Yeast Ume6p Repressor Permits Activator Binding but Restricts TBP Binding at the HOP1 Promoter

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2003 Jun 12

PMID 12799429

Citations 6

Authors

Mitsuhiro Shimizu

Keiko Takahashi

Teresa M Lamb

Heisaburo Shindo

Aaron P Mitchell

Affiliations

Soon will be listed here.

Abstract

Ume6p plays essential roles in the regulation of early meiotic genes in Saccharomyces cerevisiae. Ume6p exerts repression via recruitment of the Sin3p-Rpd3p histone deacetylase and Isw2p chromatin remodeling complexes. The transcriptional step that is ultimately inhibited by Ume6p is unknown. Here, in vivo footprinting shows that transcriptional activators Hap1p and Abf1p occupy upstream sites in repressed and derepressed promoters. In contrast, chromatin immunoprecipitation shows that TATA box-binding protein (TBP)- promoter binding is reduced upon repression of HOP1. Fusion of TBP to a zinc cluster DNA binding domain relieves repression at a HOP1 promoter modified to include the zinc cluster target site. We suggest that TBP binding is inhibited through chromatin modification by the Sin3p-Rpd3p and Isw2p complexes recruited by Ume6p.

Citing Articles

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References

Vershon A, Hollingsworth N, Johnson A . Meiotic induction of the yeast HOP1 gene is controlled by positive and negative regulatory sites. Mol Cell Biol. 1992; 12(9):3706-14. PMC: 360227. DOI: 10.1128/mcb.12.9.3706-3714.1992. 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

Mitchell A . Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiol Rev. 1994; 58(1):56-70. PMC: 372953. DOI: 10.1128/mr.58.1.56-70.1994. View

Imbalzano A, Kwon H, Green M, Kingston R . Facilitated binding of TATA-binding protein to nucleosomal DNA. Nature. 1994; 370(6489):481-5. DOI: 10.1038/370481a0. View

Chatterjee S, Struhl K . Connecting a promoter-bound protein to TBP bypasses the need for a transcriptional activation domain. Nature. 1995; 374(6525):820-2. DOI: 10.1038/374820a0. View

Dudley A, Rougeulle C, Winston F . The Spt components of SAGA facilitate TBP binding to a promoter at a post-activator-binding step in vivo. Genes Dev. 1999; 13(22):2940-5. PMC: 317152. DOI: 10.1101/gad.13.22.2940. View

Kuo M, Allis C . In vivo cross-linking and immunoprecipitation for studying dynamic Protein:DNA associations in a chromatin environment. Methods. 1999; 19(3):425-33. DOI: 10.1006/meth.1999.0879. View

Belotserkovskaya R, Sterner D, Deng M, Sayre M, Lieberman P, Berger S . Inhibition of TATA-binding protein function by SAGA subunits Spt3 and Spt8 at Gcn4-activated promoters. Mol Cell Biol. 1999; 20(2):634-47. PMC: 85153. DOI: 10.1128/MCB.20.2.634-647.2000. View

Xiao Y, Mitchell A . Shared roles of yeast glycogen synthase kinase 3 family members in nitrogen-responsive phosphorylation of meiotic regulator Ume6p. Mol Cell Biol. 2000; 20(15):5447-53. PMC: 85996. DOI: 10.1128/MCB.20.15.5447-5453.2000. View

10.

Goldmark J, Fazzio T, Estep P, Church G, Tsukiyama T . The Isw2 chromatin remodeling complex represses early meiotic genes upon recruitment by Ume6p. Cell. 2000; 103(3):423-33. DOI: 10.1016/s0092-8674(00)00134-3. View

11.

Sewack G, Ellis T, Hansen U . Binding of TATA binding protein to a naturally positioned nucleosome is facilitated by histone acetylation. Mol Cell Biol. 2001; 21(4):1404-15. PMC: 99592. DOI: 10.1128/MCB.21.4.1404-1415.2001. View

12.

Kent N, Karabetsou N, Politis P, Mellor J . In vivo chromatin remodeling by yeast ISWI homologs Isw1p and Isw2p. Genes Dev. 2001; 15(5):619-26. PMC: 312638. DOI: 10.1101/gad.190301. View

13.

Deckert J, Struhl K . Histone acetylation at promoters is differentially affected by specific activators and repressors. Mol Cell Biol. 2001; 21(8):2726-35. PMC: 86903. DOI: 10.1128/MCB.21.8.2726-2735.2001. View

14.

Sekinger E, Gross D . Silenced chromatin is permissive to activator binding and PIC recruitment. Cell. 2001; 105(3):403-14. DOI: 10.1016/s0092-8674(01)00329-4. View

15.

Breiling A, Turner B, Bianchi M, Orlando V . General transcription factors bind promoters repressed by Polycomb group proteins. Nature. 2001; 412(6847):651-5. DOI: 10.1038/35088090. View

16.

Fazzio T, Kooperberg C, Goldmark J, Neal C, Basom R, Delrow J . Widespread collaboration of Isw2 and Sin3-Rpd3 chromatin remodeling complexes in transcriptional repression. Mol Cell Biol. 2001; 21(19):6450-60. PMC: 99792. DOI: 10.1128/MCB.21.19.6450-6460.2001. View

17.

Suka N, Suka Y, Carmen A, Wu J, Grunstein M . Highly specific antibodies determine histone acetylation site usage in yeast heterochromatin and euchromatin. Mol Cell. 2001; 8(2):473-9. DOI: 10.1016/s1097-2765(01)00301-x. View

18.

Davie J, Trumbly R, Dent S . Histone-dependent association of Tup1-Ssn6 with repressed genes in vivo. Mol Cell Biol. 2002; 22(3):693-703. PMC: 133554. DOI: 10.1128/MCB.22.3.693-703.2002. View

19.

Verdone L, Wu J, Van Riper K, Kacherovsky N, Vogelauer M, Young E . Hyperacetylation of chromatin at the ADH2 promoter allows Adr1 to bind in repressed conditions. EMBO J. 2002; 21(5):1101-11. PMC: 125900. DOI: 10.1093/emboj/21.5.1101. View

20.

Deckert J, Struhl K . Targeted recruitment of Rpd3 histone deacetylase represses transcription by inhibiting recruitment of Swi/Snf, SAGA, and TATA binding protein. Mol Cell Biol. 2002; 22(18):6458-70. PMC: 135627. DOI: 10.1128/MCB.22.18.6458-6470.2002. View