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J. Biol. Chem., Vol. 279, Issue 15, 14945-14953, April 9, 2004

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End-to-End Template Jumping by the Reverse Transcriptase Encoded by the R2 Retrotransposon^*

Arkadiusz Bibillo and Thomas H. Eickbush

From the Department of Biology, University of Rochester, Rochester, New York 14627

The reverse transcriptase encoded by the non-long terminal repeat retrotransposon R2 has been shown to be able to jump from the 5'-end of one RNA template (the donor) to the 3'-end of a second RNA template (the acceptor) in the absence of preexisting sequence identity between the two templates. These jumps between RNA templates have similarity to the end-to-end template jumps described for the RNA-directed RNA polymerases encoded by certain RNA viruses. Here we describe for the first time the mechanism by which such end-to-end template jumps can occur. Most template jumps by the R2 reverse transcriptase are brought about by the enzyme's ability to add nontemplated (overhanging) nucleotides to the cDNA when it reaches the end of the donor RNA. The enzyme then anneals these overhanging nucleotides to sequences at the 3'-end of the acceptor RNA. The annealing is most efficient if it involves the terminal nucleotide(s) of the acceptor RNA but can occur to sites at least 5 nucleotides from the 3'-end. These end-to-end jumps are similar to steps proposed to be part of the integration reaction of non-long terminal repeat retrotransposons and can explain chimeric integration products derived from multiple RNA templates.

Received for publication, September 22, 2003 , and in revised form, December 30, 2003.

^* This work was supported by National Institutes of Health Grant GM42790 (to T. H. E.). 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: Human Immunodeficiency Virus Drug Resistance Program, NCI-Frederick Cancer Research and Development Center, Frederick, MD 21702.

To whom correspondence should be addressed. Tel.: 585-275-7247; Fax: 585-275-2070; E-mail: eick{at}mail.rochester.edu.

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