Cocrystal Structure of YY1 Bound to the Adeno-associated Virus P5 Initiator

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1996 Nov 26

PMID 8942976

Citations 70

Authors

H B Houbaviy

A Usheva

T Shenk

S K Burley

Affiliations

Soon will be listed here.

Abstract

Ying-Yang 1 protein (YY1) supports specific, unidirectional initiation of messenger RNA production by RNA polymerase II from two adjacent start sites in the adeno-associated virus P5 promoter, a process which is independent of the TATA box-binding protein (TBP). The 2.5-A resolution YY1-initiator element cocrystal structure reveals four zinc fingers recognizing a YY1-binding consensus sequence. Upstream of the transcription start sites protein-DNA contacts involve both strands and downstream they are virtually restricted to the template strand, permitting access to the active center of RNA polymerase II and ensuring specificity and directionality. The observed pattern of protein-DNA contacts also explains YY1 binding to a preformed transcription bubble, and YY1 binding to a DNA/RNA hybrid analog of the P5 promoter region containing a nascent RNA transcript. A model is proposed for YY1-directed, TBP-independent transcription initiation.

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References

Zawel L, Kumar K, Reinberg D . Recycling of the general transcription factors during RNA polymerase II transcription. Genes Dev. 1995; 9(12):1479-90. DOI: 10.1101/gad.9.12.1479. View

Nikolov D, Chen H, Halay E, Usheva A, Hisatake K, Lee D . Crystal structure of a TFIIB-TBP-TATA-element ternary complex. Nature. 1995; 377(6545):119-28. DOI: 10.1038/377119a0. View

Natesan S, Gilman M . DNA bending and orientation-dependent function of YY1 in the c-fos promoter. Genes Dev. 1993; 7(12B):2497-509. DOI: 10.1101/gad.7.12b.2497. View

Roy A, Malik S, Meisterernst M, Roeder R . An alternative pathway for transcription initiation involving TFII-I. Nature. 1993; 365(6444):355-9. DOI: 10.1038/365355a0. View

Smale S, Baltimore D . The "initiator" as a transcription control element. Cell. 1989; 57(1):103-13. DOI: 10.1016/0092-8674(89)90176-1. View

Houbaviy H, Usheva A, Shenk T, Burley S . Cocrystal structure of YY1 bound to the adeno-associated virus P5 initiator. Proc Natl Acad Sci U S A. 1996; 93(24):13577-82. PMC: 19349. DOI: 10.1073/pnas.93.24.13577. View

Hahn S . The Yin and the Yang of mammalian transcription. Curr Biol. 1992; 2(3):152-4. DOI: 10.1016/0960-9822(92)90268-f. View

Jennings E, Shenk T . DNA binding sites for the transcriptional activator/repressor YY1. Nucleic Acids Res. 1995; 23(21):4457-65. PMC: 307404. DOI: 10.1093/nar/23.21.4457. View

Burley S, Petsko G . Weakly polar interactions in proteins. Adv Protein Chem. 1988; 39:125-89. DOI: 10.1016/s0065-3233(08)60376-9. View

10.

Parvin J, Sharp P . DNA topology and a minimal set of basal factors for transcription by RNA polymerase II. Cell. 1993; 73(3):533-40. DOI: 10.1016/0092-8674(93)90140-l. View

11.

Javahery R, Khachi A, Lo K, Smale S . DNA sequence requirements for transcriptional initiator activity in mammalian cells. Mol Cell Biol. 1994; 14(1):116-27. PMC: 358362. DOI: 10.1128/mcb.14.1.116-127.1994. View

12.

Burley S . The TATA box binding protein. Curr Opin Struct Biol. 1996; 6(1):69-75. DOI: 10.1016/s0959-440x(96)80097-2. View

13.

Seto E, Shi Y, Shenk T . YY1 is an initiator sequence-binding protein that directs and activates transcription in vitro. Nature. 1991; 354(6350):241-5. DOI: 10.1038/354241a0. View

14.

Gill G . Transcriptional initiation. Taking the initiative. Curr Biol. 1994; 4(4):374-6. DOI: 10.1016/s0960-9822(00)00084-1. View

15.

Kim J, Nikolov D, Burley S . Co-crystal structure of TBP recognizing the minor groove of a TATA element. Nature. 1993; 365(6446):520-7. DOI: 10.1038/365520a0. View

16.

Pavletich N, Pabo C . Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A. Science. 1991; 252(5007):809-17. DOI: 10.1126/science.2028256. View

17.

Studier F, Rosenberg A, Dunn J, Dubendorff J . Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 1990; 185:60-89. DOI: 10.1016/0076-6879(90)85008-c. View

18.

Wobbe C, Struhl K . Yeast and human TATA-binding proteins have nearly identical DNA sequence requirements for transcription in vitro. Mol Cell Biol. 1990; 10(8):3859-67. PMC: 360896. DOI: 10.1128/mcb.10.8.3859-3867.1990. View

19.

Bucher P, Trifonov E . Compilation and analysis of eukaryotic POL II promoter sequences. Nucleic Acids Res. 1986; 14(24):10009-26. PMC: 341352. DOI: 10.1093/nar/14.24.10009. View

20.

Roeder R . The complexities of eukaryotic transcription initiation: regulation of preinitiation complex assembly. Trends Biochem Sci. 1991; 16(11):402-8. DOI: 10.1016/0968-0004(91)90164-q. View