Histone H3K27 trimethylation inhibits H3 binding and function of SET1-Like H3K4 methyltransferase complexes

Dae Hwan Kim, Zhanyun Tang, Miho Shimada, Beat Fierz, Brian Houck-Loomis, Maya Bar-Dagen, Seunghee Lee, Soo-Kyung Lee, Tom W. Muir, Robert G. Roeder, Jae Lee

Research output: Contribution to journalArticle

27 Citations (Scopus)

Abstract

Trimethylated histone H3 lysine 4 (H3K4) and H3K27 generally mark transcriptionally active and repressive chromatins, respectively. In most cell types, these two modifications are mutually exclusive, and this segregation is crucial for the regulation of gene expression. However, how this anticorrelation is achieved has not been fully understood. Here, we show that removal of the H3K27 trimethyl mark facilitates recruitment of SET1-like H3K4 methyltransferase complexes to their target genes by eliciting a novel interaction between histone H3 and two common subunits, WDR5 and RBBP5, of SET1-like complexes. Consistent with this result, H3K27 trimethylation destabilizes interactions of H3 with SET1-like complexes and antagonizes their ability to carry out H3K4 trimethylation of peptide (H3 residues 1 to 36), histone octamer, and mononucleosome substrates. Altogether, our studies reveal that H3K27 trimethylation of histone H3 represses a previously unrecognized interaction between H3 and SET1-like complexes. This provides an important mechanism that directs the anticorrelation between H3K4 and H3K27 trimethylation.

Original languageEnglish (US)
Pages (from-to)4936-4946
Number of pages11
JournalMolecular and Cellular Biology
Volume33
Issue number24
DOIs
StatePublished - 2013

Fingerprint

Methyltransferases
Histones
Gene Expression Regulation
Lysine
Chromatin
Peptides
Genes

ASJC Scopus subject areas

  • Molecular Biology
  • Cell Biology
  • Medicine(all)

Cite this

Histone H3K27 trimethylation inhibits H3 binding and function of SET1-Like H3K4 methyltransferase complexes. / Kim, Dae Hwan; Tang, Zhanyun; Shimada, Miho; Fierz, Beat; Houck-Loomis, Brian; Bar-Dagen, Maya; Lee, Seunghee; Lee, Soo-Kyung; Muir, Tom W.; Roeder, Robert G.; Lee, Jae.

In: Molecular and Cellular Biology, Vol. 33, No. 24, 2013, p. 4936-4946.

Research output: Contribution to journalArticle

Kim, DH, Tang, Z, Shimada, M, Fierz, B, Houck-Loomis, B, Bar-Dagen, M, Lee, S, Lee, S-K, Muir, TW, Roeder, RG & Lee, J 2013, 'Histone H3K27 trimethylation inhibits H3 binding and function of SET1-Like H3K4 methyltransferase complexes', Molecular and Cellular Biology, vol. 33, no. 24, pp. 4936-4946. https://doi.org/10.1128/MCB.00601-13
Kim, Dae Hwan ; Tang, Zhanyun ; Shimada, Miho ; Fierz, Beat ; Houck-Loomis, Brian ; Bar-Dagen, Maya ; Lee, Seunghee ; Lee, Soo-Kyung ; Muir, Tom W. ; Roeder, Robert G. ; Lee, Jae. / Histone H3K27 trimethylation inhibits H3 binding and function of SET1-Like H3K4 methyltransferase complexes. In: Molecular and Cellular Biology. 2013 ; Vol. 33, No. 24. pp. 4936-4946.
@article{850159ed037e4eda8ef5eafd5321aee1,
title = "Histone H3K27 trimethylation inhibits H3 binding and function of SET1-Like H3K4 methyltransferase complexes",
abstract = "Trimethylated histone H3 lysine 4 (H3K4) and H3K27 generally mark transcriptionally active and repressive chromatins, respectively. In most cell types, these two modifications are mutually exclusive, and this segregation is crucial for the regulation of gene expression. However, how this anticorrelation is achieved has not been fully understood. Here, we show that removal of the H3K27 trimethyl mark facilitates recruitment of SET1-like H3K4 methyltransferase complexes to their target genes by eliciting a novel interaction between histone H3 and two common subunits, WDR5 and RBBP5, of SET1-like complexes. Consistent with this result, H3K27 trimethylation destabilizes interactions of H3 with SET1-like complexes and antagonizes their ability to carry out H3K4 trimethylation of peptide (H3 residues 1 to 36), histone octamer, and mononucleosome substrates. Altogether, our studies reveal that H3K27 trimethylation of histone H3 represses a previously unrecognized interaction between H3 and SET1-like complexes. This provides an important mechanism that directs the anticorrelation between H3K4 and H3K27 trimethylation.",
author = "Kim, {Dae Hwan} and Zhanyun Tang and Miho Shimada and Beat Fierz and Brian Houck-Loomis and Maya Bar-Dagen and Seunghee Lee and Soo-Kyung Lee and Muir, {Tom W.} and Roeder, {Robert G.} and Jae Lee",
year = "2013",
doi = "10.1128/MCB.00601-13",
language = "English (US)",
volume = "33",
pages = "4936--4946",
journal = "Molecular and Cellular Biology",
issn = "0270-7306",
publisher = "American Society for Microbiology",
number = "24",

}

TY - JOUR

T1 - Histone H3K27 trimethylation inhibits H3 binding and function of SET1-Like H3K4 methyltransferase complexes

AU - Kim, Dae Hwan

AU - Tang, Zhanyun

AU - Shimada, Miho

AU - Fierz, Beat

AU - Houck-Loomis, Brian

AU - Bar-Dagen, Maya

AU - Lee, Seunghee

AU - Lee, Soo-Kyung

AU - Muir, Tom W.

AU - Roeder, Robert G.

AU - Lee, Jae

PY - 2013

Y1 - 2013

N2 - Trimethylated histone H3 lysine 4 (H3K4) and H3K27 generally mark transcriptionally active and repressive chromatins, respectively. In most cell types, these two modifications are mutually exclusive, and this segregation is crucial for the regulation of gene expression. However, how this anticorrelation is achieved has not been fully understood. Here, we show that removal of the H3K27 trimethyl mark facilitates recruitment of SET1-like H3K4 methyltransferase complexes to their target genes by eliciting a novel interaction between histone H3 and two common subunits, WDR5 and RBBP5, of SET1-like complexes. Consistent with this result, H3K27 trimethylation destabilizes interactions of H3 with SET1-like complexes and antagonizes their ability to carry out H3K4 trimethylation of peptide (H3 residues 1 to 36), histone octamer, and mononucleosome substrates. Altogether, our studies reveal that H3K27 trimethylation of histone H3 represses a previously unrecognized interaction between H3 and SET1-like complexes. This provides an important mechanism that directs the anticorrelation between H3K4 and H3K27 trimethylation.

AB - Trimethylated histone H3 lysine 4 (H3K4) and H3K27 generally mark transcriptionally active and repressive chromatins, respectively. In most cell types, these two modifications are mutually exclusive, and this segregation is crucial for the regulation of gene expression. However, how this anticorrelation is achieved has not been fully understood. Here, we show that removal of the H3K27 trimethyl mark facilitates recruitment of SET1-like H3K4 methyltransferase complexes to their target genes by eliciting a novel interaction between histone H3 and two common subunits, WDR5 and RBBP5, of SET1-like complexes. Consistent with this result, H3K27 trimethylation destabilizes interactions of H3 with SET1-like complexes and antagonizes their ability to carry out H3K4 trimethylation of peptide (H3 residues 1 to 36), histone octamer, and mononucleosome substrates. Altogether, our studies reveal that H3K27 trimethylation of histone H3 represses a previously unrecognized interaction between H3 and SET1-like complexes. This provides an important mechanism that directs the anticorrelation between H3K4 and H3K27 trimethylation.

UR - http://www.scopus.com/inward/record.url?scp=84893139184&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84893139184&partnerID=8YFLogxK

U2 - 10.1128/MCB.00601-13

DO - 10.1128/MCB.00601-13

M3 - Article

C2 - 24126056

AN - SCOPUS:84893139184

VL - 33

SP - 4936

EP - 4946

JO - Molecular and Cellular Biology

JF - Molecular and Cellular Biology

SN - 0270-7306

IS - 24

ER -