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J. Biol. Chem., Vol. 283, Issue 4, 2049-2059, January 25, 2008

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Structure and Function of the Smallest Vertebrate Telomerase RNA from Teleost Fish^*

Mingyi Xie, Axel Mosig, Xiaodong Qi, Yang Li, Peter F. Stadler^¶||**, and Julian J.-L. Chen¹

From the Department of Chemistry & Biochemistry and School of Life Sciences, Arizona State University, Tempe, Arizona 85287, the Department of Combinatorics and Geometry, CAS-MPG Partner Institute for Computational Biology, Shanghai Institutes for Biological Sciences, Shanghai 200031, China, the ^¶Bioinformatics Group, Department of Computer Science, and Interdisciplinary Center for Bioinformatics, University of Leipzig, D-04107 Leipzig, Germany, the ^||Department of Theoretical Chemistry, University of Vienna, A-1090 Wien, Austria, and the ^**Santa Fe Institute, Santa Fe, New Mexica 87501

Telomerase extends chromosome ends by copying a short template sequence within its intrinsic RNA component. Telomerase RNA (TR) from different groups of species varies dramatically in sequence and size. We report here the bioinformatic identification, secondary structure comparison, and functional analysis of the smallest known vertebrate TRs from five teleost fishes. The teleost TRs (312-348 nucleotides) are significantly smaller than the cartilaginous fish TRs (478-559 nucleotides) and tetrapod TRs. This remarkable length reduction of teleost fish TRs correlates positively with the genome size, reflecting an unusual structural plasticity of TR during evolution. The teleost TR consists of a compact three-domain structure, lacking most of the sequences in regions that are variable in other vertebrate TR structures. The medaka and fugu TRs, when assembled with their telomerase reverse transcriptase (TERT) protein counterparts, reconstituted active and processive telomerase enzymes. Titration analysis of individual RNA domains suggests that the efficient assembly of the telomerase complex is influenced more by the telomerase reverse transcriptase (TERT) binding of the CR4-CR5 domain than the pseudoknot domain of TR. The remarkably small teleost fish TR further expands our understanding about the evolutionary divergence of vertebrate TR.

Received for publication, September 26, 2007 , and in revised form, November 21, 2007.

^* This work was supported by National Science Foundation CAREER Award MCB0642857 (to J.-L. 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Table S1 and Figs. S1-S4.

¹ To whom correspondence should be addressed. Tel.: 480-965-3650; Fax: 480-965-2747; E-mail: JLChen{at}asu.edu.

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