Quantitative Interaction Proteomics and Genome-wide Profiling of Epigenetic Histone Marks and Their Readers

Michiel Vermeulen; H. Christian Eberl; Filomena Matarese; Hendrik Marks; Sergei Denissov; Falk Butter; Kenneth K. Lee; Jesper V. Olsen; Anthony A. Hyman; Henk G. Stunnenberg; Matthias Mann

doi:10.1016/j.cell.2010.08.020

Quantitative Interaction Proteomics and Genome-wide Profiling of Epigenetic Histone Marks and Their Readers

Michiel Vermeulen
, H. Christian Eberl
, Filomena Matarese
, Hendrik Marks
, Sergei Denissov
, Falk Butter
, Kenneth K. Lee
, Jesper V. Olsen
, Anthony A. Hyman
, Henk G. Stunnenberg
, Matthias Mann

Research output: Contribution to journal › Article › peer-review

672 Citations (Scopus)

Abstract

Trimethyl-lysine (me3) modifications on histones are the most stable epigenetic marks and they control chromatin-mediated regulation of gene expression. Here, we determine proteins that bind these marks by high-accuracy, quantitative mass spectrometry. These chromatin " readers" are assigned to complexes by interaction proteomics of full-length BAC-GFP-tagged proteins. ChIP-Seq profiling identifies their genomic binding sites, revealing functional properties. Among the main findings, the human SAGA complex binds to H3K4me3 via a double Tudor-domain in the C terminus of Sgf29, and the PWWP domain is identified as a putative H3K36me3 binding motif. The ORC complex, including LRWD1, binds to the three most prominent transcriptional repressive lysine methylation sites. Our data reveal a highly adapted interplay between chromatin marks and their associated protein complexes. Reading specific trimethyl-lysine sites by specialized complexes appears to be a widespread mechanism to mediate gene expression.

Original language	English
Pages (from-to)	967-980
Number of pages	14
Journal	Cell
Volume	142
Issue number	6
DOIs	https://doi.org/10.1016/j.cell.2010.08.020
Publication status	Published - Sept 2010
Externally published	Yes

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10.1016/j.cell.2010.08.020

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@article{bc6efb13427b4365b0f7dafc914c73c4,

title = "Quantitative Interaction Proteomics and Genome-wide Profiling of Epigenetic Histone Marks and Their Readers",

abstract = "Trimethyl-lysine (me3) modifications on histones are the most stable epigenetic marks and they control chromatin-mediated regulation of gene expression. Here, we determine proteins that bind these marks by high-accuracy, quantitative mass spectrometry. These chromatin {"} readers{"} are assigned to complexes by interaction proteomics of full-length BAC-GFP-tagged proteins. ChIP-Seq profiling identifies their genomic binding sites, revealing functional properties. Among the main findings, the human SAGA complex binds to H3K4me3 via a double Tudor-domain in the C terminus of Sgf29, and the PWWP domain is identified as a putative H3K36me3 binding motif. The ORC complex, including LRWD1, binds to the three most prominent transcriptional repressive lysine methylation sites. Our data reveal a highly adapted interplay between chromatin marks and their associated protein complexes. Reading specific trimethyl-lysine sites by specialized complexes appears to be a widespread mechanism to mediate gene expression.",

author = "Michiel Vermeulen and Eberl, \{H. Christian\} and Filomena Matarese and Hendrik Marks and Sergei Denissov and Falk Butter and Lee, \{Kenneth K.\} and Olsen, \{Jesper V.\} and Hyman, \{Anthony A.\} and Stunnenberg, \{Henk G.\} and Matthias Mann",

note = "Funding Information: Eva Janssen-Megens, Kees-Jan Fran{\c c}ois, and Yan Tan helped with the sequencing, the MPI core facility expressed and purified recombinant proteins, and Dr. F. Tashiro kindly provided Sgf29 antibody. This work was supported by the Max-Planck Society for the Advancement of Science, HEROIC, an Integrated Project funded by the European Union under the 6th Framework Program (LSHG-CT-2005-018883) and by Interaction Proteome (LSHG-CT-2003-505520). M.V. received a fellowship of the Dutch Cancer Society (KWF/NKB) and a grant from the Netherlands Genomics Initiative/Netherlands Organization for Scientific Research. ",

year = "2010",

month = sep,

doi = "10.1016/j.cell.2010.08.020",

language = "English",

volume = "142",

pages = "967--980",

journal = "Cell",

issn = "0092-8674",

publisher = "Elsevier B.V.",

number = "6",

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TY - JOUR

T1 - Quantitative Interaction Proteomics and Genome-wide Profiling of Epigenetic Histone Marks and Their Readers

AU - Vermeulen, Michiel

AU - Eberl, H. Christian

AU - Matarese, Filomena

AU - Marks, Hendrik

AU - Denissov, Sergei

AU - Butter, Falk

AU - Lee, Kenneth K.

AU - Olsen, Jesper V.

AU - Hyman, Anthony A.

AU - Stunnenberg, Henk G.

AU - Mann, Matthias

N1 - Funding Information: Eva Janssen-Megens, Kees-Jan François, and Yan Tan helped with the sequencing, the MPI core facility expressed and purified recombinant proteins, and Dr. F. Tashiro kindly provided Sgf29 antibody. This work was supported by the Max-Planck Society for the Advancement of Science, HEROIC, an Integrated Project funded by the European Union under the 6th Framework Program (LSHG-CT-2005-018883) and by Interaction Proteome (LSHG-CT-2003-505520). M.V. received a fellowship of the Dutch Cancer Society (KWF/NKB) and a grant from the Netherlands Genomics Initiative/Netherlands Organization for Scientific Research.

PY - 2010/9

Y1 - 2010/9

N2 - Trimethyl-lysine (me3) modifications on histones are the most stable epigenetic marks and they control chromatin-mediated regulation of gene expression. Here, we determine proteins that bind these marks by high-accuracy, quantitative mass spectrometry. These chromatin " readers" are assigned to complexes by interaction proteomics of full-length BAC-GFP-tagged proteins. ChIP-Seq profiling identifies their genomic binding sites, revealing functional properties. Among the main findings, the human SAGA complex binds to H3K4me3 via a double Tudor-domain in the C terminus of Sgf29, and the PWWP domain is identified as a putative H3K36me3 binding motif. The ORC complex, including LRWD1, binds to the three most prominent transcriptional repressive lysine methylation sites. Our data reveal a highly adapted interplay between chromatin marks and their associated protein complexes. Reading specific trimethyl-lysine sites by specialized complexes appears to be a widespread mechanism to mediate gene expression.

AB - Trimethyl-lysine (me3) modifications on histones are the most stable epigenetic marks and they control chromatin-mediated regulation of gene expression. Here, we determine proteins that bind these marks by high-accuracy, quantitative mass spectrometry. These chromatin " readers" are assigned to complexes by interaction proteomics of full-length BAC-GFP-tagged proteins. ChIP-Seq profiling identifies their genomic binding sites, revealing functional properties. Among the main findings, the human SAGA complex binds to H3K4me3 via a double Tudor-domain in the C terminus of Sgf29, and the PWWP domain is identified as a putative H3K36me3 binding motif. The ORC complex, including LRWD1, binds to the three most prominent transcriptional repressive lysine methylation sites. Our data reveal a highly adapted interplay between chromatin marks and their associated protein complexes. Reading specific trimethyl-lysine sites by specialized complexes appears to be a widespread mechanism to mediate gene expression.

UR - https://www.scopus.com/pages/publications/77956643239

U2 - 10.1016/j.cell.2010.08.020

DO - 10.1016/j.cell.2010.08.020

M3 - Article

C2 - 20850016

AN - SCOPUS:77956643239

SN - 0092-8674

VL - 142

SP - 967

EP - 980

JO - Cell

JF - Cell

IS - 6

ER -

Quantitative Interaction Proteomics and Genome-wide Profiling of Epigenetic Histone Marks and Their Readers

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