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Originally published In Press as doi:10.1074/jbc.M110164200 on March 4, 2002

J. Biol. Chem., Vol. 277, Issue 20, 18077-18083, May 17, 2002
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Ultraviolet Light Inhibits Translation through Activation of the Unfolded Protein Response Kinase PERK in the Lumen of the Endoplasmic Reticulum*

Shiyong WuDagger §, Yuanyuan HuDagger , Ju-Lin WangDagger , Madhumita ChatterjeeDagger , Yuguang Shi, and Randal J. Kaufman||

From the Departments of Dagger  Radiation Oncology and || Biological Chemistry, The Howard Hughes Medical Institute, University of Michigan Medical Center, Ann Arbor, Michigan 48109 and the  Endocrine Division, Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana 46285

Exposure to ultraviolet light can cause inflammation, premature skin aging, and cancer. UV irradiation alters the expression of multiple genes that encode functions to repair DNA damage, arrest cell growth, and induce apoptosis. In addition, UV irradiation inhibits protein synthesis, although the mechanism is not known. In this report, we show that UV irradiation induces phosphorylation of eukaryotic translation initiation factor 2 on the alpha -subunit (eIF2alpha ) and inhibits protein synthesis in a dosage- and time-dependent manner. The UV-induced phosphorylation of eIF2alpha was prevented by the overexpression of a non-phosphorylatable mutant of eIF2alpha (S51A). PERK is an eIF2alpha protein kinase localized to the endoplasmic reticulum that is activated by the accumulation of unfolded proteins in the endoplasmic reticulum. Expression of trans-dominant-negative mutants of PERK also prevented eIF2alpha phosphorylation upon UV treatment and protected from the associated translation attenuation. The luminal domain of dominant-negative mutant PERK formed heterodimers with endogenous PERK to inhibit the PERK signaling pathway. In contrast, eIF2alpha phosphorylation was not inhibited by overexpression of a trans-dominant-negative mutant kinase, PKR, supporting the theory that UV-induced eIF2alpha phosphorylation is specifically mediated by PERK. These results support a novel mechanism by which UV irradiation regulates translation via an endoplasmic reticulum-stress signaling pathway.

* This work was supported in part by National Institutes of Health Grants RO1 CA86926 (to S. W.) and RO1 AI42394 (to R. J. K.).The costs of publication of this article were defrayed in part by the payment of page charges. The 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: Rm. 4131, 1331 E. Ann St., Ann Arbor, MI 48109-0581. Tel.: 734-647-6679; Fax: 734-763-1581; E-mail: shiyongw@umich.edu.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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Copyright © 2002 by the American Society for Biochemistry and Molecular Biology.