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J Biol Chem, Vol. 274, Issue 53, 37565-37574, December 31, 1999

A Highly Conserved Mechanism of Regulated Ribosome Stalling Mediated by Fungal Arginine Attenuator Peptides That Appears Independent of the Charging Status of Arginyl-tRNAs*

Zhong WangDagger §, Anthony GabaDagger §, and Matthew S. SachsDagger ∥**

From the Dagger  Department of Biochemistry and Molecular Biology, Oregon Graduate Institute of Science and Technology, Beaverton, Oregon 97006-8921 and the ∥ Department of Molecular Microbiology and Immunology, Oregon Health Sciences University, Portland, Oregon 97201-3098

The Arg attenuator peptide (AAP) is an evolutionarily conserved peptide involved in Arg-specific negative translational control. It is encoded as an upstream open reading frame (uORF) in fungal mRNAs specifying the small subunit of Arg-specific carbamoyl phosphate synthetase. We examined the functions of the Saccharomyces cerevisiae CPA1 and Neurospora crassa arg-2 AAPs using translation extracts from S. cerevisiae, N. crassa, and wheat germ. Synthetic RNA containing AAP and firefly luciferase (LUC) sequences were used to program translation; analyses of LUC activity indicated that the AAPs conferred Arg-specific negative regulation in each system. The AAPs functioned either as uORFs or fused in-frame at the N terminus of LUC. Mutant AAPs lacking function in vivo did not function in vitro. Therefore, trans-acting factors conferring AAP-mediated regulation are in both fungal and plant systems. Analyses of ribosome stalling in the fungal extracts by primer extension inhibition (toeprint) assays showed that these AAPs acted similarly to stall ribosomes in the region immediately distal to the AAP coding region in response to Arg. The regulatory effect increased as the Arg concentration increased; all of the arginyl-tRNAs examined appeared maximally charged at low Arg concentrations. Therefore, AAP-mediated Arg-specific regulation appeared independent of the charging status of arginyl-tRNA.

* This work was supported in part by National Institutes of Health Grant GM47498.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.

§ The first two authors contributed equally to this work.

Supported by National Institutes of Health Research Supplement for Underrepresented Minorities GM47498-S.

** To whom correspondence should be addressed: Dept. of Biochemistry and Molecular Biology, Oregon Graduate Inst. of Science and Technology, 20000 N.W. Walker Rd., Beaverton, OR 97006-8921. Tel.: 503-748-1487; Fax: 503-748-1464; E-mail: msachs@bmb.ogi.edu.

Copyright © 1999 by The American Society for Biochemistry and Molecular Biology, Inc.
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