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J. Biol. Chem., Vol. 278, Issue 45, 44068-44074, November 7, 2003

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Role of XRCC1 in the Coordination and Stimulation of Oxidative DNA Damage Repair Initiated by the DNA Glycosylase hOGG1^*

Stéphanie Marsin, Antonio E. Vidal¶, Marguerite Sossou, Josiane Ménissier-de Murcia||, Florence Le Page, Serge Boiteux, Gilbert de Murcia||, and J. Pablo Radicella**

From the Département de Radiobiologie et Radiopathologie, UMR 217 CNRS, Commissariat à l'Energie Atomique, BP6, F-92265 Fontenay aux Roses and the ^||UPR 9003 CNRS, Université Louis Pasteur, Ecole Supérieure de Biotechnologie de Strasbourg, BP10413, F-67412 Illkirch, France

XRCC1 participates in DNA single strand break and base excision repair (BER) to preserve genetic stability in mammalian cells. XRCC1 participation in these pathways is mediated by its interactions with several of the acting enzymes. Here, we report that XRCC1 interacts physically and functionally with hOGG1, the human DNA glycosylase that initiates the repair by BER of the mutagenic oxidized base 8-oxoguanine. This interaction leads to a 2- to 3-fold stimulation of the DNA glycosylase activity of hOGG1. XRCC1 stimulates the formation of the hOGG1 Schiff-base DNA intermediate without interfering with the endonuclease activity of APE1, the second enzyme in the pathway. On the contrary, the stimulation in the appearance of the incision product seems to reflect the addition of the effects of XRCC1 on the two first enzymes of the pathway. The data presented support a model by which XRCC1 will pass on the DNA intermediate from hOGG1 to the endonuclease APE1. This results in an acceleration of the overall repair process of oxidized purines to yield an APE1-cleaved abasic site, which can be used as a substrate by DNA polymerase . More importantly, the results unveil a highly coordinated mechanism by which XRCC1, through its multiple protein-protein interactions, extends its orchestrating role from the base excision step to the resealing of the repaired DNA strand.

Received for publication, June 11, 2003 , and in revised form, August 18, 2003.

^* This work was supported in part by the Commissariat à l' Energie Atomique, the CNRS, Electricité de France, and l'Association pour la Recherche contre le Cancer. 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.

Both authors contributed equally to this work.

^¶ A recipient of a postdoctoral fellowship from the Ministerio de Educacion y Cultura, Spain. Present address: Laboratory of Genomic Integrity, NICHD, National Institutes of Health, Bethesda, MD 20892.

^** To whom correspondence should be addressed. Tel.: 33-1-46-54-88-57; Fax: 33-1-46-54-88-59; E-mail: jpradicella{at}cea.fr.

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