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J. Biol. Chem., Vol. 280, Issue 32, 28997-29003, August 12, 2005

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Regulation and Surveillance of Normal and 3'-Extended Forms of the Yeast Aci-reductone Dioxygenase mRNA by RNase III Cleavage and Exonucleolytic Degradation^*

Cindy Zer and Guillaume Chanfreau

From the Department of Chemistry and Biochemistry and the Molecular Biology Institute, University of California, Los Angeles, California 90095

Aci-reductone dioxygenases are key enzymes in the methionine salvage pathway. The mechanisms by which the expression of this important class of enzymes is regulated are poorly understood. Here we show that the expression of the mRNA encoding the yeast aci-reductone dioxygenase ADI1 is controlled post-transcriptionally by RNase III cleavage. Cleavage occurs in a large bipartite stem loop structure present in the open reading frame region of the ADI1 mRNA. The ADI1 mRNA is up-regulated in the absence of the yeast orthologue of RNase III Rnt1p or of the 5' 3' exonucleases Xrn1p and Rat1p. 3'-Extended forms of this mRNA, including a polycistronic mRNA ADI1-YMR010W mRNA, also accumulate in cells lacking Rnt1p, Xrn1p, and Rat1p or the nuclear exosome component Rrp6p, suggesting that these 3'-extended forms are subject to nuclear surveillance. We show that the ADI1 mRNA is up-regulated under heat shock conditions in a Rnt1p-independent manner. We propose that Rnt1p cleavage targets degradation of the ADI1 mRNA to prevent its expression prior to heat shock conditions and that RNA surveillance by multiple ribonucleases helps prevent accumulation of aberrant 3'-extended forms of this mRNA that arise from intrinsically inefficient 3'-processing signals.

Received for publication, May 31, 2005 , and in revised form, June 20, 2005.

^* This work was supported by National Institutes of Health Grant GM61518 (to G. C.). 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.

Present address: UCLA David Geffen School of Medicine, Membrane Biology Laboratory/WLA VAMC, 11301 Wilshire Blvd., Los Angeles, CA 90073.

To whom correspondence should be addressed: Dept. of Chemistry and Biochemistry, University of California, Box 951569, Los Angeles, CA 90095-1569. Tel.: 310-825-4399; Fax: 310-206-4038; E-mail: guillom{at}chem.ucla.edu.

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