Regulation of Histone H3K4 Tri-methylation and PAF Complex Recruitment by the Ccr4-Not Complex

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2007 Mar 30

PMID 17392337

Citations 45

Authors

Klaas W Mulder

Arjan B Brenkman

Akiko Inagaki

Niels J F van den Broek

H Th Marc Timmers

Affiliations

Soon will be listed here.

Abstract

Efficient transcription is linked to modification of chromatin. For instance, tri-methylation of lysine 4 on histone H3 (H3K4) strongly correlates with transcriptional activity and is regulated by the Bur1/2 kinase complex. We found that the evolutionarily conserved Ccr4-Not complex is involved in establishing H3K4 tri-methylation in Saccharomyces cerevisiae. We observed synthetic lethal interactions of Ccr4-Not components with BUR1 and BUR2. Further analysis indicated that the genes encoding the Not-proteins are essential for efficient regulation of H3K4me3, but not H3K4me1/2, H3K36me2 or H3K79me2/3 levels. Moreover, regulation of H3K4me3 levels by NOT4 is independent of defects in RNA polymerase II loading. We found NOT4 to be important for ubiquitylation of histone H2B via recruitment of the PAF complex, but not for recruitment or activation of the Bur1/2 complex. These results suggest a mechanism in which the Ccr4-Not complex functions parallel to or downstream of the Bur1/2 kinase to facilitate H3K4me3 via PAF complex recruitment.

Citing Articles

N-terminal acetylation of Set1-COMPASS fine-tunes H3K4 methylation patterns.

Woo H, Oh J, Cho Y, Oh G, Kim S, Dan K Sci Adv. 2024; 10(28):eadl6280.

PMID: 38996018 PMC: 11244526. DOI: 10.1126/sciadv.adl6280.

The Archer and the Prey: The Duality of PAF1C in Antiviral Immunity.

Kenaston M, Shah P Viruses. 2023; 15(5).

PMID: 37243120 PMC: 10222983. DOI: 10.3390/v15051032.

Identification and functional characterization of , a novel gene involved in both azoles susceptibility and hypha development in .

Huang M, Yang L, Zhou L, Sun C, Zhao W, Peng J Front Microbiol. 2022; 13:990318.

PMID: 36262330 PMC: 9575988. DOI: 10.3389/fmicb.2022.990318.

Coordinated regulation of RNA polymerase II pausing and elongation progression by PAF1.

Wang Z, Song A, Xu H, Hu S, Tao B, Peng L Sci Adv. 2022; 8(13):eabm5504.

PMID: 35363521 PMC: 11093130. DOI: 10.1126/sciadv.abm5504.

Roles of the Core Components of the Mammalian miRISC in Chromatin Biology.

La Rocca G, Cavalieri V Genes (Basel). 2022; 13(3).

PMID: 35327968 PMC: 8954937. DOI: 10.3390/genes13030414.

References

Kushnirov V . Rapid and reliable protein extraction from yeast. Yeast. 2000; 16(9):857-60. DOI: 10.1002/1097-0061(20000630)16:9<857::AID-YEA561>3.0.CO;2-B. View

Chang M, Fan H, Klein H, Denis C, Jaehning J . A complex containing RNA polymerase II, Paf1p, Cdc73p, Hpr1p, and Ccr4p plays a role in protein kinase C signaling. Mol Cell Biol. 1999; 19(2):1056-67. PMC: 116036. DOI: 10.1128/MCB.19.2.1056. View

Murray S, Udupa R, Yao S, Hartzog G, Prelich G . Phosphorylation of the RNA polymerase II carboxy-terminal domain by the Bur1 cyclin-dependent kinase. Mol Cell Biol. 2001; 21(13):4089-96. PMC: 87070. DOI: 10.1128/MCB.21.13.4089-4096.2001. View

Denis C, Chiang Y, Cui Y, Chen J . Genetic evidence supports a role for the yeast CCR4-NOT complex in transcriptional elongation. Genetics. 2001; 158(2):627-34. PMC: 1461659. DOI: 10.1093/genetics/158.2.627. View

Roguev A, Schaft D, Shevchenko A, Pijnappel W, Wilm M, Aasland R . The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4. EMBO J. 2001; 20(24):7137-48. PMC: 125774. DOI: 10.1093/emboj/20.24.7137. View

Nagy P, Griesenbeck J, Kornberg R, Cleary M . A trithorax-group complex purified from Saccharomyces cerevisiae is required for methylation of histone H3. Proc Natl Acad Sci U S A. 2001; 99(1):90-4. PMC: 117519. DOI: 10.1073/pnas.221596698. View

Gavin A, Bosche M, Krause R, Grandi P, Marzioch M, Bauer A . Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature. 2002; 415(6868):141-7. DOI: 10.1038/415141a. View

Mueller C, Jaehning J . Ctr9, Rtf1, and Leo1 are components of the Paf1/RNA polymerase II complex. Mol Cell Biol. 2002; 22(7):1971-80. PMC: 133696. DOI: 10.1128/MCB.22.7.1971-1980.2002. View

Corda Y, Schramke V, Longhese M, Smokvina T, Paciotti V, Brevet V . Interaction between Set1p and checkpoint protein Mec3p in DNA repair and telomere functions. Nat Genet. 1999; 21(2):204-8. DOI: 10.1038/5991. View

10.

Logie C, Peterson C . Purification and biochemical properties of yeast SWI/SNF complex. Methods Enzymol. 1999; 304:726-41. DOI: 10.1016/s0076-6879(99)04044-6. View

11.

Bai Y, SALVADORE C, Chiang Y, Collart M, Liu H, Denis C . The CCR4 and CAF1 proteins of the CCR4-NOT complex are physically and functionally separated from NOT2, NOT4, and NOT5. Mol Cell Biol. 1999; 19(10):6642-51. PMC: 84645. DOI: 10.1128/MCB.19.10.6642. View

12.

Schlichter A, Cairns B . Histone trimethylation by Set1 is coordinated by the RRM, autoinhibitory, and catalytic domains. EMBO J. 2005; 24(6):1222-31. PMC: 556409. DOI: 10.1038/sj.emboj.7600607. View

13.

Morillon A, Karabetsou N, Nair A, Mellor J . Dynamic lysine methylation on histone H3 defines the regulatory phase of gene transcription. Mol Cell. 2005; 18(6):723-34. DOI: 10.1016/j.molcel.2005.05.009. View

14.

Gardner R, Nelson Z, Gottschling D . Ubp10/Dot4p regulates the persistence of ubiquitinated histone H2B: distinct roles in telomeric silencing and general chromatin. Mol Cell Biol. 2005; 25(14):6123-39. PMC: 1168808. DOI: 10.1128/MCB.25.14.6123-6139.2005. View

15.

Laribee R, Krogan N, Xiao T, Shibata Y, Hughes T, Greenblatt J . BUR kinase selectively regulates H3 K4 trimethylation and H2B ubiquitylation through recruitment of the PAF elongation complex. Curr Biol. 2005; 15(16):1487-93. DOI: 10.1016/j.cub.2005.07.028. View

16.

Schneider J, Wood A, Lee J, Schuster R, Dueker J, Maguire C . Molecular regulation of histone H3 trimethylation by COMPASS and the regulation of gene expression. Mol Cell. 2005; 19(6):849-56. DOI: 10.1016/j.molcel.2005.07.024. View

17.

Zhao J, Herrera-Diaz J, Gross D . Domain-wide displacement of histones by activated heat shock factor occurs independently of Swi/Snf and is not correlated with RNA polymerase II density. Mol Cell Biol. 2005; 25(20):8985-99. PMC: 1265789. DOI: 10.1128/MCB.25.20.8985-8999.2005. View

18.

Mulder K, Winkler G, Timmers H . DNA damage and replication stress induced transcription of RNR genes is dependent on the Ccr4-Not complex. Nucleic Acids Res. 2005; 33(19):6384-92. PMC: 1278945. DOI: 10.1093/nar/gki938. View

19.

Wood A, Schneider J, Dover J, Johnston M, Shilatifard A . The Bur1/Bur2 complex is required for histone H2B monoubiquitination by Rad6/Bre1 and histone methylation by COMPASS. Mol Cell. 2005; 20(4):589-99. DOI: 10.1016/j.molcel.2005.09.010. View

20.

van Werven F, Timmers H . The use of biotin tagging in Saccharomyces cerevisiae improves the sensitivity of chromatin immunoprecipitation. Nucleic Acids Res. 2006; 34(4):e33. PMC: 1383622. DOI: 10.1093/nar/gkl003. View