A Selective Transport Route from Golgi to Late Endosomes That Requires the Yeast Gga Proteins

doi:10.1083/jcb.151.3.587

Published online 30 October 2000. doi:10.1083/jcb.151.3.587

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© The Rockefeller University Press, 0021-9525/2000//587 $5.00
The Journal of Cell Biology, Volume 151, Number 3, , 2000 587-600

Original Article

A Selective Transport Route from Golgi to Late Endosomes That Requires the Yeast Gga Proteins

Michael W. Black^a and Hugh R.B. Pelham^a

^a Medical Research Council, Laboratory of Molecular Biology, Cambridge CB2 2QH, United Kingdom
MRC Laboratory of Molecular Biology, Hills Road, Cambridge CB2 2QH, UK.44-1223-41214244-1223-402290

Pep12p is a yeast syntaxin located primarily in late endosomes.Using mutagenesis of a green fluorescent protein chimera wehave identified a sorting signal FSDSPEF, which is requiredfor transport of Pep12p from the exocytic pathway to late endosomes,from which it can, when overexpressed, reach the vacuole. Whenthis signal is mutated, Pep12p instead passes to early endosomes,a step that is determined by its transmembrane domain. Surprisingly,Pep12p is then specifically retained in early endosomes anddoes not go on to late endosomes.

By testing appropriate chimeras in mutant strains, we foundthat FSDSPEF-dependent sorting was abolished in strains lackingGga1p and Gga2p, Golgi-associated coat proteins with homologyto gamma adaptin. In the gga1 gga2 double mutant endogenousPep12p cofractionated with the early endosome marker Tlg1p,and recycling of Snc1p through early endosomes was defective.Pep12p sorting was also defective in cells lacking the clathrinheavy or light chain. We suggest that specific and direct deliveryof proteins to early and late endosomes is required to maintainthe functional heterogeneity of the endocytic pathway and thatthe GGA proteins, probably in association with clathrin, helpcreate vesicles destined for late endosomes.

Key Words: clathrin • endosomes • GGA proteins • Golgi apparatus • Pep12p

Abbreviations used in this paper: CPY, carboxypeptidase Y; GFP,green fluorescent protein; PVC, pre-vacuolar compartment; SNARE,soluble N-ethylmaleimide–sensitive fusion protein attachmentprotein receptor; TMD, transmembrane domain.

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Hinners, I., Tooze, S. A. (2003). Changing directions: clathrin-mediated transport between the Golgi and endosomes. J. Cell Sci. 116: 763-771 [Abstract] [Full Text]
Waguri, S., Dewitte, F., Le Borgne, R., Rouille, Y., Uchiyama, Y., Dubremetz, J.-F., Hoflack, B. (2003). Visualization of TGN to Endosome Trafficking through Fluorescently Labeled MPR and AP-1 in Living Cells. Mol. Biol. Cell 14: 142-155 [Abstract] [Full Text]
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Doray, B., Ghosh, P., Griffith, J., Geuze, H. J., Kornfeld, S. (2002). Cooperation of GGAs and AP-1 in Packaging MPRs at the Trans-Golgi Network. Science 297: 1700-1703 [Abstract] [Full Text]
Boman, A. L., Salo, P. D., Hauglund, M. J., Strand, N. L., Rensink, S. J., Zhdankina, O. (2002). ADP-Ribosylation Factor (ARF) Interaction Is Not Sufficient for Yeast GGA Protein Function or Localization. Mol. Biol. Cell 13: 3078-3095 [Abstract] [Full Text]
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Doray, B., Bruns, K., Ghosh, P., Kornfeld, S. A. (2002). Autoinhibition of the ligand-binding site of GGA1/3 VHS domains by an internal acidic cluster-dileucine motif. Proc. Natl. Acad. Sci. USA 99: 8072-8077 [Abstract] [Full Text]
Doray, B., Bruns, K., Ghosh, P., Kornfeld, S. (2002). Interaction of the Cation-dependent Mannose 6-Phosphate Receptor with GGA Proteins. J. Biol. Chem. 277: 18477-18482 [Abstract] [Full Text]
Volker, A., Stierhof, Y.-D., Jurgens, G. (2002). Cell cycle-independent expression of the Arabidopsis cytokinesis-specific syntaxin KNOLLE results in mistargeting to the plasma membrane and is not sufficient for cytokinesis. J. Cell Sci. 114: 3001-3012 [Abstract] [Full Text]
Mullins, C., Bonifacino, J. S. (2001). Structural Requirements for Function of Yeast GGAs in Vacuolar Protein Sorting, alpha -Factor Maturation, and Interactions with Clathrin. Mol. Cell. Biol. 21: 7981-7994 [Abstract] [Full Text]
Bagnat, M., Chang, A., Simons, K. (2001). Plasma Membrane Proton ATPase Pma1p Requires Raft Association for Surface Delivery in Yeast. Mol. Biol. Cell 12: 4129-4138 [Abstract] [Full Text]
Hirst, J., Lindsay, M. R., Robinson, M. S. (2001). Golgi-localized, gamma-Ear-containing, ADP-Ribosylation Factor-binding Proteins: Roles of the Different Domains and Comparison with AP-1 and Clathrin. Mol. Biol. Cell 12: 3573-3588 [Abstract] [Full Text]
Boehm, M., Bonifacino, J. S. (2001). Adaptins. The Final Recount. Mol. Biol. Cell 12: 2907-2920 [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]
Zhu, Y., Doray, B., Poussu, A., Lehto, V.-P., Kornfeld, S. (2001). Binding of GGA2 to the Lysosomal Enzyme Sorting Motif of the Mannose 6-Phosphate Receptor. Science 292: 1716-1718 [Abstract] [Full Text]
Costaguta, G., Stefan, C. J., Bensen, E. S., Emr, S. D., Payne, G. S. (2001). Yeast Gga Coat Proteins Function with Clathrin in Golgi to Endosome Transport. Mol. Biol. Cell 12: 1885-1896 [Abstract] [Full Text]
Boman, A. L. (2001). GGA proteins: new players in the sorting game. J. Cell Sci. 114: 3413-3418 [Abstract] [Full Text]
Takatsu, H., Katoh, Y., Shiba, Y., Nakayama, K. (2001). Golgi-localizing, gamma -Adaptin Ear Homology Domain, ADP-ribosylation Factor-binding (GGA) Proteins Interact with Acidic Dileucine Sequences within the Cytoplasmic Domains of Sorting Receptors through Their Vps27p/Hrs/STAM (VHS) Domains. J. Biol. Chem. 276: 28541-28545 [Abstract] [Full Text]