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© The Rockefeller University Press, 0021-9525/1998//665 $5.00
The Journal of Cell Biology, Volume 142, Number 3, , 1998 665-681

A Membrane Coat Complex Essential for Endosome-to-Golgi Retrograde Transport in Yeast

Division of Cellular and Molecular Medicine and Howard Hughes Medical Institute, University of California at San Diego, School of Medicine, La Jolla, California 92093–0668

We have recently characterized three yeast gene products (Vps35p, Vps29p, and Vps30p) as candidate components of the sorting machinery required for the endosome-to-Golgi retrieval of the vacuolar protein sorting receptor Vps10p (Seaman, M.N.J., E.G. Marcusson, J.-L. Cereghino, and S.D. Emr. 1997. J. Cell Biol. 137:79–92). By genetic and biochemical means we now show that Vps35p and Vps29p interact and form part of a multimeric membrane-associated complex that also contains Vps26p, Vps17p, and Vps5p. This complex, designated here as the retromer complex, assembles from two distinct subcomplexes comprising (a) Vps35p, Vps29p, and Vps26p; and (b) Vps5p and Vps17p. Density gradient fractionation of Golgi/endosomal/vesicular membranes reveals that Vps35p cofractionates with Vps5p/Vps17p in a vesicle-enriched dense membrane fraction. Furthermore, gel filtration analysis indicates that Vps35p and Vps5p are present on a population of vesicles and tubules slightly larger than COPI/coatomer-coated vesicles. We also show by immunogold EM that Vps5p is localized to discrete regions at the rims of the prevacuolar endosome where vesicles appear to be budding. Size fractionation of cytosolic and recombinant Vps5p reveals that Vps5p can self-assemble in vitro, suggesting that Vps5p may provide the mechanical impetus to drive vesicle formation. Based on these findings we propose a model in which Vps35p/Vps29p/Vps26p function to select cargo for retrieval, and Vps5p/Vps17p assemble onto the membrane to promote vesicle formation. Conservation of the yeast retromer complex components in higher eukaryotes suggests an important general role for this complex in endosome-to-Golgi retrieval.

Key Words: retrieval • endosome • Golgi • vesicle • coat

Abbreviations used in this paper: CPY, carboxypeptidase Y; DPAP A, dipeptidyl amino peptidase A; DTSSP, 3,3'-dithiobis sulfosuccinimidyl-proprionate; GST, glutathione S-transferase; HA, hemagglutinin; M6P, mannose-6-phosphate.

The present address of Matthew N.J. Seaman is Department of Clinical Biochemistry, University of Cambridge, Addenbrookes Hospital, Hills Road, Cambridge, CB2 2QR, United Kingdom.

Address all correspondence to Scott D. Emr, Division of Cellular and Molecular Medicine, Howard Hughes Medical Institute, UCSD School of Medicine, 9500 Gilman Drive, La Jolla, CA 92093-0668. Tel.: 619-534-6462; Fax: 619-534-6414; E-mail: semr{at}ucsd.edu

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• Chen, C.-Y., Ingram, M. F., Rosal, P. H., Graham, T. R. (1999). Role for Drs2p, a P-Type Atpase and Potential Aminophospholipid Translocase, in Yeast Late Golgi Function. JCB 147: 1223-1236 [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]  
• Stephens, D. J., Banting, G. (1999). Direct Interaction of the trans-Golgi Network Membrane Protein, TGN38, with the F-actin Binding Protein, Neurabin. J. Biol. Chem. 274: 30080-30086 [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]  
• Chin, L.-S., Raynor, M. C., Wei, X., Chen, H.-Q., Li, L. (2001). Hrs Interacts with Sorting Nexin 1 and Regulates Degradation of Epidermal Growth Factor Receptor. J. Biol. Chem. 276: 7069-7078 [Abstract] [Full Text]  
• Phillips, S. A., Barr, V. A., Haft, D. H., Taylor, S. I., Haft, C. R. (2001). Identification and Characterization of SNX15, a Novel Sorting Nexin Involved in Protein Trafficking. J. Biol. Chem. 276: 5074-5084 [Abstract] [Full Text]  
• Parks, W. T., Frank, D. B., Huff, C., Renfrew Haft, C., Martin, J., Meng, X., de Caestecker, M. P., McNally, J. G., Reddi, A., Taylor, S. I., Roberts, A. B., Wang, T., Lechleider, R. J. (2001). Sorting Nexin 6, a Novel SNX, Interacts with the Transforming Growth Factor-beta Family of Receptor Serine-Threonine Kinases. J. Biol. Chem. 276: 19332-19339 [Abstract] [Full Text]  
• Van Valkenburgh, H., Shern, J. F., Sharer, J. D., Zhu, X., Kahn, R. A. (2001). ADP-ribosylation factors (ARFs) and ARF-like 1 (ARL1) Have Both Specific and Shared Effectors. CHARACTERIZING ARL1-BINDING PROTEINS. J. Biol. Chem. 276: 22826-22837 [Abstract] [Full Text]  
• Borrelly, G., Boyer, J.-C., Touraine, B., Szponarski, W., Rambier, M., Gibrat, R. (2001). The yeast mutant vps5Delta affected in the recycling of Golgi membrane proteins displays an enhanced vacuolar Mg2+/H+ exchange activity. Proc. Natl. Acad. Sci. USA 98: 9660-9665 [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]  
• Jones, S. M., Foreman, S. K., Shank, B. B., Kurten, R. C. (2002). EGF receptor downregulation depends on a trafficking motif in the distal tyrosine kinase domain. Am. J. Physiol. Cell Physiol. 282: C420-C433 [Abstract] [Full Text]  

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