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J. Biol. Chem., Vol. 280, Issue 45, 37616-37622, November 11, 2005

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Discovery of a Gene Family Critical to Wyosine Base Formation in a Subset of Phenylalanine-specific Transfer RNAs^*

William F. Waas, Valérie de Crécy-Lagard1, and Paul Schimmel2

From the Department of Molecular Biology and The Skaggs Institute for Chemical Biology, The Scripps Research Institute, La, Jolla, California 92037 and the Department of Microbiology and Cell Science, University of Florida, Gainesville, Florida 32611

A large number of post-transcriptional base modifications in transfer RNAs have been described (Sprinzl, M., Horn, C., Brown, M., Ioudovitch, A., and Steinberg, S. (1998) Nucleic Acids Res. 26, 148-153). These modifications enhance and expand tRNA function to increase cell viability. The intermediates and genes essential for base modifications in many instances remain unclear. An example is wyebutosine (yW), a fluorescent tricyclic modification of an invariant guanosine situated on the 3'-side of the tRNA^Phe anticodon. Although biosynthesis of yW involves several reaction steps, only a single pathway-specific enzyme has been identified (Kalhor, H. R., Penjwini, M., and Clarke, S. (2005) Biochem. Biophys. Res. Commun. 334, 433-440). We used comparative genomics analysis to identify a cluster of orthologous groups (COG0731) of wyosine family biosynthetic proteins. Gene knock-out and complementation studies in Saccharomyces cerevisiae established a role for YPL207w, a COG0731 ortholog that encodes an 810-amino acid polypeptide. Further analysis showed the accumulation of N¹-methylguanosine (m¹G³⁷) in tRNA from cells bearing a YPL207w deletion. A similar lack of wyosine base and build-up of m¹G³⁷ is seen in certain mammalian tumor cell lines. We proposed that the 810-amino acid COG0731 polypeptide participates in converting tRNA^Phe-m¹G³⁷ to tRNA^Phe-yW.

Received for publication, June 27, 2005 , and in revised form, August 29, 2005.

^* This work was supported by Grants GM15539 and 23562 from the National Institutes of Health, a fellowship from the National Foundation for Cancer Research (to P. S.), and a Ruth L. Kirschstein National Research Service Award from the National Institutes of Health (to W. F. W.). 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.

¹ To whom correspondence may be addressed: Dept. of Microbiology and Cell Science, University of Florida, P. O. Box 110700, Gainesville, FL 32611-0700. Tel.: 352-392-9416; Fax: 352-392-5922; E-mail: vcrecy{at}ufl.edu. ² To whom correspondence may be addressed: Dept. of Molecular Biology and The Skaggs Institute for Chemical Biology, The Scripps Research Institute, 10550 N. Torrey Pines Rd., La Jolla, CA 92037. Tel.: 858-784-8970; Fax: 858-784-8990; E-mail: schimmel{at}scripps.edu.

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