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J. Biol. Chem., Vol. 279, Issue 52, 54552-54557, December 24, 2004

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lacP1 Promoter with an Extended – 10 Motif

PLEIOTROPIC EFFECTS OF CYCLIC AMP PROTEIN AT DIFFERENT STEPS OF TRANSCRIPTION INITIATION^*

Mofang Liu, Susan Garges, and Sankar Adhya

From the Laboratory of Molecular Biology, Center for Cancer Research, NCI, National Institutes of Health, Bethesda, Maryland 20892-4264

The cyclic AMP receptor protein (CRP), which activates transcription from the wild-type lacP1 promoter and most of its mutants, represses productive RNA synthesis from a lacP1 promoter variant that contains an extended -10 element, although CRP enhances RNA polymerase binding as well as open complex formation in both promoters. Moreover, abortive RNA synthesis, which is already higher in the extended -10 variant compared with the parent promoter, was further enhanced by CRP. These results, together with the observed decrease in productive RNA synthesis, indicate that CRP, while facilitating the earlier steps of initiation, inhibits transcription from the extended -10 lacP1 by hindering promoter clearance. We propose that CRP decreases energetic barriers to RNA polymerase binding, isomerization, and abortive RNA synthesis but stabilizes the abortive RNA initiating complex, which results in increasing the activation energy of the transition state before the elongation complex. The results demonstrate for the first time that a DNA-binding regulatory protein acts as an activator or a repressor in different steps of the transcription initiation pathway because of the energetic differences of the intermediate complex in the same promoter.

Received for publication, July 29, 2004 , and in revised form, September 21, 2004.

^* 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.

Present address: Office of Biodefense Research Affairs, Division of Microbiology and Infectious Diseases, NIAID, National Institutes of Health, Bethesda, MD 20892-6605.

To whom correspondence should be addressed: Laboratory of Molecular Biology, NCI, National Institutes of Health, 37 Convent Dr., Rm. 5138, Bethesda, MD 20892-4264. Tel.: 301-496-2495; Fax: 301-480-7687; E-mail: sadhya{at}helix.nih.gov.

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