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J. Biol. Chem., Vol. 279, Issue 32, 33192-33198, August 6, 2004

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Reverse Gyrase Recruitment to DNA after UV Light Irradiation in Sulfolobus solfataricus^*

Alessandra Napoli, Anna Valenti, Vincenzo Salerno, Marc Nadal, Florence Garnier, Mosè Rossi, and Maria Ciaramella¶

From the Institute of Protein Biochemistry, Consiglio Nazionale delle Ricerche, Via P. Castellino 111, 80131 Naples, Italy and the Université de Versailles-Saint-Quentin-en-Yvelines, Laboratoire de Génétique et Biologie Cellulaire, CNRS FRE 2445, Equipe Microbiologie, Btiment Buffon, 45 Avenue des Etats-Unis, 78035 Versailles Cedex, France

Induction of DNA damage triggers a complex biological response concerning not only repair systems but also virtually every cell function. DNA topoisomerases regulate the level of DNA supercoiling in all DNA transactions. Reverse gyrase is a peculiar DNA topoisomerase, specific to hyperthermophilic microorganisms, which contains a helicase and a topoisomerase IA domain that has the unique ability to introduce positive supercoiling into DNA molecules. We show here that reverse gyrase of the archaean Sulfolobus solfataricus is mobilized to DNA in vivo after UV irradiation. The enzyme, either purified or in cell extracts, forms stable covalent complexes with UV-damaged DNA in vitro. We also show that the reverse gyrase translocation to DNA in vivo and the stabilization of covalent complexes in vitro are specific effects of UV light irradiation and do not occur with the intercalating agent actinomycin D. Our results suggest that reverse gyrase might participate, directly or indirectly, in the cell response to UV light-induced DNA damage. This is the first direct evidence of the recruitment of a topoisomerase IA enzyme to DNA after the induction of DNA damage. The interaction between helicase and topoisomerase activities has been previously proposed to facilitate aspects of DNA replication or recombination in both Bacteria and Eukarya. Our results suggest a general role of the association of such activities in maintaining genome integrity and a mutual effect of DNA topology and repair.

Received for publication, March 8, 2004 , and in revised form, May 7, 2004.

^* This work was supported in part by the Consiglio Nazionale delle Ricerche-Ministero dell'Istruzione dell'Università e della Ricerca Project Grant Legge 449/97-DM 30/10/2000 and the Ministero dell'Istruzione dell'Università e della Ricerca-Decreto Direttoriale Project Grant 1105/2002. 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.

^¶ To whom correspondence should be addressed. Tel.: 39-081-613-2247; Fax: 39-081-613-2248; E-mail: m.ciaramella{at}ibp.cnr.it.

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