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J. Biol. Chem., Vol. 279, Issue 45, 47242-47253, November 5, 2004

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Proteomics of Endoplasmic Reticulum-Golgi Intermediate Compartment (ERGIC) Membranes from Brefeldin A-treated HepG2 Cells Identifies ERGIC-32, a New Cycling Protein That Interacts with Human Erv46^*

Lionel Breuza, Regula Halbeisen, Paul Jenö, Stefan Otte¶, Charles Barlowe, Wanjin Hong||, and Hans-Peter Hauri**

From the Biozentrum, University of Basel, Klingelbergstrasse 70, CH-4056 Basel, Switzerland, the Department of Biochemistry, Dartmouth Medical School, Hanover, New Hampshire, and the ^||Institute of Molecular and Cell Biology, Singapore 117609, Singapore

Cycling proteins play important roles in the organization and function of the early secretory pathway by participating in membrane traffic and selective transport of cargo between the endoplasmic reticulum (ER), the intermediate compartment (ERGIC), and the Golgi. To identify new cycling proteins, we have developed a novel procedure for the purification of ERGIC membranes from HepG2 cells treated with brefeldin A, a drug known to accumulate cycling proteins in the ERGIC. Membranes enriched 110-fold over the homogenate for ERGIC-53 were obtained and analyzed by mass spectrometry. Major proteins corresponded to established and putative cargo receptors and components mediating protein maturation and membrane traffic. Among the uncharacterized proteins, a 32-kDa protein termed ERGIC-32 is a novel cycling membrane protein with sequence homology to Erv41p and Erv46p, two proteins enriched in COPII vesicles of yeast. ERGIC-32 localizes to the ERGIC and partially colocalizes with the human homologs of Erv41p and Erv46p, which mainly localize to the cis-Golgi. ERGIC-32 interacts with human Erv46 (hErv46) as revealed by covalent cross-linking and mistargeting experiments, and silencing of ERGIC-32 by small interfering RNAs increases the turnover of hErv46. We propose that ERGIC-32 functions as a modulator of the hErv41-hErv46 complex by stabilizing hErv46. Our novel approach for the isolation of the ERGIC from BFA-treated cells may ultimately lead to the identification of all proteins rapidly cycling early in the secretory pathway.

Received for publication, June 15, 2004 , and in revised form, August 10, 2004.

The nucleotide sequence reported in this paper has been submitted to the Swiss Protein Database under Swiss-Prot accession no. Q969X5.

^* This work was supported by the Swiss National Science Foundation and the University of Basel. 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.

The on-line version of this article (available at http://www.jbc.org) contains supplementary Fig. 1.

^¶ Current address: Dept. of Biochemistry and Molecular Genetics, University of Illinois, Chicago, IL 60607.

^** To whom correspondence should be addressed. Tel.: 41-61-267-2222 or -2229; Fax: 41-61-267-2208; E-mail: Hans-Peter.Hauri{at}unibas.ch.

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