Enhancer Features that Drive Formation of Transcriptional Condensates

Enhancers are DNA elements that are bound by transcription factors (TFs), which recruit coactivators and the transcriptional machinery to genes. Phase-separated condensates of TFs and coactivators have been implicated in assembling the transcription machinery at particular enhancers, yet the role of...

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Published in	Molecular cell Vol. 75; no. 3; pp. 549 - 561.e7
Main Authors	Shrinivas, Krishna, Sabari, Benjamin R., Coffey, Eliot L., Klein, Isaac A., Boija, Ann, Zamudio, Alicia V., Schuijers, Jurian, Hannett, Nancy M., Sharp, Phillip A., Young, Richard A., Chakraborty, Arup K.
Format	Journal Article
Language	English
Published	United States Elsevier Inc 08.08.2019
Subjects	Animals Base Sequence - genetics binding sites Binding Sites - genetics Chromatin - genetics coactivator complement condensate condensates cooperativity DNA DNA - genetics DNA-Binding Proteins - genetics enhancer Enhancer Elements, Genetic Gene Expression Regulation genes Genomics loci Mice Mouse Embryonic Stem Cells multivalence nucleotide sequences phase separation regulatory element separation specificity transcription transcription (genetics) transcription factor transcription factors Transcription Factors - genetics Transcription, Genetic transcription factor enhancer phase separation regulatory element transcription cooperativity specificity condensate multivalence coactivator
Online Access	Get full text
ISSN	1097-2765 1097-4164 1097-4164
DOI	10.1016/j.molcel.2019.07.009

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Abstract	Enhancers are DNA elements that are bound by transcription factors (TFs), which recruit coactivators and the transcriptional machinery to genes. Phase-separated condensates of TFs and coactivators have been implicated in assembling the transcription machinery at particular enhancers, yet the role of DNA sequence in this process has not been explored. We show that DNA sequences encoding TF binding site number, density, and affinity above sharply defined thresholds drive condensation of TFs and coactivators. A combination of specific structured (TF-DNA) and weak multivalent (TF-coactivator) interactions allows for condensates to form at particular genomic loci determined by the DNA sequence and the complement of expressed TFs. DNA features found to drive condensation promote enhancer activity and transcription in cells. Our study provides a framework to understand how the genome can scaffold transcriptional condensates at specific loci and how the universal phenomenon of phase separation might regulate this process. [Display omitted] •Transcription machinery forms condensates localized to specific DNA elements•Combination of structured and dynamic interactions enables localized condensation•DNA encoding binding site features above threshold values drive condensation•DNA features that drive condensation promote enhancer activity in cells Shrinivas et al. demonstrate that specific types of motif compositions encoded in DNA drive localized formation of transcriptional condensates. These findings explain how phase separation can occur at specific genomic locations and shed light on why only some genomic loci become highly active enhancers.
AbstractList	Enhancers are DNA elements that are bound by transcription factors (TFs), which recruit coactivators and the transcriptional machinery to genes. Phase-separated condensates of TFs and coactivators have been implicated in assembling the transcription machinery at particular enhancers, yet the role of DNA sequence in this process has not been explored. We show that DNA sequences encoding TF binding site number, density, and affinity above sharply defined thresholds drive condensation of TFs and coactivators. A combination of specific structured (TF-DNA) and weak multivalent (TF-coactivator) interactions allows for condensates to form at particular genomic loci determined by the DNA sequence and the complement of expressed TFs. DNA features found to drive condensation promote enhancer activity and transcription in cells. Our study provides a framework to understand how the genome can scaffold transcriptional condensates at specific loci and how the universal phenomenon of phase separation might regulate this process. [Display omitted] •Transcription machinery forms condensates localized to specific DNA elements•Combination of structured and dynamic interactions enables localized condensation•DNA encoding binding site features above threshold values drive condensation•DNA features that drive condensation promote enhancer activity in cells Shrinivas et al. demonstrate that specific types of motif compositions encoded in DNA drive localized formation of transcriptional condensates. These findings explain how phase separation can occur at specific genomic locations and shed light on why only some genomic loci become highly active enhancers. Enhancers are DNA elements that are bound by transcription factors (TFs), which recruit coactivators and the transcriptional machinery to genes. Phase-separated condensates of TFs and coactivators have been implicated in assembling the transcription machinery at particular enhancers, yet the role of DNA sequence in this process has not been explored. We show that DNA sequences encoding TF binding site number, density, and affinity above sharply defined thresholds drive condensation of TFs and coactivators. A combination of specific structured (TF-DNA) and weak multivalent (TF-coactivator) interactions allows for condensates to form at particular genomic loci determined by the DNA sequence and the complement of expressed TFs. DNA features found to drive condensation promote enhancer activity and transcription in cells. Our study provides a framework to understand how the genome can scaffold transcriptional condensates at specific loci and how the universal phenomenon of phase separation might regulate this process.Enhancers are DNA elements that are bound by transcription factors (TFs), which recruit coactivators and the transcriptional machinery to genes. Phase-separated condensates of TFs and coactivators have been implicated in assembling the transcription machinery at particular enhancers, yet the role of DNA sequence in this process has not been explored. We show that DNA sequences encoding TF binding site number, density, and affinity above sharply defined thresholds drive condensation of TFs and coactivators. A combination of specific structured (TF-DNA) and weak multivalent (TF-coactivator) interactions allows for condensates to form at particular genomic loci determined by the DNA sequence and the complement of expressed TFs. DNA features found to drive condensation promote enhancer activity and transcription in cells. Our study provides a framework to understand how the genome can scaffold transcriptional condensates at specific loci and how the universal phenomenon of phase separation might regulate this process. Enhancers are DNA elements that are bound by transcription factors (TFs), which recruit coactivators and the transcriptional machinery to genes. Phase-separated condensates of TFs and coactivators have been implicated in assembling the transcription machinery at particular enhancers, yet the role of DNA sequence in this process has not been explored. We show that DNA sequences encoding TF binding site number, density, and affinity above sharply defined thresholds drive condensation of TFs and coactivators. A combination of specific structured (TF-DNA) and weak multivalent (TF-coactivator) interactions allows for condensates to form at particular genomic loci determined by the DNA sequence and the complement of expressed TFs. DNA features found to drive condensation promote enhancer activity and transcription in cells. Our study provides a framework to understand how the genome can scaffold transcriptional condensates at specific loci, and how the universal phenonomenon of phase separation might regulate this process. Shrinivas et al. demonstrate that specific types of motif compositions encoded in DNA drive localized formation of transcriptional condensates. These findings explain how phase separation can occur at specific genomic locations and shed light on why only some genomic loci become highly active enhancers. Enhancers are DNA elements that are bound by transcription factors (TFs), which recruit coactivators and the transcriptional machinery to genes. Phase-separated condensates of TFs and coactivators have been implicated in assembling the transcription machinery at particular enhancers, yet the role of DNA sequence in this process has not been explored. We show that DNA sequences encoding TF binding site number, density, and affinity above sharply defined thresholds drive condensation of TFs and coactivators. A combination of specific structured (TF-DNA) and weak multivalent (TF-coactivator) interactions allows for condensates to form at particular genomic loci determined by the DNA sequence and the complement of expressed TFs. DNA features found to drive condensation promote enhancer activity and transcription in cells. Our study provides a framework to understand how the genome can scaffold transcriptional condensates at specific loci and how the universal phenomenon of phase separation might regulate this process.
Author	Shrinivas, Krishna Coffey, Eliot L. Sharp, Phillip A. Chakraborty, Arup K. Zamudio, Alicia V. Young, Richard A. Sabari, Benjamin R. Boija, Ann Hannett, Nancy M. Klein, Isaac A. Schuijers, Jurian
AuthorAffiliation	3 Whitehead Institute for Biomedical Research, 455 Main Street, Cambridge, MA 02142 USA 5 Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School Boston, MA 02215 USA 4 Department of Biology, Massachusetts Institute of Technology, Cambridge MA 02139 USA 8 Ragon Institute of Massachusetts General Hospital, Massachusetts Institute of Technology, and Harvard University, Cambridge MA 02139 USA 7 Department of Physics, Massachusetts Institute of Technology, Cambridge MA 02139 USA 10 These authors contributed equally 1 Department of Chemical Engineering, Massachusetts Institute of Technology, Cambridge MA 02139 USA 9 Department of Chemistry, Massachusetts Institute of Technology, Cambridge MA 02139 USA 11 Lead contact 2 Institute of Medical Engineering & Science, Massachusetts Institute of Technology, Cambridge MA 02139 USA 6 Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge MA 02139 USA
AuthorAffiliation_xml	– name: 1 Department of Chemical Engineering, Massachusetts Institute of Technology, Cambridge MA 02139 USA – name: 11 Lead contact – name: 2 Institute of Medical Engineering & Science, Massachusetts Institute of Technology, Cambridge MA 02139 USA – name: 4 Department of Biology, Massachusetts Institute of Technology, Cambridge MA 02139 USA – name: 5 Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School Boston, MA 02215 USA – name: 9 Department of Chemistry, Massachusetts Institute of Technology, Cambridge MA 02139 USA – name: 7 Department of Physics, Massachusetts Institute of Technology, Cambridge MA 02139 USA – name: 10 These authors contributed equally – name: 6 Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge MA 02139 USA – name: 3 Whitehead Institute for Biomedical Research, 455 Main Street, Cambridge, MA 02142 USA – name: 8 Ragon Institute of Massachusetts General Hospital, Massachusetts Institute of Technology, and Harvard University, Cambridge MA 02139 USA
Author_xml	– sequence: 1 givenname: Krishna surname: Shrinivas fullname: Shrinivas, Krishna organization: Department of Chemical Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA – sequence: 2 givenname: Benjamin R. surname: Sabari fullname: Sabari, Benjamin R. organization: Whitehead Institute for Biomedical Research, 455 Main Street, Cambridge, MA 02142, USA – sequence: 3 givenname: Eliot L. surname: Coffey fullname: Coffey, Eliot L. organization: Whitehead Institute for Biomedical Research, 455 Main Street, Cambridge, MA 02142, USA – sequence: 4 givenname: Isaac A. surname: Klein fullname: Klein, Isaac A. organization: Whitehead Institute for Biomedical Research, 455 Main Street, Cambridge, MA 02142, USA – sequence: 5 givenname: Ann surname: Boija fullname: Boija, Ann organization: Whitehead Institute for Biomedical Research, 455 Main Street, Cambridge, MA 02142, USA – sequence: 6 givenname: Alicia V. surname: Zamudio fullname: Zamudio, Alicia V. organization: Whitehead Institute for Biomedical Research, 455 Main Street, Cambridge, MA 02142, USA – sequence: 7 givenname: Jurian surname: Schuijers fullname: Schuijers, Jurian organization: Whitehead Institute for Biomedical Research, 455 Main Street, Cambridge, MA 02142, USA – sequence: 8 givenname: Nancy M. surname: Hannett fullname: Hannett, Nancy M. organization: Whitehead Institute for Biomedical Research, 455 Main Street, Cambridge, MA 02142, USA – sequence: 9 givenname: Phillip A. surname: Sharp fullname: Sharp, Phillip A. email: sharppa@mit.edu organization: Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA – sequence: 10 givenname: Richard A. surname: Young fullname: Young, Richard A. email: young@wi.mit.edu organization: Whitehead Institute for Biomedical Research, 455 Main Street, Cambridge, MA 02142, USA – sequence: 11 givenname: Arup K. surname: Chakraborty fullname: Chakraborty, Arup K. email: arupc@mit.edu organization: Department of Chemical Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/31398323$$D View this record in MEDLINE/PubMed
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Author Contributions: Conceptualization: K.S., B.R.S., P.A.S., A.K.C., R.A.Y. Methodology: K.S., B.R.S., A.K.C., A.V.Z, J.S., E.L.C., I.A.K., A.B. Software: K.S. Formal Analysis: K.S. Investigation: K.S., B.R.S., A.V.Z, J.S., E.L.C., I.A.K., A.B. Resources: J.S., I.A.K., A.B., N.M.H, P.A.S., A.K.C., R.A.Y. Data Curation: K.S. Writing - Original Draft: K.S., B.R.S., P.A.S., A.K.C., R.A.Y. Writing - Reviewing and Editing: All authors. Visualization: K.S., B.R.S., A.V.Z. Supervision: P.A.S., A.K.C., R.A.Y. Funding Acquisition: P.A.S., A.K.C., R.A.Y.
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Snippet	Enhancers are DNA elements that are bound by transcription factors (TFs), which recruit coactivators and the transcriptional machinery to genes....
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SubjectTerms	Animals Base Sequence - genetics binding sites Binding Sites - genetics Chromatin - genetics coactivator complement condensate condensates cooperativity DNA DNA - genetics DNA-Binding Proteins - genetics enhancer Enhancer Elements, Genetic Gene Expression Regulation genes Genomics loci Mice Mouse Embryonic Stem Cells multivalence nucleotide sequences phase separation regulatory element separation specificity transcription transcription (genetics) transcription factor transcription factors Transcription Factors - genetics Transcription, Genetic
Title	Enhancer Features that Drive Formation of Transcriptional Condensates
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