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Originally published In Press as doi:10.1074/jbc.M004402200 on January 26, 2001

J. Biol. Chem., Vol. 276, Issue 18, 14614-14622, May 4, 2001
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DNA Bends in TATA-binding Protein·TATA Complexes in Solution Are DNA Sequence-dependent*

Jiong WuDagger , Kay M. ParkhurstDagger , Robyn M. PowellDagger , Michael Brenowitz§, and Lawrence J. ParkhurstDagger

From the Dagger  Department of Chemistry, University of Nebraska-Lincoln, Lincoln, Nebraska 68588-0304 and the § Department of Biochemistry, Albert Einstein College of Medicine, Bronx, New York 10461

The TATA-binding protein (TBP) initiates assembly of transcription preinitiation complexes on eukaryotic class II promoters, binding to and restructuring consensus and variant "TATA box" sequences. The sequence dependence of the DNA structure in TBP·TATA complexes has been investigated in solution using fluorescence resonance energy transfer. The mean 5'dye-3'dye distance varies significantly among oligomers bearing the adenovirus major late promoter sequence (AdMLP) and five single-site variants bound to Saccharomyces cerevisiae TBP, consistent with solution bend angles for AdMLP of 76° and for the variants ranging from 30° to 62°. These solution bends contrast sharply with the corresponding co-crystal structures, which show ~80° bends for all sequences. Transcription activities for these TATA sequences are strongly correlated with the solution bend angles but not with TBP·DNA binding affinities. Our results support a model in which transcription efficiency derives primarily from the sequence-dependent structure of the TBP·TATA binary complex. Specifically, the distance distribution for the average solution structure of the TBP·TATA complex may reflect the sequence-dependent probability for the complex to assume a conformation in which the TATA box DNA is severely bent. Upon assumption of this geometry, the binary complex becomes a target for binding and correctly orienting the other components of the preinitiation complex.

* This work was supported by a Fellowship from the Program in Mathematics and Molecular Biology at the University of California-Berkeley, which is sponsored by National Science Foundation Grant DMS-9406348 (to R. M. P.), by Wheeler (to J. W.) and McDonald (to R. M. P.) Fellowships from the College of Graduate Studies, University of Nebraska-Lincoln, and by National Institutes of Health Grants GM59346 and CA76049 (to L. J. P.) and GM39929 (to M. B.).The costs of publication of this article were defrayed in part by the payment of page charges. The 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: Dept. of Chemistry, University of Nebraska-Lincoln, 525 Hamilton Hall, Lincoln, NE 68588-0304. Tel.: 402-472-3501; Fax: 402-472-2044.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.


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