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Originally published as MBC in Press, 10.1091/mbc.E05-08-0792 on January 18, 2006

Vol. 17, Issue 4, 1514-1526, April 2006

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Rab1 Defines a Novel Pathway Connecting the Pre-Golgi Intermediate Compartment with the Cell PeripheryFormula

Ragna Sannerud * {dagger}, Michaël Marie *, Clément Nizak {ddagger} §, Hege Avsnes Dale ||, Karin Pernet-Gallay {ddagger}, Franck Perez {ddagger}, Bruno Goud {ddagger}, and Jaakko Saraste *

* Section of Anatomy and Cell Biology, University of Bergen, N-5009 Bergen, Norway; || Molecular Imaging Center, Department of Biomedicine, University of Bergen, N-5009 Bergen, Norway; and {ddagger} Centre National de la Recherche Scientifique Unité Mixte de Recherche 144, Institut Curie, Section de Recherche, 75248 Paris Cedex 05, France

Submitted August 25, 2005; Revised December 21, 2005; Accepted January 5, 2006
Monitoring Editor: Jennifer Lippincott-Schwartz

The function of the pre-Golgi intermediate compartment (IC) and its relationship with the endoplasmic reticulum (ER) and Golgi remain only partially understood. Here, we report striking segregation of IC domains in polarized PC12 cells that develop neurite-like processes. Differentiation involves expansion of the IC and movement of Rab1-containing tubules to the growth cones of the neurites, whereas p58- and COPI-positive IC elements, like rough ER and Golgi, remain in the cell body. Exclusion of Rab1 effectors p115 and GM130 from the neurites further indicated that the centrifugal, Rab1-mediated pathway has functions that are not directly related to ER-to-Golgi trafficking. Disassembly of COPI coats did not affect this pathway but resulted in missorting of p58 to the neurites. Live cell imaging showed that green fluorescent protein (GFP)–Rab1A-containing IC elements move bidirectionally both within the neurites and cell bodies, interconnecting different ER exit sites and the cis-Golgi region. Moreover, in nonpolarized cells GFP-Rab1A-positive tubules moved centrifugally towards the cell cortex. Hydroxymethylglutaryl-CoA reductase, the key enzyme of cholesterol biosynthesis, colocalized with slowly sedimenting, Rab1-enriched membranes when the IC subdomains were separated by velocity sedimentation. These results reveal a novel pathway directly connecting the IC with the cell periphery and suggest that this Rab1-mediated pathway is linked to the dynamics of smooth ER.

This article was published online ahead of print in MBC in Press (http://www.molbiolcell.org/cgi/doi/10.1091/mbc.E05-08-0792) on January 18, 2006.

Formula The online version of this article contains supplemental material at MBC Online (http://www.molbiolcell.org).

{dagger} Present address: Laboratory for Membrane Trafficking, Center for Human Genetics, Gasthuisberg, KULeuven/VIB4, B-3000 Leuven, Belgium

§ Present address: Rockefeller University, Center for Studies in Physics and Biology, Living Matter Laboratory, Box 34, 1230 York Avenue, New York, NY 10021.

Address correspondence to: Jaakko Saraste (jaakko.saraste{at}biomed.uib.no).




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