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J. Biol. Chem., Vol. 280, Issue 51, 42423-42432, December 23, 2005

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Analysis of RovA, a Transcriptional Regulator of Yersinia pseudotuberculosis Virulence That Acts through Antirepression and Direct Transcriptional Activation^*

Hien J. Tran, Ann Kathrin Heroven, Lars Winkler, Thomas Spreter, Birgitta Beatrix, and Petra Dersch1

From the Junior Research Group 6, Robert Koch-Institut, Nordufer 20, 13353 Berlin, Germany and the Freie Universität Berlin, Takustrasse 6, 14195 Berlin, Germany

The transcription factor RovA of Yersinia pseudotuberculosis and analogous proteins in other Enterobacteriaceae activate the expression of virulence genes that play a crucial role in stress adaptation and pathogenesis. In this study, we demonstrate that the RovA protein forms dimers independent of DNA binding, stimulates RNA polymerase, most likely via its C-terminal domain, and counteracts transcriptional repression by the histone-like protein H-NS. As the molecular function of the RovA family is largely uncharacterized, random mutagenesis and terminal deletions were used to identify functionally important domains. Our analysis showed that a winged-helix motif in the center of the molecule is essential and directly involved in DNA binding. Terminal deletions and amino acid changes within both termini also abrogate RovA activation and DNA-binding functions, most likely due to their implication in dimer formation. Finally, we show that the last four amino acids of RovA are crucial for activation of gene transcription. Successive deletions of these residues result in a continuous loss of RovA activity. Their removal reduced the capacity of RovA to activate RNA polymerase and abolished transcription of RovA-activated promoters in the presence of H-NS, although dimerization and DNA binding functions were retained. Our structural model implies that the final amino acids of RovA play a role in protein-protein interactions, adjusting RovA activity.

Received for publication, April 25, 2005 , and in revised form, October 24, 2005.

^* This work was supported by Grant DE 616/3 from the Deutsche Forschungsgemeinschaft (to P. 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.

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

¹ To whom correspondence should be addressed. Tel.: 49-30-4547-2373; Fax: 49-30-4547-2328; E-mail: derschp{at}rki.de.

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