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J. Biol. Chem., Vol. 280, Issue 28, 26177-26184, July 15, 2005

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A Superhelical Spiral in the Escherichia coli DNA Gyrase A C-terminal Domain Imparts Unidirectional Supercoiling Bias^*

Alexander J. Ruthenburg, Daina M. Graybosch¶, John C. Huetsch||, and Gregory L. Verdine**

From the Departments of Chemistry and Chemical Biology and ^**Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts 02138

DNA gyrase is unique among type II topoisomerases in that its DNA supercoiling activity is unidirectional. The C-terminal domain of the gyrase A subunit (GyrA-CTD) is required for this supercoiling bias. We report here the x-ray structure of the Escherichia coli GyrA-CTD (Protein Data Bank code 1ZI0). The E. coli GyrA-CTD adopts a circular-shaped -pinwheel fold first seen in the Borrelia burgdorferi GyrA-CTD. However, whereas the B. burgdorferi GyrA-CTD is flat, the E. coli GyrA-CTD is spiral. DNA relaxation assays reveal that the E. coli GyrA-CTD wraps DNA inducing substantial (+) superhelicity, while the B. burgdorferi GyrA-CTD introduces a more modest (+) superhelicity. The observation of a superhelical spiral in the present structure and that of the Bacillus stearothermophilus ParC-CTD structure suggests unexpected similarities in substrate selectivity between gyrase and Topo IV enzymes. We propose a model wherein the right-handed ((+) solenoidal) wrapping of DNA around the E. coli GyrA-CTD enforces unidirectional (–) DNA supercoiling.

Received for publication, March 15, 2005 , and in revised form, April 27, 2005.

^* This project was supported by National Institutes of Health Grant GM51330. 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 text, references, Figs. 1–3, and a table.

The atomic coordinates and structure factors (code 1ZI0) have been deposited in the Protein Data Bank, Research Collaboratory for Structural Bioinformatics, Rutgers University, New Brunswick, NJ (http://www.rcsb.org/).

Supported by a graduate research fellowship from the National Science Foundation.

^¶ Supported by a National Institutes of Health training grant.

^|| Supported by a Robert Flack Norris undergraduate fellowship from the American Chemical Society.

To whom correspondence should be addressed. Tel.: 617-495-5323; Fax: 617-495-8755; E-mail: verdine{at}chemistry.harvard.edu.

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