Coregulation of transcription factor binding and nucleosome occupancy through DNA features of mammalian enhancers

Transcription factors (TFs) preferentially bind sites contained in regions of computationally predicted high nucleosomal occupancy, suggesting that nucleosomes are gatekeepers of TF binding sites. However, because of their complexity mammalian genomes contain millions of randomly occurring, unbound...

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Published in:	Molecular cell Vol. 54; no. 5; p. 844
Main Authors:	Barozzi, Iros, Simonatto, Marta, Bonifacio, Silvia, Yang, Lin, Rohs, Remo, Ghisletti, Serena, Natoli, Gioacchino
Format:	Journal Article
Language:	English
Published:	United States 05.06.2014
Subjects:	Animals Base Sequence Binding Sites Cells, Cultured Consensus Sequence Enhancer Elements, Genetic Gene Expression Regulation Gene Knockdown Techniques Humans Mice Models, Genetic Nucleosomes - genetics Nucleosomes - metabolism Proto-Oncogene Proteins - genetics Proto-Oncogene Proteins - metabolism RNA, Small Interfering - genetics Sequence Analysis, DNA Support Vector Machine Trans-Activators - genetics Trans-Activators - metabolism
ISSN:	1097-4164, 1097-4164
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Abstract	Transcription factors (TFs) preferentially bind sites contained in regions of computationally predicted high nucleosomal occupancy, suggesting that nucleosomes are gatekeepers of TF binding sites. However, because of their complexity mammalian genomes contain millions of randomly occurring, unbound TF consensus binding sites. We hypothesized that the information controlling nucleosome assembly may coincide with the information that enables TFs to bind cis-regulatory elements while ignoring randomly occurring sites. Hence, nucleosomes would selectively mask genomic sites that can be contacted by TFs and thus be potentially functional. The hematopoietic pioneer TF Pu.1 maintained nucleosome depletion at macrophage-specific enhancers that displayed a broad range of nucleosome occupancy in other cell types and in reconstituted chromatin. We identified a minimal set of DNA sequence and shape features that accurately predicted both Pu.1 binding and nucleosome occupancy genome-wide. These data reveal a basic organizational principle of mammalian cis-regulatory elements whereby TF recruitment and nucleosome deposition are controlled by overlapping DNA sequence features.
AbstractList	Transcription factors (TFs) preferentially bind sites contained in regions of computationally predicted high nucleosomal occupancy, suggesting that nucleosomes are gatekeepers of TF binding sites. However, because of their complexity mammalian genomes contain millions of randomly occurring, unbound TF consensus binding sites. We hypothesized that the information controlling nucleosome assembly may coincide with the information that enables TFs to bind cis-regulatory elements while ignoring randomly occurring sites. Hence, nucleosomes would selectively mask genomic sites that can be contacted by TFs and thus be potentially functional. The hematopoietic pioneer TF Pu.1 maintained nucleosome depletion at macrophage-specific enhancers that displayed a broad range of nucleosome occupancy in other cell types and in reconstituted chromatin. We identified a minimal set of DNA sequence and shape features that accurately predicted both Pu.1 binding and nucleosome occupancy genome-wide. These data reveal a basic organizational principle of mammalian cis-regulatory elements whereby TF recruitment and nucleosome deposition are controlled by overlapping DNA sequence features.Transcription factors (TFs) preferentially bind sites contained in regions of computationally predicted high nucleosomal occupancy, suggesting that nucleosomes are gatekeepers of TF binding sites. However, because of their complexity mammalian genomes contain millions of randomly occurring, unbound TF consensus binding sites. We hypothesized that the information controlling nucleosome assembly may coincide with the information that enables TFs to bind cis-regulatory elements while ignoring randomly occurring sites. Hence, nucleosomes would selectively mask genomic sites that can be contacted by TFs and thus be potentially functional. The hematopoietic pioneer TF Pu.1 maintained nucleosome depletion at macrophage-specific enhancers that displayed a broad range of nucleosome occupancy in other cell types and in reconstituted chromatin. We identified a minimal set of DNA sequence and shape features that accurately predicted both Pu.1 binding and nucleosome occupancy genome-wide. These data reveal a basic organizational principle of mammalian cis-regulatory elements whereby TF recruitment and nucleosome deposition are controlled by overlapping DNA sequence features. Transcription factors (TFs) preferentially bind sites contained in regions of computationally predicted high nucleosomal occupancy, suggesting that nucleosomes are gatekeepers of TF binding sites. However, because of their complexity mammalian genomes contain millions of randomly occurring, unbound TF consensus binding sites. We hypothesized that the information controlling nucleosome assembly may coincide with the information that enables TFs to bind cis-regulatory elements while ignoring randomly occurring sites. Hence, nucleosomes would selectively mask genomic sites that can be contacted by TFs and thus be potentially functional. The hematopoietic pioneer TF Pu.1 maintained nucleosome depletion at macrophage-specific enhancers that displayed a broad range of nucleosome occupancy in other cell types and in reconstituted chromatin. We identified a minimal set of DNA sequence and shape features that accurately predicted both Pu.1 binding and nucleosome occupancy genome-wide. These data reveal a basic organizational principle of mammalian cis-regulatory elements whereby TF recruitment and nucleosome deposition are controlled by overlapping DNA sequence features.
Author	Bonifacio, Silvia Barozzi, Iros Yang, Lin Ghisletti, Serena Rohs, Remo Simonatto, Marta Natoli, Gioacchino
Author_xml	– sequence: 1 givenname: Iros surname: Barozzi fullname: Barozzi, Iros organization: Department of Experimental Oncology, European Institute of Oncology (IEO), Via Adamello 16, I-20139 Milan, Italy – sequence: 2 givenname: Marta surname: Simonatto fullname: Simonatto, Marta organization: Department of Experimental Oncology, European Institute of Oncology (IEO), Via Adamello 16, I-20139 Milan, Italy – sequence: 3 givenname: Silvia surname: Bonifacio fullname: Bonifacio, Silvia organization: Department of Experimental Oncology, European Institute of Oncology (IEO), Via Adamello 16, I-20139 Milan, Italy – sequence: 4 givenname: Lin surname: Yang fullname: Yang, Lin organization: Molecular and Computational Biology Program, University of Southern California, Los Angeles, CA 90089, USA – sequence: 5 givenname: Remo surname: Rohs fullname: Rohs, Remo organization: Molecular and Computational Biology Program, University of Southern California, Los Angeles, CA 90089, USA – sequence: 6 givenname: Serena surname: Ghisletti fullname: Ghisletti, Serena organization: Department of Experimental Oncology, European Institute of Oncology (IEO), Via Adamello 16, I-20139 Milan, Italy – sequence: 7 givenname: Gioacchino surname: Natoli fullname: Natoli, Gioacchino organization: Department of Experimental Oncology, European Institute of Oncology (IEO), Via Adamello 16, I-20139 Milan, Italy
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Snippet	Transcription factors (TFs) preferentially bind sites contained in regions of computationally predicted high nucleosomal occupancy, suggesting that nucleosomes...
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SubjectTerms	Animals Base Sequence Binding Sites Cells, Cultured Consensus Sequence Enhancer Elements, Genetic Gene Expression Regulation Gene Knockdown Techniques Humans Mice Models, Genetic Nucleosomes - genetics Nucleosomes - metabolism Proto-Oncogene Proteins - genetics Proto-Oncogene Proteins - metabolism RNA, Small Interfering - genetics Sequence Analysis, DNA Support Vector Machine Trans-Activators - genetics Trans-Activators - metabolism
Title	Coregulation of transcription factor binding and nucleosome occupancy through DNA features of mammalian enhancers
URI	https://www.ncbi.nlm.nih.gov/pubmed/24813947 https://www.proquest.com/docview/1534474220
Volume	54
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