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J. Biol. Chem., Vol. 281, Issue 39, 28811-28821, September 29, 2006

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RuvABC Is Required to Resolve Holliday Junctions That Accumulate following Replication on Damaged Templates in Escherichia coli^*

From the Department of Biology, Portland State University, Portland, Oregon 97207

RuvABC is a complex that promotes branch migration and resolution of Holliday junctions. Although ruv mutants are hypersensitive to UV irradiation, the molecular event(s) that necessitate RuvABC processing in vivo are not known. Here, we used a combination of two-dimensional gel analysis and electron microscopy to reveal that although ruvAB and ruvC mutants are able to resume replication following arrest at UV-induced lesions, molecules that replicate in the presence of DNA damage accumulate unresolved Holliday junctions. The failure to resolve the Holliday junctions on the fully replicated molecules correlates with a delayed loss of genomic integrity that is likely to account for the loss of viability in these cells. The strand exchange intermediates that accumulate in ruv mutants are distinct from those observed at arrested replication forks and are not subject to resolution by RecG. These results indicate that the Holliday junctions observed in ruv mutants are intermediates of a repair pathway that is distinct from that of the recovery of arrested replication forks. A model is proposed in which RuvABC is required to resolve junctions that arise during the repair of a subset of nonarresting lesions after replication has passed through the template.

Received for publication, April 25, 2006 , and in revised form, July 12, 2006.

^* This work was supported by National Science Foundation Career Award MCB0551798, NIGMS, National Institutes of Health, National Research Service Award F32 GM068566 (to C. T. C.), and a Sigma Xi grant-in-aid for research (to J. R. D.). 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.

¹ To whom correspondence should be addressed: NIDDK, National Institutes of Health, GBB, 5 Memorial Dr. MSC 0538, Bethesda, MD 20892. Tel.: 301-496-4637; Fax: 301-496-9878; E-mail: donaldsonjr{at}niddk.nih.gov.

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