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J. Biol. Chem., Vol. 283, Issue 12, 7368-7378, March 21, 2008

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Promoter Influences Transcription Elongation

TATA-BOX ELEMENT MEDIATES THE ASSEMBLY OF PROCESSIVE TRANSCRIPTION COMPLEXES RESPONSIVE TO CYCLIN-DEPENDENT KINASE 9^*

Immaculada Montanuy¹, Rosana Torremocha², Cristina Hernández-Munain, and Carlos Suñé³

From the Departments of Molecular Biology and Cell Biology and Immunology, Instituto de Parasitología y Biomedicina "López Neyra," Consejo Superior de Investigaciones Científicas, 18100 Granada, Spain

Pausing of RNA polymerase II (RNAPII) during transcript elongation is an important mechanism for regulating gene expression at many genes. In this study we investigated the mechanism of regulated elongation of c-myc and human immunodeficiency virus-1 (HIV-1) using an in vitro elongation assay that reproduces the conditional block to elongation. We found that HIV-1 Tat can activate the RNAPII transcription complexes paused on c-myc by enhancing their elongation efficiency. We determined that cyclin-dependent kinase 9 (CDK9), the kinase subunit of positive transcription elongation factor b (P-TEFb) complex, regulates transcriptional elongation of c-myc and is present in transcription pre-initiation complexes formed on the c-myc promoter, which emphasizes a common mechanism of elongation control between HIV-1 and c-myc genes. We also investigated the roles of upstream elements of the HIV-1 and c-myc promoters in CDK9-activated transcriptional elongation. We found that the TATA-box element mediates the assembly of processive transcription complexes responsive to CDK9 and that specific combinations of upstream activation binding sites contribute to the recruitment of these complexes. We propose a common mechanism for elongation control at the c-myc and HIV-1 genes with an essential role for the TATA-box and specific modulatory contribution of upstream regulatory sequences, derived from the unique structure of the promoters, to form a composite surface for efficient recruitment of elongation-competent transcription complexes.

Received for publication, July 30, 2007 , and in revised form, January 23, 2008.

^* This research was supported in part by Spanish Ministry of Health Grants FIS04/0488 and FIS05/0355, Spanish Ministry of Education and Science Grant BFU2005-02806, and Fundación para la investigación y la prevención del SIDA en España (FIPSE) Grant 36473/05 (to C. S.) and by Spanish Ministry of Education and Science Grant BFU2005-01715 (to C. H. 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.

¹ Supported by a fellowship from the Consejo Superior de Investigaciones Científicas (I3P Program).

² Present address: Unidad de Genómica-PCM, Facultad de Ciencias Biológicas, Universidad Complutense de Madrid, 28040-Madrid, Spain.

³ To whom correspondence should be addressed: Instituto de Parasitología y Biomedicina "López Neyra," CSIC, Parque Tecnológico de Ciencias de la Salud, Avenida del Conocimiento s/n, Armilla, 18100 Granada, Spain. Tel.: 34-958181645; Fax: 34-958181632; E-mail: csune{at}ipb.csic.es.

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