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J. Biol. Chem., Vol. 282, Issue 42, 30776-30784, October 19, 2007

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Single Molecule Imaging of Tid1/Rdh54, a Rad54 Homolog That Translocates on Duplex DNA and Can Disrupt Joint Molecules^*

Amitabh V. Nimonkar, Ichiro Amitani, Ronald J. Baskin, and Stephen C. Kowalczykowski¹

From the Section of Microbiology and Section of Molecular and Cellular Biology, University of California, Davis, California 95616

The Saccharomyces cerevisiae Tid1 protein is important for the recombinational repair of double-stranded DNA breaks during meiosis. Tid1 is a member of Swi2/Snf2 family of chromatin remodeling proteins and shares homology with Rad54. Members of this family hydrolyze ATP and promote 1) chromatin remodeling, 2) DNA topology alterations, and 3) displacement of proteins from DNA. All of these activities are presumed to require translocation of the protein on DNA. Here we use single-molecule visualization to provide direct evidence for the ability of Tid1 to translocate on DNA. Tid1 translocation is ATP-dependent, and the velocities are broadly distributed, with the average being 84 ± 39 base pairs/s. Translocation is processive, with the average molecule traveling 10,000 base pairs before pausing or dissociating. Many molecules display simple monotonic unidirectional translocation, but the majority display complex translocation behavior comprising intermittent pauses, direction reversals, and velocity changes. Finally, we demonstrate that translocation by Tid1 on DNA can result in disruption of three-stranded DNA structures. The ability of Tid1 translocation to clear DNA of proteins and to migrate recombination intermediates may be of critical importance for DNA repair and chromosome dynamics.

Received for publication, June 11, 2007 , and in revised form, August 13, 2007.

^* This work was supported by National Institutes of Health Grants GM-62653 and GM-64745 (to S. C. K.). 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 supplemental Movies M1–M4.

¹ To whom correspondence should be addressed: University of California, Section of Microbiology, One Shields Ave., Briggs Hall, Rm. 310, Davis, CA 95616-8665. Tel.: 530-752-5938; Fax: 530-752-5939; E-mail: sckowalczykowski{at}ucdavis.edu.

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