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J. Biol. Chem., Vol. 280, Issue 29, 26788-26795, July 22, 2005

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Uncoupling the Chemical Steps of Telomere Resolution by ResT^*

Kerri Kobryn, Alex B. Burgin¶, and George Chaconas||

From the Department of Biochemistry & Molecular Biology and Department of Microbiology & Infectious Diseases, University of Calgary, Calgary, Alberta T2N 4N1, Canada and the ^¶deCode BioStructures, Bainbridge Island, Washington 98110

ResT is the telomere resolvase of the spirochete Borrelia burgdorferi, the causative agent of Lyme disease. ResT is an essential cellular function that processes replication intermediates to produce linear replicons terminated by covalently closed hairpin telomeres. ResT generates these hairpin telomeres in a reaction with mechanistic similarities to those catalyzed by type IB topoisomerases and tyrosine recombinases. We report here, that like most of the tyrosine recombinases, ResT requires interprotomer communication, likely in an in-line synapse, to activate reaction chemistry. Unlike the tyrosine recombinases, however, we infer that the cleavage and strand transfer reactions on the two sides of the replicated telomere occur nearly simultaneously. Nonetheless, the chemical steps of the forward and reverse reactions performed by ResT can occur in a non-concerted fashion (i.e. events on the two sides of the replicated telomere can occur independently). We propose that uncoupling of reaction completion on the two sides of the substrate is facilitated by an early commitment to hairpin formation that is imposed by the precleavage action of the hairpin binding module of the ResT active site.

Received for publication, April 26, 2005

^* This work was supported in part by the Canadian Institutes of Health Research (CIHR), the Canada Research Chairs Program, and the Alberta Heritage Fund for Medical Research. 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: Dépt. de Microbiologie et d'Infectiologie, Faculté de Medicine, 3001, 12e ave. Nord, Université de Sherbrooke, Sherbrooke, Québec J1H 5N4, Canada.

^|| Supported by a Scientist Award from the Alberta Heritage Fund for Medical Research and a Canada Research Chair in the Molecular Biology of Lyme Disease. To whom correspondence should be addressed: Dept. of Biochemistry & Molecular Biology, University of Calgary, 3330 Hospital Drive N.W., Calgary, AB, T2N 4N1, Canada. Tel.: 403-210-9692; Fax: 403-270-2772; E-mail: chaconas{at}ucalgary.ca.

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