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J. Biol. Chem., Vol. 279, Issue 30, 31259-31267, July 23, 2004

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Photocross-linking of the RNA Polymerase I Preinitiation and Immediate Postinitiation Complexes

IMPLICATIONS FOR PROMOTER RECRUITMENT^*

Anka Bric, Catherine A. Radebaugh, and Marvin R. Paule

From the Department of Biochemistry and Molecular Biology, Colorado State University, Fort Collins, Colorado 80523-1870

The architecture of eukaryotic rRNA transcription complexes was analyzed, revealing facts significant to the RNA polymerase (pol) I initiation process. Functional initiation and elongation complexes were mapped by site-specific photocross-linking to template DNA. Polymerase I is recruited to the promoter via protein-protein interactions with DNA-bound transcription initiation factor-IB. The latter's TATA-binding protein (TBP) and TAFs photocross-link to the promoter from –78 to +10 relative to the tis (+1). Although TBP does not bind DNA using its TATA-binding saddle, it does photocross-link to a 22-bp sequence that does not resemble a TATA box. Only TAF_I96 (the mammalian TAF_I 68, yeast Rrn7p homolog) overlaps significantly with the DNA interaction cleft of pol I based on modeling to the pol II crystal structure. None of the pol I-specific subunits that are localized on the lips of the cleft (A49 and A34.5) or the pol I-specific stalk (A43 and A14) cross-link to DNA. Pol I does not extend significantly upstream of the promoter-proximal border of the factor complex (–11 to –14), and similarly in the promoter proximal elongation complex, the enzyme does not contact DNA upstream of its normal exit from the cleft.

Received for publication, October 28, 2003 , and in revised form, April 23, 2004.

^* This work was supported by U.S. Public Health Service Grant GM22580 (to M. R. P.). 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.

To whom correspondence should be addressed. Tel.: 970-491-6748; Fax: 907-491-0494; E-mail: mpaule{at}lamar.colostate.edu.

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