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J. Biol. Chem., Vol. 278, Issue 52, 53112-53122, December 26, 2003

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Intra-Golgi Protein Transport Depends on a Cholesterol Balance in the Lipid Membrane^*

Ernstpeter Stüven, Amir Porat¶, Frida Shimron¶, Ephraim Fass¶, Dora Kaloyanova||, Britta Brügger, Felix T. Wieland, Zvulun Elazar¶, and J. Bernd Helms||**

From the Biochemie-Zentrum Heidelberg, University of Heidelberg, Im Neuenheimer Feld 328, 69120 Heidelberg, Germany, the ^¶Department of Biological Chemistry, The Weizmann Institute of Science, Rehovot 76100, Israel, and the ^||Department of Biochemistry and Cell Biology, University of Utrecht, P. O. Box 80176, 3508 TD Utrecht, The Netherlands

Transport of proteins between intracellular membrane compartments is mediated by a protein machinery that regulates the budding and fusion processes of individual transport steps. Although the core proteins of both processes are defined at great detail, much less is known about the involvement of lipids. Here we report that changing the cellular balance of cholesterol resulted in changes of the morphology of the Golgi apparatus, accompanied by an inhibition of protein transport. By using a well characterized cell-free intra-Golgi transport assay, these observations were further investigated, and it was found that the transport reaction is sensitive to small changes in the cholesterol content of Golgi membranes. Addition as well as removal of cholesterol (10 ± 6%) to Golgi membranes by use of methyl--cyclodextrin specifically inhibited the intra-Golgi transport assay. Transport inhibition occurred at the fusion step. Modulation of the cholesterol content changed the lipid raft partitioning of phosphatidylcholine and heterotrimeric G proteins, but not of other (non) lipid raft proteins and lipids. We suggest that the cholesterol balance in Golgi membranes plays an essential role in intra-Golgi protein transport and needs to be carefully regulated to maintain the structural and functional organization of the Golgi apparatus.

Received for publication, January 14, 2003 , and in revised form, September 9, 2003.

^* This work was supported by grants from the German-Israeli Foundation for scientific research and development (to F. T. W., Z. E., and J. B. H.), the German Research Council (Deutsche Forschungsgemeinschaft HE 2705 to J. B. H. and F. T. W.), and the European Community Research Training Network (Grant HPRN-CT-2000-00077 to J. B. H.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Both authors contributed equally to this work.

^** To whom correspondence should be addressed: Dept. of Biochemistry and Cell Biology, University of Utrecht, P. O. Box 80176, 3508 TD Utrecht, The Netherlands. Tel.: 31-30-253-5375; Fax: 31-30-253-5492; E-mail: j.b.helms{at}vet.uu.nl.

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