Localization, Dynamics, and Protein Interactions Reveal Distinct Roles for ER and Golgi SNAREs

doi:10.1083/jcb.141.7.1489

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© The Rockefeller University Press, 0021-9525/1998//1489 $5.00
The Journal of Cell Biology, Volume 141, Number 7, , 1998 1489-1502

Articles

Localization, Dynamics, and Protein Interactions Reveal Distinct Roles for ER and Golgi SNAREs

Jesse C. Hay^*, Judith Klumperman, Viola Oorschot, Martin Steegmaier^*, Christin S. Kuo^*, and Richard H. Scheller^*

^* Howard Hughes Medical Institute, Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, California 94305-5428; and Medical School, University of Utrecht, 3584CX Utrecht, The Netherlands

ER-to-Golgi transport, and perhaps intraGolgi transport involvesa set of interacting soluble N-ethylmaleimide–sensitivefactor attachment protein receptor (SNARE) proteins includingsyntaxin 5, GOS-28, membrin, rsec22b, and rbet1. By immunoelectron microscopy we find that rsec22b and rbet1 are enriched inCOPII-coated vesicles that bud from the ER and presumably fusewith nearby vesicular tubular clusters (VTCs). However, allof the SNAREs were found on both COPII- and COPI-coated membranes,indicating that similar SNARE machinery directs both vesicle pathways. rsec22b and rbet1 do not appear beyond the firstGolgi cisterna, whereas syntaxin 5 and membrin penetrate deeplyinto the Golgi stacks. Temperature shifts reveal that membrin,rsec22b, rbet1, and syntaxin 5 are present together on membranesthat rapidly recycle between peripheral and Golgi-centric locations. GOS-28, on the other hand, maintains a fixed localization inthe Golgi. By immunoprecipitation analysis, syntaxin 5 existsin at least two major subcomplexes: one containing syntaxin5 (34-kD isoform) and GOS-28, and another containing syntaxin5 (41- and 34-kD isoforms), membrin, rsec22b, and rbet1. Bothsubcomplexes appear to involve direct interactions of each SNARE with syntaxin 5. Our results indicate a central rolefor complexes among rbet1, rsec22b, membrin, and syntaxin 5(34 and 41 kD) at two membrane fusion interfaces: the fusionof ER-derived vesicles with VTCs, and the assembly of VTCsto form cis-Golgi elements. The 34-kD syntaxin 5 isoform, membrin,and GOS-28 may function in intraGolgi transport.

Abbreviations used in this paper: IC, intermediate compartment; SNARE, soluble N-ethylmaleimide–sensitive factor attachment protein receptor; VTC, vesicular tubular cluster.

Jesse C. Hay and Judith Klumpermancontributed equally to thispaper. The present address of Jesse C. Hay is Department ofBiology, University of Michigan, 830 N. University, Ann Arbor,MI 48109-1048.

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