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J. Biol. Chem., Vol. 278, Issue 25, 22250-22256, June 20, 2003

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The Mechanism of Regulation of Bacteriophage p_R Promoter Activity by Escherichia coli DnaA Protein^*

Monika Glinkowska , Jerzy Majka  ¶, Walter Messer  || and Grzegorz Wegrzyn  ** 

From the Department of Molecular Biology, University of Gdansk, Kladki 24, 80-822 Gdansk, Poland, the Max-Planck-Institute for Molecular Genetics, Ihnestrasse 73, D-14195 Berlin-Dahlem, Germany, and the ^**Institute of Oceanology, Polish Academy of Sciences, Sw. Wojciecha 5, 81-347 Gdynia, Poland

Apart from its function as an initiator of DNA replication, the Escherichia coli DnaA protein is also a specific transcription factor. It activates and represses a number of promoters. However, mechanisms of transcription stimulation by DnaA remained unknown. Bacteriophage p_R promoter is one of the promoters activated by DnaA. It was reported previously that DnaA binds downstream of the p_R promoter and perhaps interacts with the RNA polymerase subunit. Here we demonstrate that DnaA positively regulates transcription from p_R by stimulation of two steps in transcription initiation: RNA polymerase binding to the promoter region and promoter escape. For this transcription activation, two weak DnaA boxes located downstream of p_R are necessary and sufficient. Such a mechanism of transcription activation and location of the activator-binding sites relative to the transcription start point are unusual in prokaryotes. Changes in the distance between the transcription start point and the first DnaA box by 5 and 10 bp and alterations in the orientation of these boxes did not abolish the stimulation of transcription by DnaA, but the efficiency of the promoter activation was different for various mutations. It seems plausible that formation of higher order nucleoprotein structures, involving DNA looping, is necessary for effective stimulation of the p_R promoter. At high concentrations, DnaA is a repressor of p_R rather than an activator. This repression was found to be because of inhibition of RNA polymerase binding to the promoter region.

Received for publication, December 9, 2002 , and in revised form, March 24, 2003.

^* This work was supported in part by Polish State Committee for Scientific Research Grant 3 P04A 049 24 (to G. W.), National Institutes of Health Fogarty International Research Collaboration Award (FIRCA) Program Grant TW01244 (to G. W. and Dr. V. James Hernandez, State University of New York, Buffalo, NY), and Volkswagen-Stiftung Grant I/74 639 (to G. W. and W. M.). 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.

^¶ Supported by Alexander von Humboldt Foundation Fellowship IVPOL 1063505 STP.

^|| Supported by the Fonds der chemischen Industrie (Germany).

Supported by Foundation for Polish Science subsidy 14/2000. To whom correspondence should be addressed: Dept. of Molecular Biology, University of Gdansk, Kladki 24, 80-822 Gdansk, Poland. Tel.: 48-58-346-3014; Fax: 48-58-301-0072; E-mail: wegrzyn{at}biotech.univ.gda.pl.

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