Enhancer decommissioning by LSD1 during embryonic stem cell differentiation
In embryonic stem cells, the histone demethylase LSD1 occupies the enhancers of active genes and, together with the NuRD complex, decommissions the enhancers during differentiation. A turn-off for genes Gene activation in the developing embryo occurs when transcription factors bind to enhancer eleme...
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| Published in | Nature (London) Vol. 482; no. 7384; pp. 221 - 225 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
09.02.2012
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | In embryonic stem cells, the histone demethylase LSD1 occupies the enhancers of active genes and, together with the NuRD complex, decommissions the enhancers during differentiation.
A turn-off for genes
Gene activation in the developing embryo occurs when transcription factors bind to enhancer elements and recruit coactivators and chromatin regulators to facilitate transcription initiation. However, relatively little is known about how enhancers are deactivated when a gene needs to be silenced. Here, Whyte
et al
. show that in embryonic stem cells, the histone demethylase LSD1 is essential for enhancer deactivation, acting with other components of the NuRD (nucleosome remodelling and histone deacetylase) complex.
Transcription factors and chromatin modifiers are important in the programming and reprogramming of cellular states during development
1
,
2
. Transcription factors bind to enhancer elements and recruit coactivators and chromatin-modifying enzymes to facilitate transcription initiation
3
,
4
. During differentiation a subset of these enhancers must be silenced, but the mechanisms underlying enhancer silencing are poorly understood. Here we show that the histone demethylase lysine-specific demethylase 1 (LSD1; ref.
5
), which demethylates histone H3 on Lys 4 or Lys 9 (H3K4/K9), is essential in decommissioning enhancers during the differentiation of mouse embryonic stem cells (ESCs). LSD1 occupies enhancers of active genes that are critical for control of the state of ESCs. However, LSD1 is not essential for the maintenance of ESC identity. Instead, ESCs lacking LSD1 activity fail to differentiate fully, and ESC-specific enhancers fail to undergo the histone demethylation events associated with differentiation. At active enhancers, LSD1 is a component of the NuRD (nucleosome remodelling and histone deacetylase) complex, which contains additional subunits that are necessary for ESC differentiation. We propose that the LSD1–NuRD complex decommissions enhancers of the pluripotency program during differentiation, which is essential for the complete shutdown of the ESC gene expression program and the transition to new cell states. |
|---|---|
| AbstractList | Transcription factors and chromatin modifiers are important in the programming and reprogramming of cellular states during development
1
,
2
. Transcription factors bind to enhancer elements and recruit coactivators and chromatin-modifying enzymes to facilitate transcription initiation
3
,
4
. During differentiation a subset of these enhancers must be silenced, but the mechanisms underlying enhancer silencing are poorly understood. Here we show that the histone demethylase lysine-specific demethylase 1 (LSD1; ref.
5
), which demethylates histone H3 on Lys 4 or Lys 9 (H3K4/K9), is essential in decommissioning enhancers during the differentiation of mouse embryonic stem cells (ESCs). LSD1 occupies enhancers of active genes that are critical for control of the state of ESCs. However, LSD1 is not essential for the maintenance of ESC identity. Instead, ESCs lacking LSD1 activity fail to differentiate fully, and ESC-specific enhancers fail to undergo the histone demethylation events associated with differentiation. At active enhancers, LSD1 is a component of the NuRD (nucleosome remodelling and histone deacetylase) complex, which contains additional subunits that are necessary for ESC differentiation. We propose that the LSD1–NuRD complex decommissions enhancers of the pluripotency program during differentiation, which is essential for the complete shutdown of the ESC gene expression program and the transition to new cell states. Transcription factors and chromatin modifiers are important in the programming and reprogramming of cellular states during development. Transcription factors bind to enhancer elements and recruit coactivators and chromatin-modifying enzymes to facilitate transcription initiation. During differentiation a subset of these enhancers must be silenced, but the mechanisms underlying enhancer silencing are poorly understood. Here we show that the histone demethylase lysine-specific demethylase 1 (LSD1; ref. 5), which demethylates histone H3 on Lys 4 or Lys 9 (H3K4/K9), is essential in decommissioning enhancers during the differentiation of mouse embryonic stem cells (ESCs). LSD1 occupies enhancers of active genes that are critical for control of the state of ESCs. However, LSD1 is not essential for the maintenance of ESC identity. Instead, ESCs lacking LSD1 activity fail to differentiate fully, and ESC-specific enhancers fail to undergo the histone demethylation events associated with differentiation. At active enhancers, LSD1 is a component of the NuRD (nucleosome remodelling and histone deacetylase) complex, which contains additional subunits that are necessary for ESC differentiation. We propose that the LSD1-NuRD complex decommissions enhancers of the pluripotency program during differentiation, which is essential for the complete shutdown of the ESC gene expression program and the transition to new cell states. [PUBLICATION ABSTRACT] Transcription factors and chromatin modifiers are important in the programming and reprogramming of cellular states during development. Transcription factors bind to enhancer elements and recruit coactivators and chromatin-modifying enzymes to facilitate transcription initiation. During differentiation a subset of these enhancers must be silenced, but the mechanisms underlying enhancer silencing are poorly understood. Here we show that the histone demethylase lysine-specific demethylase 1 (LSD1; ref. 5), which demethylates histone H3 on Lys 4 or Lys 9 (H3K4/K9), is essential in decommissioning enhancers during the differentiation of mouse embryonic stem cells (ESCs). LSD1 occupies enhancers of active genes that are critical for control of the state of ESCs. However, LSD1 is not essential for the maintenance of ESC identity. Instead, ESCs lacking LSD1 activity fail to differentiate fully, and ESC-specific enhancers fail to undergo the histone demethylation events associated with differentiation. At active enhancers, LSD1 is a component of the NuRD (nucleosome remodelling and histone deacetylase) complex, which contains additional subunits that are necessary for ESC differentiation. We propose that the LSD1-NuRD complex decommissions enhancers of the pluripotency program during differentiation, which is essential for the complete shutdown of the ESC gene expression program and the transition to new cell states. Transcription factors and chromatin modifiers are important in the programming and reprogramming of cellular states during development. Transcription factors bind to enhancer elements and recruit coactivators and chromatin-modifying enzymes to facilitate transcription initiation. During differentiation a subset of these enhancers must be silenced, but the mechanisms underlying enhancer silencing are poorly understood. Here we show that the histone demethylase lysine-specific demethylase 1 (LSD1; ref. 5), which demethylates histone H3 on Lys4 or Lys9 (H3K4/K9), is essential in decommissioning enhancers during the differentiation of mouse embryonic stem cells (ESCs). LSD1 occupies enhancers of active genes that are critical for control of the state of ESCs. However, LSD1 is not essential for the maintenance of ESC identity. Instead, ESCs lacking LSD1 activity fail to differentiate fully, and ESC-specific enhancers fail to undergo the histone demethylation events associated with differentiation. At active enhancers, LSD1 is a component of the NuRD (nucleosome remodelling and histone deacetylase) complex, which contains additional subunits that are necessary for ESC differentiation. We propose that the LSD1-NuRD complex decommissions enhancers of the pluripotency program during differentiation, which is essential for the complete shutdown of the ESC gene expression program and the transition to new cell states. In embryonic stem cells, the histone demethylase LSD1 occupies the enhancers of active genes and, together with the NuRD complex, decommissions the enhancers during differentiation. A turn-off for genes Gene activation in the developing embryo occurs when transcription factors bind to enhancer elements and recruit coactivators and chromatin regulators to facilitate transcription initiation. However, relatively little is known about how enhancers are deactivated when a gene needs to be silenced. Here, Whyte et al . show that in embryonic stem cells, the histone demethylase LSD1 is essential for enhancer deactivation, acting with other components of the NuRD (nucleosome remodelling and histone deacetylase) complex. Transcription factors and chromatin modifiers are important in the programming and reprogramming of cellular states during development 1 , 2 . Transcription factors bind to enhancer elements and recruit coactivators and chromatin-modifying enzymes to facilitate transcription initiation 3 , 4 . During differentiation a subset of these enhancers must be silenced, but the mechanisms underlying enhancer silencing are poorly understood. Here we show that the histone demethylase lysine-specific demethylase 1 (LSD1; ref. 5 ), which demethylates histone H3 on Lys 4 or Lys 9 (H3K4/K9), is essential in decommissioning enhancers during the differentiation of mouse embryonic stem cells (ESCs). LSD1 occupies enhancers of active genes that are critical for control of the state of ESCs. However, LSD1 is not essential for the maintenance of ESC identity. Instead, ESCs lacking LSD1 activity fail to differentiate fully, and ESC-specific enhancers fail to undergo the histone demethylation events associated with differentiation. At active enhancers, LSD1 is a component of the NuRD (nucleosome remodelling and histone deacetylase) complex, which contains additional subunits that are necessary for ESC differentiation. We propose that the LSD1–NuRD complex decommissions enhancers of the pluripotency program during differentiation, which is essential for the complete shutdown of the ESC gene expression program and the transition to new cell states. |
| Author | Bilodeau, Steve Frampton, Garrett M. Foster, Charles T. Young, Richard A. Hoke, Heather A. Cowley, Shaun M. Whyte, Warren A. Orlando, David A. |
| AuthorAffiliation | 3 Department of Molecular Biology, Adolf-Butenandt Institut, Ludwig-Maximilians-Universität München, 80336 Munich, Germany 2 Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA 1 Whitehead Institute for Biomedical Research, 9 Cambridge Center, Cambridge, Massachusetts 02142, USA 4 Department of Biochemistry, University of Leicester, Leicester LE1 9HN, UK |
| AuthorAffiliation_xml | – name: 4 Department of Biochemistry, University of Leicester, Leicester LE1 9HN, UK – name: 1 Whitehead Institute for Biomedical Research, 9 Cambridge Center, Cambridge, Massachusetts 02142, USA – name: 2 Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA – name: 3 Department of Molecular Biology, Adolf-Butenandt Institut, Ludwig-Maximilians-Universität München, 80336 Munich, Germany |
| Author_xml | – sequence: 1 givenname: Warren A. surname: Whyte fullname: Whyte, Warren A. organization: Whitehead Institute for Biomedical Research, 9 Cambridge Center, Department of Biology, Massachusetts Institute of Technology – sequence: 2 givenname: Steve surname: Bilodeau fullname: Bilodeau, Steve organization: Whitehead Institute for Biomedical Research, 9 Cambridge Center – sequence: 3 givenname: David A. surname: Orlando fullname: Orlando, David A. organization: Whitehead Institute for Biomedical Research, 9 Cambridge Center – sequence: 4 givenname: Heather A. surname: Hoke fullname: Hoke, Heather A. organization: Whitehead Institute for Biomedical Research, 9 Cambridge Center, Department of Biology, Massachusetts Institute of Technology – sequence: 5 givenname: Garrett M. surname: Frampton fullname: Frampton, Garrett M. organization: Whitehead Institute for Biomedical Research, 9 Cambridge Center, Department of Biology, Massachusetts Institute of Technology – sequence: 6 givenname: Charles T. surname: Foster fullname: Foster, Charles T. organization: Department of Molecular Biology, Adolf-Butenandt Institut, Ludwig-Maximilians-Universität München, 80336 Munich, Germany, Department of Biochemistry, University of Leicester, Leicester LE1 9HN, UK – sequence: 7 givenname: Shaun M. surname: Cowley fullname: Cowley, Shaun M. organization: Department of Biochemistry, University of Leicester, Leicester LE1 9HN, UK – sequence: 8 givenname: Richard A. surname: Young fullname: Young, Richard A. email: young@wi.mit.edu organization: Whitehead Institute for Biomedical Research, 9 Cambridge Center, Department of Biology, Massachusetts Institute of Technology |
| BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=25455381$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/22297846$$D View this record in MEDLINE/PubMed |
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| Snippet | In embryonic stem cells, the histone demethylase LSD1 occupies the enhancers of active genes and, together with the NuRD complex, decommissions the enhancers... Transcription factors and chromatin modifiers are important in the programming and reprogramming of cellular states during development. Transcription factors... Transcription factors and chromatin modifiers are important in the programming and reprogramming of cellular states during development 1 , 2 . Transcription... |
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| SubjectTerms | 631/136/532/1360 631/208/176/2016 631/208/199 Animals Biological and medical sciences Cell differentiation Cell Differentiation - genetics Cell differentiation, maturation, development, hematopoiesis Cell physiology Decommissioning Embryonic Stem Cells - cytology Embryonic Stem Cells - metabolism Enhancer Elements, Genetic - genetics Experiments Fibroblasts Fundamental and applied biological sciences. Psychology Gene expression Gene Silencing Histone Demethylases Humanities and Social Sciences letter Mi-2 Nucleosome Remodeling and Deacetylase Complex - metabolism Mice Molecular and cellular biology multidisciplinary Oxidoreductases, N-Demethylating - antagonists & inhibitors Oxidoreductases, N-Demethylating - metabolism Promoter Regions, Genetic - genetics RNA polymerase Science Stem cells Studies |
| Title | Enhancer decommissioning by LSD1 during embryonic stem cell differentiation |
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