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J. Biol. Chem., Vol. 283, Issue 17, 11260-11269, April 25, 2008

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A Dynamic Polymerase Exchange with Escherichia coli DNA Polymerase IV Replacing DNA Polymerase III on the Sliding Clamp^*

Asako Furukohri, Myron F. Goodman, and Hisaji Maki¹

From the Department of Molecular Biology, Graduate School of Biological Sciences, Nara Institute of Science and Technology, Ikoma, Nara 630-0192, Japan and the Department of Biological Sciences and Chemistry, University of Southern California, Los Angeles, California 90089

An assay that measures synchronized, processive DNA replication by Escherichia coli DNA polymerase III holoenzyme was used to reveal replacement of pol III by the specialized lesion bypass DNA polymerase IV when the replicative polymerase is stalled. When idled replication is restarted, a rapid burst of pol III-catalyzed synthesis accompanied by 7-kb full-length products is strongly inhibited by the presence of pol IV. The production of slower-forming, shorter length DNA reflects a rapid takeover of DNA synthesis by pol IV. Here we demonstrate that pol IV rapidly (<15 s) obstructs the stable interaction between pol III* and the β clamp (the lifetime of the complex is >5 min), causing the removal of pol III* from template DNA. We propose that the rapid replacement of pol III* on the β clamp with pol IV is mediated by two processes, an interaction between pol IV and the β clamp and a separate interaction between pol IV and pol III*. This newly discovered property of pol IV facilitates a dynamic exchange between the two free polymerases at the primer terminus. Our study suggests a model in which the interaction between pol III* and the β clamp is mediated by pol IV to ensure that DNA replication proceeds with minimal interruption.

Received for publication, November 27, 2007 , and in revised form, February 25, 2008.

^* This work was supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan 17370063 and 17013060 (to H. M.), and by National Institutes of Health Grants R37GM21422 and ES012259 (to M. F. G.). 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.

The on-line version of this article (available at http://www.jbc.org) contains two supplemental figures.

This article was selected as a Paper of the Week.

¹ To whom correspondence should be addressed. Tel.: 81-743-72-5490; Fax: 81-743-72-5499; E-mail: maki{at}bs.naist.jp.

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