lncRNA DIGIT and BRD3 protein form phase-separated condensates to regulate endoderm differentiation

Cooperation between DNA, RNA and protein regulates gene expression and controls differentiation through interactions that connect regions of nucleic acids and protein domains and through the assembly of biomolecular condensates. Here, we report that endoderm differentiation is regulated by the inter...

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Published inNature cell biology Vol. 22; no. 10; pp. 1211 - 1222
Main Authors Daneshvar, Kaveh, Ardehali, M. Behfar, Klein, Isaac A., Hsieh, Fu-Kai, Kratkiewicz, Arcadia J., Mahpour, Amin, Cancelliere, Sabrina O. L., Zhou, Chan, Cook, Brett M., Li, Wenyang, Pondick, Joshua V., Gupta, Sweta K., Moran, Sean P., Young, Richard A., Kingston, Robert E., Mullen, Alan C.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.10.2020
Nature Publishing Group
Subjects
13/100
14
14/63
38
38/109
38/32
38/71
38/91
42
42/35
45
45/90
631/136/142
631/337/100/2285
631/337/384/2568
631/337/572
631/532/2117
82/58
82/83
Acetylation
Biomedical and Life Sciences
Cancer Research
Cell Biology
Cell Differentiation
Condensates
Cooperation
Cooperativity
Deoxyribonucleic acid
Depletion
Developmental Biology
Differentiation
DNA
Endoderm
Endoderm - cytology
Endoderm - metabolism
Enhancers
Gene expression
Genome, Human
Genomes
Histone H3
Histones
Histones - genetics
Histones - metabolism
Human Embryonic Stem Cells - cytology
Human Embryonic Stem Cells - metabolism
Humans
Life Sciences
Lysine
Lysine - genetics
Lysine - metabolism
Non-coding RNA
Nucleic acids
Phase Transition
Protein Domains
Protein Processing, Post-Translational
Proteins
Ribonucleic acid
RNA
RNA, Long Noncoding - genetics
Stem Cells
Transcription factors
Transcription Factors - genetics
Transcription Factors - metabolism
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Abstract Cooperation between DNA, RNA and protein regulates gene expression and controls differentiation through interactions that connect regions of nucleic acids and protein domains and through the assembly of biomolecular condensates. Here, we report that endoderm differentiation is regulated by the interaction between the long non-coding RNA (lncRNA) DIGIT and the bromodomain and extraterminal domain protein BRD3. BRD3 forms phase-separated condensates of which the formation is promoted by DIGIT, occupies enhancers of endoderm transcription factors and is required for endoderm differentiation. BRD3 binds to histone H3 acetylated at lysine 18 (H3K18ac) in vitro and co-occupies the genome with H3K18ac. DIGIT is also enriched in regions of H3K18ac, and the depletion of DIGIT results in decreased recruitment of BRD3 to these regions. Our findings show that cooperation between DIGIT and BRD3 at regions of H3K18ac regulates the transcription factors that drive endoderm differentiation and suggest that protein–lncRNA phase-separated condensates have a broader role as regulators of transcription. Daneshvar et al. show that BRD3 and the lncRNA DIGIT form phase-separated condensates at genomic regions with H3K18ac to co-regulate the transcription of genes that drive endoderm differentiation.
AbstractList Cooperation between DNA, RNA and protein regulates gene expression and controls differentiation through interactions that connect regions of nucleic acids and protein domains and through the assembly of biomolecular condensates. Here, we report that endoderm differentiation is regulated by the interaction between the long non-coding RNA (lncRNA) DIGIT and the bromodomain and extraterminal domain protein BRD3. BRD3 forms phase-separated condensates of which the formation is promoted by DIGIT, occupies enhancers of endoderm transcription factors and is required for endoderm differentiation. BRD3 binds to histone H3 acetylated at lysine 18 (H3K18ac) in vitro and co-occupies the genome with H3K18ac. DIGIT is also enriched in regions of H3K18ac, and the depletion of DIGIT results in decreased recruitment of BRD3 to these regions. Our findings show that cooperation between DIGIT and BRD3 at regions of H3K18ac regulates the transcription factors that drive endoderm differentiation and suggest that protein-lncRNA phase-separated condensates have a broader role as regulators of transcription.
Cooperation between DNA, RNA and protein regulates gene expression and controls differentiation through interactions that connect regions of nucleic acids and protein domains and through the assembly of biomolecular condensates. Here, we report that endoderm differentiation is regulated by the interaction between the long non-coding RNA (lncRNA) DIGIT and the bromodomain and extraterminal domain protein BRD3. BRD3 forms phase-separated condensates of which the formation is promoted by DIGIT, occupies enhancers of endoderm transcription factors and is required for endoderm differentiation. BRD3 binds to histone H3 acetylated at lysine 18 (H3K18ac) in vitro and co-occupies the genome with H3K18ac. DIGIT is also enriched in regions of H3K18ac, and the depletion of DIGIT results in decreased recruitment of BRD3 to these regions. Our findings show that cooperation between DIGIT and BRD3 at regions of H3K18ac regulates the transcription factors that drive endoderm differentiation and suggest that protein-lncRNA phase-separated condensates have a broader role as regulators of transcription.Cooperation between DNA, RNA and protein regulates gene expression and controls differentiation through interactions that connect regions of nucleic acids and protein domains and through the assembly of biomolecular condensates. Here, we report that endoderm differentiation is regulated by the interaction between the long non-coding RNA (lncRNA) DIGIT and the bromodomain and extraterminal domain protein BRD3. BRD3 forms phase-separated condensates of which the formation is promoted by DIGIT, occupies enhancers of endoderm transcription factors and is required for endoderm differentiation. BRD3 binds to histone H3 acetylated at lysine 18 (H3K18ac) in vitro and co-occupies the genome with H3K18ac. DIGIT is also enriched in regions of H3K18ac, and the depletion of DIGIT results in decreased recruitment of BRD3 to these regions. Our findings show that cooperation between DIGIT and BRD3 at regions of H3K18ac regulates the transcription factors that drive endoderm differentiation and suggest that protein-lncRNA phase-separated condensates have a broader role as regulators of transcription.
Cooperation between DNA, RNA and protein regulates gene expression and controls differentiation through interactions that connect regions of nucleic acids and protein domains and through the assembly of biomolecular condensates. Here, we report that endoderm differentiation is regulated by the interaction between the long non-coding RNA (lncRNA) DIGIT and the bromodomain and extraterminal domain protein BRD3. BRD3 forms phase-separated condensates of which the formation is promoted by DIGIT, occupies enhancers of endoderm transcription factors and is required for endoderm differentiation. BRD3 binds to histone H3 acetylated at lysine 18 (H3K18ac) in vitro and co-occupies the genome with H3K18ac. DIGIT is also enriched in regions of H3K18ac, and the depletion of DIGIT results in decreased recruitment of BRD3 to these regions. Our findings show that cooperation between DIGIT and BRD3 at regions of H3K18ac regulates the transcription factors that drive endoderm differentiation and suggest that protein–lncRNA phase-separated condensates have a broader role as regulators of transcription. Daneshvar et al. show that BRD3 and the lncRNA DIGIT form phase-separated condensates at genomic regions with H3K18ac to co-regulate the transcription of genes that drive endoderm differentiation.
Cooperation between DNA, RNA and protein regulates gene expression and controls differentiation through interactions connecting regions of nucleic acids and protein domains and through the assembly of biomolecular condensates. Here, we report that endoderm differentiation is regulated through the interaction of the long noncoding (lnc) RNA DIGIT and the bromodomain and extra-terminal domain protein BRD3. BRD3 forms phase-separated condensates, the formation of which are promoted by DIGIT , occupies enhancers of endoderm transcription factors, and is required for endoderm differentiation. BRD3 binds acetylated histone H3 lysine 18 (H3K18ac) in vitro and co-occupies the genome with H3K18ac. DIGIT is also enriched in regions of H3K18ac, and depletion of DIGIT results in decreased recruitment of BRD3 to these regions. Our findings show that cooperation between DIGIT and BRD3 at regions of H3K18ac regulates the transcription factors that drive endoderm differentiation and suggest a broader role for protein-lncRNA phase-separated condensates as regulators of transcription.
Cooperation between DNA, RNA and protein regulates gene expression and controls differentiation through interactions that connect regions of nucleic acids and protein domains and through the assembly of biomolecular condensates. Here, we report that endoderm differentiation is regulated by the interaction between the long non-coding RNA (lncRNA) DIGIT and the bromodomain and extraterminal domain protein BRD3. BRD3 forms phase-separated condensates of which the formation is promoted by DIGIT, occupies enhancers of endoderm transcription factors and is required for endoderm differentiation. BRD3 binds to histone H3 acetylated at lysine 18 (H3K18ac) in vitro and co-occupies the genome with H3K18ac. DIGIT is also enriched in regions of H3K18ac, and the depletion of DIGIT results in decreased recruitment of BRD3 to these regions. Our findings show that cooperation between DIGIT and BRD3 at regions of H3K18ac regulates the transcription factors that drive endoderm differentiation and suggest that protein–lncRNA phase-separated condensates have a broader role as regulators of transcription.Daneshvar et al. show that BRD3 and the lncRNA DIGIT form phase-separated condensates at genomic regions with H3K18ac to co-regulate the transcription of genes that drive endoderm differentiation.
Author Cancelliere, Sabrina O. L.
Mahpour, Amin
Cook, Brett M.
Young, Richard A.
Hsieh, Fu-Kai
Moran, Sean P.
Zhou, Chan
Pondick, Joshua V.
Daneshvar, Kaveh
Ardehali, M. Behfar
Gupta, Sweta K.
Klein, Isaac A.
Kingston, Robert E.
Kratkiewicz, Arcadia J.
Li, Wenyang
Mullen, Alan C.
AuthorAffiliation 3 Department of Molecular Biology and MGH Research Institute, Massachusetts General Hospital, Boston, MA 02114, USA
9 Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA
6 Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA
4 Department of Genetics, Harvard Medical School, Boston, MA 02115, USA
2 Harvard Medical School, Boston, MA 02115, USA
1 Gastrointestinal Unit, Massachusetts General Hospital, Boston, MA 02114, USA
5 Whitehead Institute for Biomedical Research, Cambridge, MA 02142, USA
8 Optical Biosystems, Inc. Santa Clara, CA 95050, USA
7 Harvard Stem Cell Institute, Cambridge, MA 02138, USA
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– name: 5 Whitehead Institute for Biomedical Research, Cambridge, MA 02142, USA
– name: 6 Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA
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– name: 8 Optical Biosystems, Inc. Santa Clara, CA 95050, USA
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/32895492$$D View this record in MEDLINE/PubMed
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Copyright The Author(s), under exclusive licence to Springer Nature Limited 2020
The Author(s), under exclusive licence to Springer Nature Limited 2020.
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Author contribution
K.D. and A.C.M. conceived the study. K.D. and A.C.M. designed the experiments with MB.A., I.A.K. and A.M. M.B.A made a conceptual contribution to the functional characterization of BRD3. Computational analyses were performed by C.Z. and A.M. with help from K.D., A.J.K., and S.P.M. Bench experiments were performed by K.D., M.B.A., I.A.K, F.H., A.J.K., S.O.L.C., A.M., W.L., B.M.C., S.K.G. and J.V.P. The manuscript was written by K.D. and A.C.M. with input from R.A.Y., R.E.K. and all other authors.
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0000-0002-4096-3106
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0000-0002-7863-0489
0000-0002-7157-8956
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  ident: 572_CR66
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btp352
– volume: 8
  start-page: e60298
  year: 2013
  ident: 572_CR60
  publication-title: PLoS ONE
  doi: 10.1371/journal.pone.0060298
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Snippet Cooperation between DNA, RNA and protein regulates gene expression and controls differentiation through interactions that connect regions of nucleic acids and...
Cooperation between DNA, RNA and protein regulates gene expression and controls differentiation through interactions connecting regions of nucleic acids and...
SourceID pubmedcentral
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springer
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StartPage 1211
SubjectTerms 13/100
14
14/63
38
38/109
38/32
38/71
38/91
42
42/35
45
45/90
631/136/142
631/337/100/2285
631/337/384/2568
631/337/572
631/532/2117
82/58
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Acetylation
Biomedical and Life Sciences
Cancer Research
Cell Biology
Cell Differentiation
Condensates
Cooperation
Cooperativity
Deoxyribonucleic acid
Depletion
Developmental Biology
Differentiation
DNA
Endoderm
Endoderm - cytology
Endoderm - metabolism
Enhancers
Gene expression
Genome, Human
Genomes
Histone H3
Histones
Histones - genetics
Histones - metabolism
Human Embryonic Stem Cells - cytology
Human Embryonic Stem Cells - metabolism
Humans
Life Sciences
Lysine
Lysine - genetics
Lysine - metabolism
Non-coding RNA
Nucleic acids
Phase Transition
Protein Domains
Protein Processing, Post-Translational
Proteins
Ribonucleic acid
RNA
RNA, Long Noncoding - genetics
Stem Cells
Transcription factors
Transcription Factors - genetics
Transcription Factors - metabolism
Title lncRNA DIGIT and BRD3 protein form phase-separated condensates to regulate endoderm differentiation
URI https://link.springer.com/article/10.1038/s41556-020-0572-2
https://www.ncbi.nlm.nih.gov/pubmed/32895492
https://www.proquest.com/docview/2449455367
https://www.proquest.com/docview/2727100127
https://www.proquest.com/docview/2440904302
https://pubmed.ncbi.nlm.nih.gov/PMC8008247
Volume 22
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