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J. Biol. Chem., Vol. 278, Issue 45, 44041-44048, November 7, 2003

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Interactions between the Aryl Hydrocarbon Receptor and P-TEFb

SEQUENTIAL RECRUITMENT OF TRANSCRIPTION FACTORS AND DIFFERENTIAL PHOSPHORYLATION OF C-TERMINAL DOMAIN OF RNA POLYMERASE II AT cyp1a1 PROMOTER^*

Yanan Tian, Sui Ke, Min Chen, and Tao Sheng

From the Department of Veterinary Physiology and Pharmacology, MS 4466, Texas A&M University, College Station, Texas 77843

The expression of the cytochrome P450 1A1 gene (cyp1a1) is regulated by the aryl hydrocarbon receptor (AhR), which is a ligand-activated transcription factor that mediates most toxic responses induced by 2,3,7,8tetrachlorodibenzo-p-dioxin (TCDD). In the nucleus, ligand-activated AhR binds to the xenobiotic response elements, initiating chromatin remodeling and recruitment of coregulators, leading to the formation of preinitiation complex followed by elongation. Here, we report that ligand-activated AhR recruits the positive transcription elongation factor (P-TEFb) and RNA polymerase II (RNA PII) to the cyp1a1 promoter with concomitant phosphorylation of the RNA PII carboxyl domain (CTD). Interestingly, the serine 2 and serine 5 of the heptapeptide repeats (YSPTSPS) were sequentially phosphorylated upon TCDD treatment. Inhibition of P-TEFb kinase activity by 5,6-dichloro-1--D-ribofuranosyl-benzimidazole (DRB) suppressed CTD phosphorylation (especially serine 2 phosphorylation) and abolished processive elongation without disrupting the assembly of the preinitiation complex at the cyp1a1 promoter. Remarkably, we found that activation of NF-B by TNF- selectively inhibited TCDD-induced serine 2 phosphorylation in mouse liver cells, suggesting that residue-specific phosphorylation of RNA PII CTD at the cyp1a1 promoter is an important regulatory point upon which signal "cross-talk" converges. Finally, we show that ligand-activated AhR associated with P-TEFb through the C terminus of cyclin T1, suggesting that AhR recruit the P-TEFb to the cyp1a1 promoter whereupon its kinase subunit phosphorylates the RNA PII CTD.

Received for publication, June 18, 2003 , and in revised form, August 12, 2003.

^* This research was funded in part by NIEHS, National Institutes of Health Grants ES 09859 and ES 09106 and American Heart Association Grant 0355131Y. 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.

Current address: Center for Cancer Cell Biology, University of Texas Medical Branch, Galveston, TX 77555.

To whom correspondence should be addressed. Tel.: 979-458-3599; Fax: 979-458-4485; E-mail: ytian{at}cvm.tamu.edu.

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