Systematic identification of proteins binding to chromatin-embedded ubiquitylated H2B reveals recruitment of SWI/SNF to regulate transcription

Efrat Shema-Yaacoby; Miroslav Nikolov; Mahmood Haj-Yahya; Peter Siman; Eric Allemand; Yuki Yamaguchi; Christian Muchardt; Henning Urlaub; Ashraf Brik; Moshe Oren; Wolfgang Fischle

doi:10.1016/j.celrep.2013.07.014

Systematic identification of proteins binding to chromatin-embedded ubiquitylated H2B reveals recruitment of SWI/SNF to regulate transcription

Efrat Shema-Yaacoby, Miroslav Nikolov, Mahmood Haj-Yahya, Peter Siman, Eric Allemand, Yuki Yamaguchi, Christian Muchardt, Henning Urlaub, Ashraf Brik, Moshe Oren^*, Wolfgang Fischle

^*Corresponding author for this work

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

71 Scopus citations

Abstract

Chromatin posttranslational modifications (PTMs), including monoubiquitylation of histone H2B on lysine 120 (H2Bub1), play a major role in regulating genome functions. To elucidate the molecular mechanisms of H2Bub1 activity, a chromatin template uniformly containing H2Bub1 was used as an affinity matrix to identify preferentially interacting human proteins. Over 90 such factors were found, including proteins and protein complexes associated with transcription, RNA posttranscriptional modifications, and DNA replication and repair. Notably, we found that the SWI/SNF chromatin remodeling complex associates preferentially with H2Bub1-rich chromatin. Moreover,SWI/SNF is required for optimal transcription of a subset of genes that are selectively dependent on H2Bub1. Our findings substantially expand the known H2Bub1 interactome and provide insights into the functions of this PTM in mammalian gene regulation

Original language	English (US)
Pages (from-to)	601-608
Number of pages	8
Journal	Cell reports
Volume	4
Issue number	3
DOIs	https://doi.org/10.1016/j.celrep.2013.07.014
State	Published - 2013
Externally published	Yes

Bibliographical note

Funding Information:
We are grateful to Moshe Yaniv, Frauke Melchior, Steven Bergink, Gilad Fuchs, Eran Kotler, and Lior Golomb for helpful discussions. We thank Tamar Unger and Shira Albeck for preparing H2B and ubiquitin and Uwe Plessmann and Monika Raabe for expert technical assistance. This work was supported in part by grant 293438 (RUBICAN) from the European Research Council (to M.O.), grant R37 CA40099 from the National Cancer Institute (to M.O.), the Dr. Miriam and Sheldon G. Adelson Medical Research Foundation (to M.O.), the Edmond J. Safra Foundation (A.B.), the Lower Saxony-Israeli Association (to M.O. and W.F.), the Max Planck Society (to H.U. and W.F.), and the Mina and James Heinemann Foundation (to W.F.). M.O. is the incumbent of the Andre Lwoff chair in molecular biology. E.S. is supported by the Adams Fellowship Program of the Israel Academy of Sciences and Humanities. M.N. is supported by a fellowship from the MSc/PhD program “Molecular Biology” International Max Planck Research School at the Georg August University, Göttingen.

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.celrep.2013.07.014

Cite this

Shema-Yaacoby, E., Nikolov, M., Haj-Yahya, M., Siman, P., Allemand, E., Yamaguchi, Y., Muchardt, C., Urlaub, H., Brik, A., Oren, M., & Fischle, W. (2013). Systematic identification of proteins binding to chromatin-embedded ubiquitylated H2B reveals recruitment of SWI/SNF to regulate transcription. Cell reports, 4(3), 601-608. https://doi.org/10.1016/j.celrep.2013.07.014

@article{aaf03ad71ba64cfc84a7f952a34e1d8e,

title = "Systematic identification of proteins binding to chromatin-embedded ubiquitylated H2B reveals recruitment of SWI/SNF to regulate transcription",

abstract = "Chromatin posttranslational modifications (PTMs), including monoubiquitylation of histone H2B on lysine 120 (H2Bub1), play a major role in regulating genome functions. To elucidate the molecular mechanisms of H2Bub1 activity, a chromatin template uniformly containing H2Bub1 was used as an affinity matrix to identify preferentially interacting human proteins. Over 90 such factors were found, including proteins and protein complexes associated with transcription, RNA posttranscriptional modifications, and DNA replication and repair. Notably, we found that the SWI/SNF chromatin remodeling complex associates preferentially with H2Bub1-rich chromatin. Moreover,SWI/SNF is required for optimal transcription of a subset of genes that are selectively dependent on H2Bub1. Our findings substantially expand the known H2Bub1 interactome and provide insights into the functions of this PTM in mammalian gene regulation",

author = "Efrat Shema-Yaacoby and Miroslav Nikolov and Mahmood Haj-Yahya and Peter Siman and Eric Allemand and Yuki Yamaguchi and Christian Muchardt and Henning Urlaub and Ashraf Brik and Moshe Oren and Wolfgang Fischle",

note = "Funding Information: We are grateful to Moshe Yaniv, Frauke Melchior, Steven Bergink, Gilad Fuchs, Eran Kotler, and Lior Golomb for helpful discussions. We thank Tamar Unger and Shira Albeck for preparing H2B and ubiquitin and Uwe Plessmann and Monika Raabe for expert technical assistance. This work was supported in part by grant 293438 (RUBICAN) from the European Research Council (to M.O.), grant R37 CA40099 from the National Cancer Institute (to M.O.), the Dr. Miriam and Sheldon G. Adelson Medical Research Foundation (to M.O.), the Edmond J. Safra Foundation (A.B.), the Lower Saxony-Israeli Association (to M.O. and W.F.), the Max Planck Society (to H.U. and W.F.), and the Mina and James Heinemann Foundation (to W.F.). M.O. is the incumbent of the Andre Lwoff chair in molecular biology. E.S. is supported by the Adams Fellowship Program of the Israel Academy of Sciences and Humanities. M.N. is supported by a fellowship from the MSc/PhD program “Molecular Biology” International Max Planck Research School at the Georg August University, G{\"o}ttingen. ",

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Shema-Yaacoby, E, Nikolov, M, Haj-Yahya, M, Siman, P, Allemand, E, Yamaguchi, Y, Muchardt, C, Urlaub, H, Brik, A, Oren, M & Fischle, W 2013, 'Systematic identification of proteins binding to chromatin-embedded ubiquitylated H2B reveals recruitment of SWI/SNF to regulate transcription', Cell reports, vol. 4, no. 3, pp. 601-608. https://doi.org/10.1016/j.celrep.2013.07.014

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T1 - Systematic identification of proteins binding to chromatin-embedded ubiquitylated H2B reveals recruitment of SWI/SNF to regulate transcription

AU - Shema-Yaacoby, Efrat

AU - Nikolov, Miroslav

AU - Haj-Yahya, Mahmood

AU - Siman, Peter

AU - Allemand, Eric

AU - Yamaguchi, Yuki

AU - Muchardt, Christian

AU - Urlaub, Henning

AU - Brik, Ashraf

AU - Oren, Moshe

AU - Fischle, Wolfgang

N1 - Funding Information: We are grateful to Moshe Yaniv, Frauke Melchior, Steven Bergink, Gilad Fuchs, Eran Kotler, and Lior Golomb for helpful discussions. We thank Tamar Unger and Shira Albeck for preparing H2B and ubiquitin and Uwe Plessmann and Monika Raabe for expert technical assistance. This work was supported in part by grant 293438 (RUBICAN) from the European Research Council (to M.O.), grant R37 CA40099 from the National Cancer Institute (to M.O.), the Dr. Miriam and Sheldon G. Adelson Medical Research Foundation (to M.O.), the Edmond J. Safra Foundation (A.B.), the Lower Saxony-Israeli Association (to M.O. and W.F.), the Max Planck Society (to H.U. and W.F.), and the Mina and James Heinemann Foundation (to W.F.). M.O. is the incumbent of the Andre Lwoff chair in molecular biology. E.S. is supported by the Adams Fellowship Program of the Israel Academy of Sciences and Humanities. M.N. is supported by a fellowship from the MSc/PhD program “Molecular Biology” International Max Planck Research School at the Georg August University, Göttingen.

PY - 2013

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N2 - Chromatin posttranslational modifications (PTMs), including monoubiquitylation of histone H2B on lysine 120 (H2Bub1), play a major role in regulating genome functions. To elucidate the molecular mechanisms of H2Bub1 activity, a chromatin template uniformly containing H2Bub1 was used as an affinity matrix to identify preferentially interacting human proteins. Over 90 such factors were found, including proteins and protein complexes associated with transcription, RNA posttranscriptional modifications, and DNA replication and repair. Notably, we found that the SWI/SNF chromatin remodeling complex associates preferentially with H2Bub1-rich chromatin. Moreover,SWI/SNF is required for optimal transcription of a subset of genes that are selectively dependent on H2Bub1. Our findings substantially expand the known H2Bub1 interactome and provide insights into the functions of this PTM in mammalian gene regulation

AB - Chromatin posttranslational modifications (PTMs), including monoubiquitylation of histone H2B on lysine 120 (H2Bub1), play a major role in regulating genome functions. To elucidate the molecular mechanisms of H2Bub1 activity, a chromatin template uniformly containing H2Bub1 was used as an affinity matrix to identify preferentially interacting human proteins. Over 90 such factors were found, including proteins and protein complexes associated with transcription, RNA posttranscriptional modifications, and DNA replication and repair. Notably, we found that the SWI/SNF chromatin remodeling complex associates preferentially with H2Bub1-rich chromatin. Moreover,SWI/SNF is required for optimal transcription of a subset of genes that are selectively dependent on H2Bub1. Our findings substantially expand the known H2Bub1 interactome and provide insights into the functions of this PTM in mammalian gene regulation

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DO - 10.1016/j.celrep.2013.07.014

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JF - Cell reports

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ER -

Systematic identification of proteins binding to chromatin-embedded ubiquitylated H2B reveals recruitment of SWI/SNF to regulate transcription

Abstract

Bibliographical note

ASJC Scopus subject areas

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