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J. Biol. Chem., Vol. 282, Issue 31, 22499-22512, August 3, 2007

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Regulation of ERGIC-53 Gene Transcription in Response to Endoplasmic Reticulum Stress^*

Maurizio Renna, Maria Gabriella Caporaso, Stefano Bonatti, Randal J. Kaufman^¶1, and Paolo Remondelli²

From the Dipartimento di Scienze Farmaceutiche, Università degli Studi di Salerno, Fisciano-Salerno I-84034, Italy, the Dipartimento di Biochimica e Biotecnologie Mediche, Università degli Studi di Napoli "Federico II," Naples I-80131, Italy, and the ^¶Department of Biological Chemistry and Internal Medicine and the Howard Hughes Medical Institute, University of Michigan Medical Center, Ann Arbor, Michigan 48109

Accumulation of unfolded proteins within the endoplasmic reticulum (ER) activates the unfolded protein response, also known as the ER stress response. We previously demonstrated that ER stress induces transcription of the ER Golgi intermediate compartment protein ERGIC-53. To investigate the molecular events that regulate unfolded protein response-mediated induction of the gene, we have analyzed the transcriptional regulation of ERGIC-53. We found that the ERGIC-53 promoter contains a single cis-acting element that mediates induction of the gene by thapsigargin and other ER stress-causing agents. This ER stress response element proved to retain a novel structure and to be highly conserved in mammalian ERGIC-53 genes. The ER stress response element identified contains a 5'-end CCAAT sequence that constitutively binds NFY/CBF and, 9 nucleotides away, a 3'-end region (5'-CCCTGTTGGCCATC-3') that is equally important for ER stress-mediated induction of the gene. This sequence is the binding site for endogenous YY1 at the 5'-CCCTGTTGG-3' part and for undefined factors at the CCATC 3'-end. ATF6-YY1, but not XBP1, interacted with the ERGIC-53 regulatory region and activated ERGIC-53 ER stress response element-dependent transcription. A molecular model for the transcriptional regulation of the ERGIC-53 gene is proposed.

Received for publication, May 8, 2007

^* This work was supported in part by grants from the Consorzio Interuniversitario per le Biotecnologie 2003 (to S. B.) and the Università di Salerno (ex 60% 2005 and 2006) (to P. R.). Portions of this work were supported by National Institutes of Health Grants HL52173 and HL057346 (to R. J. K.). 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 supplemental Fig. S1.

¹ An investigator of the Howard Hughes Medical Institute.

² To whom correspondence should be addressed: Dipartimento di Scienze Farmaceutiche, Università degli Studi di Salerno, Via Ponte Don Melillo, Fisciano-Salerno, Italy I-84034. Tel.: 39-089-962767; Fax: 39-089-969602; E-mail: premondelli{at}unisa.it.

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