by Different Enzymes. J. Biol. Chem. 273: 30550-30559 [Abstract] [Full Text]
Majoul, I., Sohn, K., Wieland, F. T., Pepperkok, R., Pizza, M., Hillemann, J., Soling, H.-D. (1998). KDEL Receptor (Erd2p)-mediated Retrograde Transport of the Cholera Toxin A Subunit from the Golgi Involves COPI, p23, and the COOH Terminus of Erd2p. JCB 143: 601-612 [Abstract] [Full Text]
Schmidt, W. K., Tam, A., Fujimura-Kamada, K., Michaelis, S. (1998). Endoplasmic reticulum membrane localization of Rce1p and Ste24p, yeast proteases involved in carboxyl-terminal CAAX protein processing and amino-terminal a-factor cleavage. Proc. Natl. Acad. Sci. USA 95: 11175-11180 [Abstract] [Full Text]
Powers, J., Barlowe, C. (1998). Transport of Axl2p Depends on Erv14p, an ER-Vesicle Protein Related to the Drosophila cornichon Gene Product. JCB 142: 1209-1222 [Abstract] [Full Text]
Honsho, M., Mitoma, J.-y., Ito, A. (1998). Retention of Cytochrome b5 in the Endoplasmic Reticulum Is Transmembrane and Luminal Domain-dependent. J. Biol. Chem. 273: 20860-20866 [Abstract] [Full Text]
Romano, J. D., Schmidt, W. K., Michaelis, S. (1998). The Saccharomyces cerevisiae Prenylcysteine Carboxyl Methyltransferase Ste14p Is in the Endoplasmic Reticulum Membrane. Mol. Biol. Cell 9: 2231-2247 [Abstract] [Full Text]
Schroder-Kohne, S, Letourneur, F, Riezman, H (1998). Alpha-COP can discriminate between distinct, functional di-lysine signals in vitro and regulates access into retrograde transport. J. Cell Sci. 111: 3459-3470 [Abstract]
Ballensiefen, W, Ossipov, D, Schmitt, H. (1998). Recycling of the yeast v-SNARE Sec22p involves COPI-proteins and the ER transmembrane proteins Ufe1p and Sec20p. J. Cell Sci. 111: 1507-1520 [Abstract]
Fiedler, K., Rothman, J. E. (1997). Sorting Determinants in the Transmembrane Domain of p24 Proteins. J. Biol. Chem. 272: 24739-24742 [Abstract] [Full Text]
Sato, K., Sato, M., Nakano, A. (1997). Rer1p as common machinery for the endoplasmic reticulum localization of membrane�proteins. Proc. Natl. Acad. Sci. USA 94: 9693-9698 [Abstract] [Full Text]
Campbell, J.�L., Schekman, R. (1997). Selective packaging of cargo molecules into endoplasmic reticulum-derived�COPII�vesicles. Proc. Natl. Acad. Sci. USA 94: 837-842 [Abstract] [Full Text]
Boehm, J, Letourneur, F, Ballensiefen, W, Ossipov, D, Demolliere, C, Schmitt, H. (1997). Sec12p requires Rer1p for sorting to coatomer (COPI)-coated vesicles and retrieval to the ER. J. Cell Sci. 110: 991-1003 [Abstract]
Kokame, K., Agarwala, K. L., Kato, H., Miyata, T. (2000). Herp, a New Ubiquitin-like Membrane Protein Induced by Endoplasmic Reticulum Stress. J. Biol. Chem. 275: 32846-32853 [Abstract] [Full Text]
Szczesna-Skorupa, E., Kemper, B. (2000). Endoplasmic Reticulum Retention Determinants in the Transmembrane and Linker Domains of Cytochrome P450 2C1. J. Biol. Chem. 275: 19409-19415 [Abstract] [Full Text]
Szczesna-Skorupa, E., Kemper, B. (2001). The Juxtamembrane Sequence of Cytochrome P-450 2C1 Contains an Endoplasmic Reticulum Retention Signal. J. Biol. Chem. 276: 45009-45014 [Abstract] [Full Text]
Mottola, G., Jourdan, N., Castaldo, G., Malagolini, N., Lahm, A., Serafini-Cessi, F., Migliaccio, G., Bonatti, S. (2000). A New Determinant of Endoplasmic Reticulum Localization Is Contained in the Juxtamembrane Region of the Ectodomain of Hepatitis C Virus Glycoprotein E1. J. Biol. Chem. 275: 24070-24079 [Abstract] [Full Text]