Histone Acetyltransferase p300 Induces De Novo Super-Enhancers to Drive Cellular Senescence
Accumulation of senescent cells during aging contributes to chronic inflammation and age-related diseases. While senescence is associated with profound alterations of the epigenome, a systematic view of epigenetic factors in regulating senescence is lacking. Here, we curated a library of short hairp...
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Published in | Molecular cell Vol. 73; no. 4; pp. 684 - 698.e8 |
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Main Authors | , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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Elsevier Inc
21.02.2019
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Abstract | Accumulation of senescent cells during aging contributes to chronic inflammation and age-related diseases. While senescence is associated with profound alterations of the epigenome, a systematic view of epigenetic factors in regulating senescence is lacking. Here, we curated a library of short hairpin RNAs for targeted silencing of all known epigenetic proteins and performed a high-throughput screen to identify key candidates whose downregulation can delay replicative senescence of primary human cells. This screen identified multiple new players including the histone acetyltransferase p300 that was found to be a primary driver of the senescent phenotype. p300, but not the paralogous CBP, induces a dynamic hyper-acetylated chromatin state and promotes the formation of active enhancer elements in the non-coding genome, leading to a senescence-specific gene expression program. Our work illustrates a causal role of histone acetyltransferases and acetylation in senescence and suggests p300 as a potential therapeutic target for senescence and age-related diseases.
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•High-throughput screening identifies key epigenetic proteins driving senescence•Depletion of the histone acetyltransferase p300 delays senescence•p300 induces the formation of de novo super enhancers in senescence•Depletion of p300 suppresses senescence-related gene expression
Epigenetic dysregulation is a hallmark of senescence and aging. In this article, Sen et al. have identified the histone acetyltransferase p300 as a key protein regulating senescence from a high-throughput screen. p300 induces formation of new super enhancers that drive senescence-related gene expression. p300 is an attractive candidate for anti-aging therapy. |
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AbstractList | Accumulation of senescent cells during aging contributes to chronic inflammation and age-related diseases. While senescence is associated with profound alterations of the epigenome, a systematic view of epigenetic factors in regulating senescence is lacking. Here, we curated a library of short hairpin RNAs for targeted silencing of all known epigenetic proteins and performed a high-throughput screen to identify key candidates whose downregulation can delay replicative senescence of primary human cells. This screen identified multiple new players including the histone acetyltransferase p300 that was found to be a primary driver of the senescent phenotype. p300, but not the paralogous CBP, induces a dynamic hyper-acetylated chromatin state and promotes the formation of active enhancer elements in the non-coding genome, leading to a senescence-specific gene expression program. Our work illustrates a causal role of histone acetyltransferases and acetylation in senescence and suggests p300 as a potential therapeutic target for senescence and age-related diseases.
[Display omitted]
•High-throughput screening identifies key epigenetic proteins driving senescence•Depletion of the histone acetyltransferase p300 delays senescence•p300 induces the formation of de novo super enhancers in senescence•Depletion of p300 suppresses senescence-related gene expression
Epigenetic dysregulation is a hallmark of senescence and aging. In this article, Sen et al. have identified the histone acetyltransferase p300 as a key protein regulating senescence from a high-throughput screen. p300 induces formation of new super enhancers that drive senescence-related gene expression. p300 is an attractive candidate for anti-aging therapy. Accumulation of senescent cells during aging contributes to chronic inflammation and age-related diseases. While senescence is associated with profound alterations of the epigenome, a systematic view of epigenetic factors in regulating senescence is lacking. Here, we curated a library of short hairpin RNAs for targeted silencing of all known epigenetic proteins and performed a high-throughput screen to identify key candidates whose downregulation can delay replicative senescence of primary human cells. This screen identified multiple new players including the histone acetyltransferase p300 that was found to be a primary driver of the senescent phenotype. p300, but not the paralogous CBP, induces a dynamic hyper-acetylated chromatin state and promotes the formation of active enhancer elements in the non-coding genome, leading to a senescence-specific gene expression program. Our work illustrates a causal role of histone acetyltransferases and acetylation in senescence and suggests p300 as a potential therapeutic target for senescence and age-related diseases. Accumulation of senescent cells during aging contributes to chronic inflammation and age-related diseases. While senescence is associated with profound alterations of the epigenome, a systematic view of epigenetic factors in regulating senescence is lacking. Here, we curated a library of short hairpin RNAs for targeted silencing of all known epigenetic proteins and performed a high-throughput screen to identify key candidates whose downregulation can delay replicative senescence of primary human cells. This screen identified multiple new players including the histone acetyltransferase p300 that was found to be a primary driver of the senescent phenotype. p300, but not the paralogous CBP, induces a dynamic hyper-acetylated chromatin state and promotes the formation of active enhancer elements in the non-coding genome, leading to a senescence-specific gene expression program. Our work illustrates a causal role of histone acetyltransferases and acetylation in senescence, and suggests p300 as a potential therapeutic target for senescence and age-related diseases. Epigenetic dysregulation is a hallmark of senescence/aging. In this article, Sen et al. have identified the histone acetyltransferase p300 as a key protein regulating senescence from a high-throughput screen. p300 induces formation of new super enhancers that drive senescence-related gene expression. p300 is an attractive candidate for anti-aging therapy. |
Author | Adams, Peter D. Garcia, Benjamin A. Lan, Yemin Donahue, Greg Li, Catherine Y. Dang, Weiwei Schultz, David C. Berger, Shelley L. Sen, Payel Dou, Zhixun Chen, Qijun Frederick, Brian Johnson, F. Bradley Sidoli, Simone Luense, Lacey J. |
AuthorAffiliation | 9 Huffington Center on Aging, Baylor College of Medicine, Houston, TX 77030, USA 2 Department of Genetics, University of Pennsylvania, Philadelphia, PA 19104, USA 8 Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA 5 Sanford Burnham Prebys Medical Discovery Institute, 10901 North Torrey Pines Road La Jolla, CA 92037, USA 1 Epigenetics Institute, Department of Cell and Developmental Biology, University of Pennsylvania, Philadelphia, PA 19104, USA 4 Department of Biochemistry and Biophysics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA 6 Institute of Cancer Sciences, University of Glasgow, Glasgow G61 1BD, UK 3 Department of Biology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA 19104, USA 7 High Throughput Screening Core, Department of Microbiology, University of Pennsylvania, Philadelphia, PA 19104, USA |
AuthorAffiliation_xml | – name: 7 High Throughput Screening Core, Department of Microbiology, University of Pennsylvania, Philadelphia, PA 19104, USA – name: 1 Epigenetics Institute, Department of Cell and Developmental Biology, University of Pennsylvania, Philadelphia, PA 19104, USA – name: 3 Department of Biology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA 19104, USA – name: 4 Department of Biochemistry and Biophysics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA – name: 2 Department of Genetics, University of Pennsylvania, Philadelphia, PA 19104, USA – name: 9 Huffington Center on Aging, Baylor College of Medicine, Houston, TX 77030, USA – name: 8 Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA – name: 5 Sanford Burnham Prebys Medical Discovery Institute, 10901 North Torrey Pines Road La Jolla, CA 92037, USA – name: 6 Institute of Cancer Sciences, University of Glasgow, Glasgow G61 1BD, UK |
Author_xml | – sequence: 1 givenname: Payel surname: Sen fullname: Sen, Payel organization: Epigenetics Institute, Department of Cell and Developmental Biology, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 2 givenname: Yemin surname: Lan fullname: Lan, Yemin organization: Epigenetics Institute, Department of Cell and Developmental Biology, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 3 givenname: Catherine Y. surname: Li fullname: Li, Catherine Y. organization: Epigenetics Institute, Department of Cell and Developmental Biology, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 4 givenname: Simone surname: Sidoli fullname: Sidoli, Simone organization: Epigenetics Institute, Department of Cell and Developmental Biology, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 5 givenname: Greg surname: Donahue fullname: Donahue, Greg organization: Epigenetics Institute, Department of Cell and Developmental Biology, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 6 givenname: Zhixun surname: Dou fullname: Dou, Zhixun organization: Epigenetics Institute, Department of Cell and Developmental Biology, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 7 givenname: Brian surname: Frederick fullname: Frederick, Brian organization: High Throughput Screening Core, Department of Microbiology, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 8 givenname: Qijun surname: Chen fullname: Chen, Qijun organization: Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 9 givenname: Lacey J. surname: Luense fullname: Luense, Lacey J. organization: Epigenetics Institute, Department of Cell and Developmental Biology, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 10 givenname: Benjamin A. surname: Garcia fullname: Garcia, Benjamin A. organization: Epigenetics Institute, Department of Cell and Developmental Biology, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 11 givenname: Weiwei surname: Dang fullname: Dang, Weiwei organization: Huffington Center on Aging, Baylor College of Medicine, Houston, TX 77030, USA – sequence: 12 givenname: F. Bradley surname: Johnson fullname: Johnson, F. Bradley organization: Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 13 givenname: Peter D. surname: Adams fullname: Adams, Peter D. organization: Sanford Burnham Prebys Medical Discovery Institute, 10901 North Torrey Pines Road, La Jolla, CA 92037, USA – sequence: 14 givenname: David C. surname: Schultz fullname: Schultz, David C. organization: High Throughput Screening Core, Department of Microbiology, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 15 givenname: Shelley L. surname: Berger fullname: Berger, Shelley L. email: bergers@pennmedicine.upenn.edu organization: Epigenetics Institute, Department of Cell and Developmental Biology, University of Pennsylvania, Philadelphia, PA 19104, USA |
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Keywords | senescence p300 enhancers chromatin epigenetics |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 P.S., W.D., D.C.S. and S.L.B conceptualized the project. P.S. and C.Y.L. performed all wet lab experiments. Y.L. and G.D. performed bioinformatics. B.F. and D.C.S. constructed the shRNA library. S.S. and B.A.G. contributed to mass spec sample running and analysis. Q.C. and F.B.J. performed the TIF experiments. Z.D., L.J.L., P.D.A. and F.B.J. contributed to screen execution and design of follow-up experiments. Author contributions |
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SubjectTerms | Acetylation Cell Proliferation - genetics Cellular Senescence - genetics chromatin Chromatin - enzymology Chromatin - genetics Chromatin Assembly and Disassembly - genetics enhancers Epigenetic Repression epigenetics Fibroblasts - enzymology HEK293 Cells High-Throughput Nucleotide Sequencing - methods Histones - genetics Histones - metabolism Humans p300 p300-CBP Transcription Factors - genetics p300-CBP Transcription Factors - metabolism Protein Processing, Post-Translational RNA Interference RNA, Small Interfering - genetics RNA, Small Interfering - metabolism senescence Signal Transduction Time Factors Transcription, Genetic |
Title | Histone Acetyltransferase p300 Induces De Novo Super-Enhancers to Drive Cellular Senescence |
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