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Originally published In Press as doi:10.1074/jbc.M409034200 on September 1, 2004 Originally published In Press as doi:10.1074/jbc.M409034200 on August 25, 2004 Originally published In Press as doi:10.1074/jbc.M409034200 on August 24, 2004

J. Biol. Chem., Vol. 279, Issue 44, 45676-45684, October 29, 2004
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AAA ATPase p97/Valosin-containing Protein Interacts with gp78, a Ubiquitin Ligase for Endoplasmic Reticulum-associated Degradation*

Xiaoyan Zhong{ddagger}, Yuxian Shen{ddagger}, Petek Ballar{ddagger}, Andria Apostolou{ddagger}, Reuven Agami§, and Shengyun Fang{ddagger}

From the {ddagger}Medical Biotechnology Center, University of Maryland Biotechnology Institute, Baltimore, Maryland 21201 and the §Division of Tumor Biology, The Netherlands Cancer Institute, Plesmanlaan 121, Amsterdam 1066 CX, The Netherlands

Endoplasmic reticulum-associated degradation (ERAD) is a protein quality control mechanism that eliminates unwanted proteins from the endoplasmic reticulum (ER) through a ubiquitin-dependent proteasomal degradation pathway. gp78 is a previously described ER membrane-anchored ubiquitin ligase (E3) involved in ubiquitination of ER proteins. AAA ATPase (ATPase associated with various cellular activities) p97/valosin-containing protein (VCP) subsequently dislodges the ubiquitinated proteins from the ER and chaperones them to the cytosol, where they undergo proteasomal degradation. We now report that gp78 physically interacts with p97/VCP and enhances p97/VCP-polyubiquitin association. The enhanced association correlates with decreases in ER stress-induced accumulation of polyubiquitinated proteins. This effect is abolished when the p97/VCP-interacting domain of gp78 is removed. Further, using ERAD substrate CD3{delta}, gp78 consistently enhances p97/VCP-CD3{delta} binding and facilitates CD3{delta} degradation. Moreover, inhibition of endogenous gp78 expression by RNA interference markedly increases the levels of total polyubiquitinated proteins, including CD3{delta}, and abrogates VCP-CD3{delta} interactions. The gp78 mutant with deletion of its p97/VCP-interacting domain fails to increase CD3{delta} degradation and leads to accumulation of polyubiquitinated CD3{delta}, suggesting a failure in delivering ubiquitinated CD3{delta} for degradation. These data suggest that gp78-p97/VCP interaction may represent one way of coupling ubiquitination with retrotranslocation and degradation of ERAD substrates.

Received for publication, August 6, 2004

* This work was supported by National Institutes of Health Grant R01 GM69967-01A1 (to S. F.). 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.

To whom correspondence should be addressed: Medical Biotechnology Center, University of Maryland Biotechnology Institute, UMBI Bldg., N359, 725 W. Lombard St., Baltimore, MD 21201. E-mail: fangs{at}umbi.umd.edu.


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