Mechanism by Which the IFN-beta Enhanceosome Activates Transcription

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1999 Nov 11

PMID 10557281

Citations 37

Authors

J Yie

K Senger

D Thanos

Affiliations

Soon will be listed here.

Abstract

We demonstrate that in contrast to previous findings by using simple synthetic promoters or activators, the natural IFN-beta enhanceosome activates transcription by causing a dramatic increase of the rate by which preinitiation complexes assemble at the promoter. This effect totally depends on the recruitment of the CBP-PolII holoenzyme by the enhanceosome, because its depletion from the extract decelerates the rate of transcription. However, addition of the CBP-PolII holoenzyme back to these extracts fully restores the speed by which the enhanceosome activates transcription. Strikingly, preincubation of the enhanceosome with the CBP-RNA PolII holoenzyme complex results in instant assembly of preinitiation complexes. In contrast, individual IFN-beta gene activators function solely by increasing the number of functional preinitiation complexes and not the rate of their assembly. Thus, fast recruitment of the CBP-RNA PolII holoenzyme complex is critical for the rapid activation of IFN-beta gene expression by virus infection.

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References

Kee B, Arias J, Montminy M . Adaptor-mediated recruitment of RNA polymerase II to a signal-dependent activator. J Biol Chem. 1996; 271(5):2373-5. DOI: 10.1074/jbc.271.5.2373. View

Walters M, Fiering S, Eidemiller J, Magis W, Groudine M, Martin D . Enhancers increase the probability but not the level of gene expression. Proc Natl Acad Sci U S A. 1995; 92(15):7125-9. PMC: 41484. DOI: 10.1073/pnas.92.15.7125. View

Kim M, Peterson D . Oct-1 protein promotes functional transcription complex assembly on the mouse mammary tumor virus promoter. J Biol Chem. 1995; 270(46):27823-8. View

Yie J, Merika M, Munshi N, Chen G, Thanos D . The role of HMG I(Y) in the assembly and function of the IFN-beta enhanceosome. EMBO J. 1999; 18(11):3074-89. PMC: 1171389. DOI: 10.1093/emboj/18.11.3074. View

Kuras L, Struhl K . Binding of TBP to promoters in vivo is stimulated by activators and requires Pol II holoenzyme. Nature. 1999; 399(6736):609-13. DOI: 10.1038/21239. View

Sandaltzopoulos R, Becker P . Heat shock factor increases the reinitiation rate from potentiated chromatin templates. Mol Cell Biol. 1998; 18(1):361-7. PMC: 121506. DOI: 10.1128/MCB.18.1.361. View

Kim T, Kim T, Maniatis T . Efficient recruitment of TFIIB and CBP-RNA polymerase II holoenzyme by an interferon-beta enhanceosome in vitro. Proc Natl Acad Sci U S A. 1998; 95(21):12191-6. PMC: 22807. DOI: 10.1073/pnas.95.21.12191. View

Thanos D, Maniatis T . The high mobility group protein HMG I(Y) is required for NF-kappa B-dependent virus induction of the human IFN-beta gene. Cell. 1992; 71(5):777-89. DOI: 10.1016/0092-8674(92)90554-p. View

Carey M . The enhanceosome and transcriptional synergy. Cell. 1998; 92(1):5-8. DOI: 10.1016/s0092-8674(00)80893-4. View

10.

Bagchi M, Tsai S, Weigel N, Tsai M, OMalley B . Regulation of in vitro transcription by progesterone receptor. Characterization and kinetic studies. J Biol Chem. 1990; 265(9):5129-34. View

11.

Thanos D, Maniatis T . Virus induction of human IFN beta gene expression requires the assembly of an enhanceosome. Cell. 1995; 83(7):1091-100. DOI: 10.1016/0092-8674(95)90136-1. View

12.

Li X, Virbasius A, Zhu X, Green M . Enhancement of TBP binding by activators and general transcription factors. Nature. 1999; 399(6736):605-9. DOI: 10.1038/21232. View

13.

Du W, Thanos D, Maniatis T . Mechanisms of transcriptional synergism between distinct virus-inducible enhancer elements. Cell. 1993; 74(5):887-98. DOI: 10.1016/0092-8674(93)90468-6. View

14.

Triezenberg S . Structure and function of transcriptional activation domains. Curr Opin Genet Dev. 1995; 5(2):190-6. DOI: 10.1016/0959-437x(95)80007-7. View

15.

HAWLEY D, Roeder R . Functional steps in transcription initiation and reinitiation from the major late promoter in a HeLa nuclear extract. J Biol Chem. 1987; 262(8):3452-61. View

16.

Katagiri F, Yamazaki K, Horikoshi M, Roeder R, Chua N . A plant DNA-binding protein increases the number of active preinitiation complexes in a human in vitro transcription system. Genes Dev. 1990; 4(11):1899-909. DOI: 10.1101/gad.4.11.1899. View

17.

Johnson F, Krasnow M . Differential regulation of transcription preinitiation complex assembly by activator and repressor homeo domain proteins. Genes Dev. 1992; 6(11):2177-89. DOI: 10.1101/gad.6.11.2177. View

18.

Thanos D, Du W, Maniatis T . The high mobility group protein HMG I(Y) is an essential structural component of a virus-inducible enhancer complex. Cold Spring Harb Symp Quant Biol. 1993; 58:73-81. DOI: 10.1101/sqb.1993.058.01.011. View

19.

Merika M, Williams A, Chen G, Collins T, Thanos D . Recruitment of CBP/p300 by the IFN beta enhanceosome is required for synergistic activation of transcription. Mol Cell. 1998; 1(2):277-87. DOI: 10.1016/s1097-2765(00)80028-3. View

20.

Myer V, Young R . RNA polymerase II holoenzymes and subcomplexes. J Biol Chem. 1998; 273(43):27757-60. DOI: 10.1074/jbc.273.43.27757. View