Human TFIIB in the TFIIB-TBP-TATA-Element Ternary Complex

Josh Cowgill '08, Nick Fanning '08 and Albert Coombs III '07


Contents


I. Introduction

TFIIB is a eukaryotic general transcription factor (GTF) that is necessary for both RNA polymerase II promoter binding and promoter clearance. With regard to only the necessary GTF's, TFIID, which contains TATA binding protein (TBP), binds the TATA-element on DNA and starts the formation of the transcriptional pre-initiation complex. TFIIB binds next, and together the DNA, TBP, and TFIIB form a molecular binding platform that is recognized by RNA polymerase II. In this ternary complex, the role of TFIIB is to bind both the DNA and TBP to create stabilizing interactions.

II. TFIIB General Structure

The protein's N-terminal portion contains a putative Zinc-binding sequence that plays a major role in the successful binding of RNA polymerase II. This N-terminal region does not, however, have a very large role in this ternary complex and thus is not shown here. Core TFIIB, on the other hand, is extremely important to this ternary complex, and it has a two-domain alpha-helical structure . The core region/C-terminal region together consist of two 84-amino-acid direct repeats. Overall, the protein has dimensions of 65A x 32A x 32A.


III. Core TFIIB Specifics

As previously mentioned, core TFIIB has two nearly identical domains, which are connected by a short linker region and rotated by 90 degrees with respect to one another. Each domain consists of five alpha-helices (domain I has helices BH1-BH5, while domain II has helices BH1'-BH5') arranged in a compact globular fashion with BH3/BH3' in the hydrophobic core . Just past BH5' in the C-terminal direction is the short alpha helix BH6' and a random coil segment that extends to the molecule's C-terminus . These two structures form the molecule's C-terminal region and have no analogs in domain I. The solitary molecule is held together by limited interdomain hydrophobic interactions between residues in BH4 and the BH4'-BH5' loop and between residues in BH1' and the BH3-BH4 loop .


IV. Interactions of the Ternary Complex

TBP binds DNA at the TATA-element, and as a subunit of TFIID it is the first protein to bind DNA during eukaryotic transcription initiation. TBP recognizes the TATA-element via an induced-fit mechanism where beta-sheets on TBP insert into the DNA's minor groove . Phenylalanine residues near these beta-sheets intercalate between bases in the DNA and cause two distinct kinks . These kinks generate a sterically favorable complementary interaction surface for TBP and the DNA.

It is this TBP-TATA-element complex that is recognized by TFIIB. TFIIB acts as a clamp holding TBP tightly to the TATA-element DNA . It does this by binding TBP in its cleft between the plane of beta-sheets and alpha-helices and by binding backbones of both coding and non-coding DNA upstream and downstream of the TATA-element (see section V for specifics). This binding is non-sequence specific because TFIIB does not contact any of the DNA bases. Overall ternary complex stability comes from favorable Van der Waals and electrostatic interactions between TFIIB and the TBP-TATA-element complex.


V. TFIIB Specifics in the Ternary Complex

As previously mentioned, TFIIB binds the DNA backbone of the coding region and non-coding region both upstream and downstream of the TATA-element in a non-sequence specific manner . It does this by using many positively charged basic residues to form charge-charge interactions with the negatively charged DNA backbone . As we will see later on, many basic residues of TFIIB also interact with the acidic C-terminal stirrup of TBP . In the ternary complex overall, this positive charge provided by TFIIB helps to cancel much of the negative charge of the acidic C-terminal stirrup and the negative charge of the DNA backbone, thus greatly stabilizing the whole complex.

The so-called "C-terminal stirrup" of TBP constitutes the primary binding site for TFIIB in this ternary complex. Residues 143-147 on the stirrup form salt bridges, hydrogen bonds, and Van der Waals contacts with at least ten TFIIB residues. Residues on TBP are listed in red, residues on TFIIB are listed in blue, and all residues are displayed in white. On the C-terminal stirrup alone, Glu146--> Lys188 form a salt bridge ; Glu144--> Arg169, Glu146--> Tyr165, and Glu146--> Phe177 form hydrogen bonds , while Tyr143--> Leu208, Glu144--> Phe195, Pro145--> Ser249, Pro145--> Pro250, Glu146--> Thr176, Leu147--> Phe177, and Leu147--> Gly192 all make Van der Waals contacts .

In addition to the C-terminal stirrup, residues on TBP's alpha-helix H1' also interact with at least two residues on TFIIB. Tyr135--> Asp207 form a hydrogen bond , while Glu131--> Leu208 and Tyr135--> Leu208 form Van der Waals contacts . Finally, Lys197, located near TBP's C-terminus, forms a salt bridge with TFIIB's Asp243 .

The overall purpose of TFIIB in this ternary complex is to stabilize TBP to the TATA-element DNA and to create a stable binding platform for RNA polymerase II. Perhaps an even more interesting region of TFIIB is its N-terminal zinc-ribbon. The N-terminus plays a huge role in RNA polymerase II binding and promoter clearance. We believe that we know most of the functions of this region, but the crystal structure of this region on human TFIIB has not yet been determined.



VI. References

Kosa PF, Ghosh G, DeDecker BS, and Sigler PB. The 2.1-A crystal structure of an archaeal preinitiation complex: TATA-box-binding protein/transcription factor (II)B core/TATA-box. Proc Natl Acad Sci USA. 1997. 94(12): 6042-6047.

Nikolov DB, Chen H, Halay ED, Usheva AA, Hisatake K, Lee DK, Roeder RG, and Burley SK. Crystal structure of a TFIIB-TBP-TATA-element ternary complex. Nature. 1995. 377: 119-128.

Nikolov DB, Chen H, Hoffman A, Halay ED, Roeder RG, and Burley SK. Crystal structure of a human TATA box-binding protein/TATA element complex. Proc Natl Acad Sci USA.. 1996. 93(10): 4862-4867.

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