Abstract
Tethering complexes contribute to the specificity of membrane fusion by recognizing organelle features on both donor and acceptor membranes. The Golgi-associated retrograde protein (GARP) complex is required for retrograde traffic from both early and late endosomes to the trans-Golgi network (TGN), presenting a paradox as to how a single complex can interact specifically with vesicles from multiple upstream compartments. We have found that a subunit of the GARP complex, Vps54, can be separated into N- and C-terminal regions that have different functions. Whereas the N-terminus of Vps54 is important for GARP complex assembly and stability, a conserved C-terminal domain mediates localization to an early endocytic compartment. Mutation of this C-terminal domain has no effect on retrograde transport from late endosomes. However, a specific defect in retrieval of Snc1 from early endosomes is observed when recycling from late endosomes to the Golgi is blocked. These data suggest that separate domains recruit tethering complexes to different upstream compartments to regulate individual trafficking pathways.
References
56
Referenced
43
-
Andag, U., Neumann, T., and Schmitt, H. D. (2001). The coatomer-interacting protein Dsl1p is required for Golgi-to-endoplasmic reticulum retrieval in yeast.J. Biol. Chem.276, 39150-39160.
(
10.1074/jbc.M105833200
) -
Ayscough, K. R., Stryker, J., Pokala, N., Sanders, M., Crews, P., and Drubin, D. G. (1997). High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A.J. Cell Biol.137, 399-416.
(
10.1083/jcb.137.2.399
) -
Boyd, C., Hughes, T., Pypaert, M., and Novick, P. (2004). Vesicles carry most exocyst subunits to exocytic sites marked by the remaining two subunits, Sec3p and Exo70p.J. Cell Biol.167, 889-901.
(
10.1083/jcb.200408124
) -
Chen, L., and Davis, N. G. (2000). Recycling of the yeast a-factor receptor.J. Cell Biol.151, 731-738.
(
10.1083/jcb.151.3.731
) 10.1091/mbc.e04-03-0258
-
Chivian, D., Kim, D. E., Malmström, L., Bradley, P., Robertson, T., Murphy, P., Strauss, C.E.M., Bonneau, R., Rohl, C. A., and Baker, D. (2003). Automated prediction of CASP-5 structures using the Robetta server.Proteins Struct. Funct. Genet.53, 524-533.
(
10.1002/prot.10529
) 10.1091/mbc.11.7.2429
10.1091/mbc.e02-10-0654
-
Conibear, E., and Stevens, T. H. (1998). Multiple sorting pathways between the late Golgi and the vacuole in yeast.Biochim. Biophys. Acta1404, 211-230.
(
10.1016/S0167-4889(98)00058-5
) 10.1091/mbc.11.1.305
-
Conibear, E., and Stevens, T. H. (2002). Studying yeast vacuoles.Methods Enzymol.351, 408-432.
(
10.1016/S0076-6879(02)51861-9
) -
Cooper, A. A., and Stevens, T. H. (1996). Vps10p cycles between the late-Golgi and prevacuolar compartments in its function as the sorting receptor for multiple yeast vacuolar hydrolases.J. Cell Biol.133, 529-541.
(
10.1083/jcb.133.3.529
) 10.1091/mbc.12.1.37
-
Folsch, H., Pypaert, M., Maday, S., Pelletier, L., and Mellman, I. (2003). The AP-1A and AP-1B clathrin adaptor complexes define biochemically and functionally distinct membrane domains.J. Cell Biol.163, 351-362.
(
10.1083/jcb.200309020
) -
Galan, J. M., Wiederkehr, A., Seol, J. H., Haguenauer-Tsapis, R., Deshaies, R. J., Riezman, H., and Peter, M. (2001). Skp1p and the F-box protein Rcy1p form a non-SCF complex involved in recycling of the SNARE Snc1p in yeast.Mol. Cell. Biol.21, 3105-3117.
(
10.1128/MCB.21.9.3105-3117.2001
) -
Graham, L. A., Hill, K. J., and Stevens, T. H. (1998). Assembly of the yeast vacuolar H+-ATPase occurs in the endoplasmic reticulum and requires a Vma12p/Vma22p assembly complex.J. Cell Biol.142, 39-49.
(
10.1083/jcb.142.1.39
) -
Guo, W., Roth, D., Walch-Solimena, C., and Novick, P. (1999). The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis.EMBO J.18, 1071-1080.
(
10.1093/emboj/18.4.1071
) -
Guo, W., Tamanoi, F., and Novick, P. (2001). Spatial regulation of the exocyst complex by Rho1 GTPase.Nat. Cell Biol.3, 353-360.
(
10.1038/35070029
) -
Haase, S. B., and Lew, D. J. (1997). Flow cytometric analysis of DNA content in budding yeast.Methods Enzymol.283, 322-332.
(
10.1016/S0076-6879(97)83026-1
) -
Hettema, E. H., Lewis, M. J., Black, M. W., and Pelham, H. R. (2003). Retromer and the sorting nexins Snx4/41/42 mediate distinct retrieval pathways from yeast endosomes.EMBO J.22, 548-557.
(
10.1093/emboj/cdg062
) -
Huh, W. K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weissman, J. S., and O'Shea, E. K. (2003). Global analysis of protein localization in budding yeast.Nature425, 686-691.
(
10.1038/nature02026
) -
Kim, D. E., Chivian, D., and Baker, D. (2004). Protein structure prediction and analysis using the Robetta server.Nucleic Acids Res.32, W526-W531.
(
10.1093/nar/gkh468
) -
Lafourcade, C., Galan, J. M., and Peter, M. (2003). Opposite roles of the F-box protein Rcy1p and the GTPase-activating protein Gyp2p during recycling of internalized proteins in yeast.Genetics164, 469-477.
(
10.1093/genetics/164.2.469
) 10.1091/mbc.11.1.23
-
Liewen, H., Meinhold-Heerlein, I., Oliveira, V., Schwarzenbacher, R., Luo, G., Wadle, A., Jung, M., Pfreundschuh, M., and Stenner-Liewen, F. (2005). Characterization of the human GARP (Golgi associated retrograde protein) complex.Exp. Cell Res.306, 24-34.
(
10.1016/j.yexcr.2005.01.022
) -
Longtine, M., Mckenzie, A., III, Demarini, D. J., Nirav, G., Wach, S. A., Brachat, A., Philippsen, P., and Pringle, J. R. (1998). Additional modules for versatile and economical PCR-based gene deletion and modification inSaccharomyces cerevisiae.Yeast14, 953-961.
(
10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U
) -
Lupashin, V., and Sztul, E. (2005). Golgi tethering factors.Biochim. Biophys. Acta1744, 325-339.
(
10.1016/j.bbamcr.2005.03.013
) -
Maxfield, F. R., and McGraw, T. E. (2004). Endocytic Recycling.Nat. Rev. Mol. Cell Biol.5, 121-132.
(
10.1038/nrm1315
) -
Mehta, S. Q.et al.(2005). Mutations inDrosophilasec15 reveal a function in neuronal targeting for a subset of exocyst components.Neuron46, 219-232.
(
10.1016/j.neuron.2005.02.029
) -
Morsomme, P., and Riezman, H. (2002). The Rab GTPase Ypt1p and tethering factors couple protein sorting at the ER to vesicle targeting to the Golgi apparatus.Dev. Cell2, 307-317.
(
10.1016/S1534-5807(02)00133-8
) -
Munro, S. (2004). Organelle identity and the organization of membrane traffic.Nat. Cell Biol.6, 469-472.
(
10.1038/ncb0604-469
) -
Notredame, C., Higgins, D. G., and Heringa, J. (2000). T-coffee: a novel method for fast and accurate multiple sequence alignment.J. Mol. Biol.302, 205-217.
(
10.1006/jmbi.2000.4042
) -
Panic, B., Whyte, J. R., and Munro, S. (2003). The ARF-like GTPases Arl1p and Arl3p act in a pathway that interacts with vesicle-tethering factors at the Golgi apparatus.Curr. Biol.13, 405-410.
(
10.1016/S0960-9822(03)00091-5
) -
Pfeffer, S. R. (1996). Transport vesicle docking: SNAREs and associates.Annu. Rev. Cell Dev. Biol.12, 441-461.
(
10.1146/annurev.cellbio.12.1.441
) -
Prigent, M., Dubois, T., Raposo, G., Derrien, V., Tenza, D., Rosse, C., Camonis, J., and Chavrier, P. (2003). ARF6 controls post-endocytic recycling through its downstream exocyst complex effector.J. Cell Biol.163, 1111-1121.
(
10.1083/jcb.200305029
) -
Reggiori, F., Wang, C. W., Stromhaug, P. E., Shintani, T., and Klionsky, D. J. (2003). Vps51 is part of the yeast Vps fifty-three tethering complex essential for retrograde traffic from the early endosome and Cvt vesicle completion.J. Biol. Chem.278, 5009-5020.
(
10.1074/jbc.M210436200
) 10.1091/mbc.7.6.985
-
Rossanese, O. W., Reinke, C. A., Bevis, B. J., Hammond, A. T., Sears, I. B., O'Connor, J., and Glick, B. S. (2001). A role for actin, Cdc1p, and Myo2p in the inheritance of late Golgi elements inSaccharomyces cerevisiae.J. Cell Biol.153, 47-62.
(
10.1083/jcb.153.1.47
) -
Roumanie, O., Wu, H., Molk, J. N., Rossi, G., Bloom, K., and Brennwald, P. (2005). Rho GTPase regulation of exocytosis in yeast is independent of GTP hydrolysis and polarization of the exocyst complex.J. Cell Biol.170, 583-594.
(
10.1083/jcb.200504108
) -
Seaman, M. N., McCaffery, J. M., and Emr, S. D. (1998). A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast.J. Cell Biol.142, 665-681.
(
10.1083/jcb.142.3.665
) -
Sikorski, R. S., and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA inSaccharomyces cerevisiae.Genetics122, 19-27.
(
10.1093/genetics/122.1.19
) -
Siniossoglou, S., and Pelham, H. R. (2001). An effector of Ypt6p binds the SNARE Tlg1p and mediates selective fusion of vesicles with late Golgi membranes.EMBO J.20, 5991-5998.
(
10.1093/emboj/20.21.5991
) -
Siniossoglou, S., and Pelham, H. R. (2002). Vps51p links the VFT complex to the SNARE Tlg1p.J. Biol. Chem.277, 48318-48324.
(
10.1074/jbc.M209428200
) -
Sommer, B., Oprins, A., Rabouille, C., and Munro, S. (2005). The exocyst component Sec5 is present on endocytic vesicles in the oocyte ofDrosophila melanogaster.J. Cell Biol.169, 953-963.
(
10.1083/jcb.200411053
) -
Suvorova, E. S., Duden, R., and Lupashin, V. V. (2002). The Sec34/Sec35p complex, a Ypt1p effector required for retrograde intra-Golgi trafficking, interacts with Golgi SNAREs and COPI vesicle coat proteins.J. Cell Biol.157, 631-643.
(
10.1083/jcb.200111081
) -
TerBush, D. R., and Novick, P. (1995). Sec6, Sec8, and Sec15 are components of a multisubunit complex which localizes to small bud tips inSaccharomyces cerevisiae.J. Cell Biol.130, 299-312.
(
10.1083/jcb.130.2.299
) -
Tong, A. H., and Boone, C. (2005). Synthetic genetic array analysis inSaccharomyces cerevisiae.Methods Mol. Biol.313, 171-192.
(
10.1385/1-59259-958-3:171
) -
Tong, A.H.Y.et al.(2001). Systematic genetic analysis with ordered arrays of yeast deletion mutants.Science294, 2364-2368.
(
10.1126/science.1065810
) -
Valdivia, R. H., Baggott, D., Chuang, J. S., and Schekman, R. W. (2002). The yeast clathrin adaptor protein complex 1 is required for the efficient retention of a subset of late Golgi membrane proteins.Dev. Cell2, 283-294.
(
10.1016/S1534-5807(02)00127-2
) -
Vernet, T., Dignard, D., and Thomas, D. Y. (1987). A family of yeast expression vectors containing the phage f1 intergenic region.Gene52, 225-233.
(
10.1016/0378-1119(87)90049-7
) -
Vida, T. A., and Emr, S. D. (1995). A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast.J. Cell Biol.128, 779-792.
(
10.1083/jcb.128.5.779
) -
Whyte, J. R., and Munro, S. (2001). The Sec34/35 Golgi transport complex is related to the exocyst, defining a family of complexes involved in multiple steps of membrane traffic.Dev. Cell1, 527-537.
(
10.1016/S1534-5807(01)00063-6
) -
Whyte, J. R., and Munro, S. (2002). Vesicle tethering complexes in membrane traffic.J. Cell Sci.115, 2627-2637.
(
10.1242/jcs.115.13.2627
) -
Zhang, X., Bi, E., Novick, P., Du, L., Kozminski, K. G., Lipschutz, J. H., and Guo, W. (2001). Cdc42 interacts with the exocyst and regulates polarized secretion.J. Biol. Chem.276, 46745-46750.
(
10.1074/jbc.M107464200
) -
Zhang, X. M., Ellis, S., Sriratana, A., Mitchell, C. A., and Rowe, T. (2004). Sec15 is an effector for the Rab11 GTPase in mammalian cells.J. Biol. Chem.279, 43027-43034.
(
10.1074/jbc.M402264200
) -
Zolov, S. N., and Lupashin, V. V. (2005). Cog3p depletion blocks vesicle-mediated Golgi retrograde trafficking in HeLa cells.J. Cell Biol.168, 747-759.
(
10.1083/jcb.200412003
)
Dates
Type | When |
---|---|
Created | 19 years, 6 months ago (Feb. 1, 2006, 9:09 p.m.) |
Deposited | 4 years, 1 month ago (July 23, 2021, 7:52 a.m.) |
Indexed | 1 month, 3 weeks ago (July 2, 2025, 1:52 p.m.) |
Issued | 19 years, 4 months ago (April 1, 2006) |
Published | 19 years, 4 months ago (April 1, 2006) |
Published Print | 19 years, 4 months ago (April 1, 2006) |
@article{Quenneville_2006, title={Domains within the GARP Subunit Vps54 Confer Separate Functions in Complex Assembly and Early Endosome Recognition}, volume={17}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.e05-11-1002}, DOI={10.1091/mbc.e05-11-1002}, number={4}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Quenneville, Nicole R. and Chao, Tzu-Yuan and McCaffery, J. Michael and Conibear, Elizabeth}, year={2006}, month=apr, pages={1859–1870} }