Integrating diverse datasets improves developmental enhancer prediction.
Identifieur interne : 002A86 ( PubMed/Corpus ); précédent : 002A85; suivant : 002A87Integrating diverse datasets improves developmental enhancer prediction.
Auteurs : Genevieve D. Erwin ; Nir Oksenberg ; Rebecca M. Truty ; Dennis Kostka ; Karl K. Murphy ; Nadav Ahituv ; Katherine S. Pollard ; John A. CapraSource :
- PLoS computational biology [ 1553-7358 ] ; 2014.
English descriptors
- KwdEn :
- MESH :
- chemical , genetics : Histones.
- genetics : Enhancer Elements, Genetic, Organ Specificity.
- methods : Genomics.
- Animals, Artificial Intelligence, Databases, Genetic, Genome-Wide Association Study, Humans, Mice, Mice, Transgenic, Models, Statistical.
Abstract
Gene-regulatory enhancers have been identified using various approaches, including evolutionary conservation, regulatory protein binding, chromatin modifications, and DNA sequence motifs. To integrate these different approaches, we developed EnhancerFinder, a two-step method for distinguishing developmental enhancers from the genomic background and then predicting their tissue specificity. EnhancerFinder uses a multiple kernel learning approach to integrate DNA sequence motifs, evolutionary patterns, and diverse functional genomics datasets from a variety of cell types. In contrast with prediction approaches that define enhancers based on histone marks or p300 sites from a single cell line, we trained EnhancerFinder on hundreds of experimentally verified human developmental enhancers from the VISTA Enhancer Browser. We comprehensively evaluated EnhancerFinder using cross validation and found that our integrative method improves the identification of enhancers over approaches that consider a single type of data, such as sequence motifs, evolutionary conservation, or the binding of enhancer-associated proteins. We find that VISTA enhancers active in embryonic heart are easier to identify than enhancers active in several other embryonic tissues, likely due to their uniquely high GC content. We applied EnhancerFinder to the entire human genome and predicted 84,301 developmental enhancers and their tissue specificity. These predictions provide specific functional annotations for large amounts of human non-coding DNA, and are significantly enriched near genes with annotated roles in their predicted tissues and lead SNPs from genome-wide association studies. We demonstrate the utility of EnhancerFinder predictions through in vivo validation of novel embryonic gene regulatory enhancers from three developmental transcription factor loci. Our genome-wide developmental enhancer predictions are freely available as a UCSC Genome Browser track, which we hope will enable researchers to further investigate questions in developmental biology.
DOI: 10.1371/journal.pcbi.1003677
PubMed: 24967590
Links to Exploration step
pubmed:24967590Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Integrating diverse datasets improves developmental enhancer prediction.</title><author><name sortKey="Erwin, Genevieve D" sort="Erwin, Genevieve D" uniqKey="Erwin G" first="Genevieve D" last="Erwin">Genevieve D. Erwin</name><affiliation><nlm:affiliation>Gladstone Institute of Cardiovascular Disease, San Francisco, California, United States of America; Institute for Human Genetics, University of California San Francisco, San Francisco, California, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Oksenberg, Nir" sort="Oksenberg, Nir" uniqKey="Oksenberg N" first="Nir" last="Oksenberg">Nir Oksenberg</name><affiliation><nlm:affiliation>Institute for Human Genetics, University of California San Francisco, San Francisco, California, United States of America; Department of Bioengineering and Therapeutic Sciences, University of California San Francisco, San Francisco, California, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Truty, Rebecca M" sort="Truty, Rebecca M" uniqKey="Truty R" first="Rebecca M" last="Truty">Rebecca M. Truty</name><affiliation><nlm:affiliation>Gladstone Institute of Cardiovascular Disease, San Francisco, California, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Kostka, Dennis" sort="Kostka, Dennis" uniqKey="Kostka D" first="Dennis" last="Kostka">Dennis Kostka</name><affiliation><nlm:affiliation>Department of Developmental Biology and Department of Computational and Systems Biology, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Murphy, Karl K" sort="Murphy, Karl K" uniqKey="Murphy K" first="Karl K" last="Murphy">Karl K. Murphy</name><affiliation><nlm:affiliation>Institute for Human Genetics, University of California San Francisco, San Francisco, California, United States of America; Department of Bioengineering and Therapeutic Sciences, University of California San Francisco, San Francisco, California, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Ahituv, Nadav" sort="Ahituv, Nadav" uniqKey="Ahituv N" first="Nadav" last="Ahituv">Nadav Ahituv</name><affiliation><nlm:affiliation>Institute for Human Genetics, University of California San Francisco, San Francisco, California, United States of America; Department of Bioengineering and Therapeutic Sciences, University of California San Francisco, San Francisco, California, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Pollard, Katherine S" sort="Pollard, Katherine S" uniqKey="Pollard K" first="Katherine S" last="Pollard">Katherine S. Pollard</name><affiliation><nlm:affiliation>Gladstone Institute of Cardiovascular Disease, San Francisco, California, United States of America; Institute for Human Genetics, University of California San Francisco, San Francisco, California, United States of America; Department of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, California, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Capra, John A" sort="Capra, John A" uniqKey="Capra J" first="John A" last="Capra">John A. Capra</name><affiliation><nlm:affiliation>Center for Human Genetics Research and Department of Biomedical Informatics, Vanderbilt University, Nashville, Tennessee, United States of America.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2014">2014</date><idno type="RBID">pubmed:24967590</idno><idno type="pmid">24967590</idno><idno type="doi">10.1371/journal.pcbi.1003677</idno><idno type="wicri:Area/PubMed/Corpus">002A86</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Corpus" wicri:corpus="PubMed">002A86</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Integrating diverse datasets improves developmental enhancer prediction.</title><author><name sortKey="Erwin, Genevieve D" sort="Erwin, Genevieve D" uniqKey="Erwin G" first="Genevieve D" last="Erwin">Genevieve D. Erwin</name><affiliation><nlm:affiliation>Gladstone Institute of Cardiovascular Disease, San Francisco, California, United States of America; Institute for Human Genetics, University of California San Francisco, San Francisco, California, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Oksenberg, Nir" sort="Oksenberg, Nir" uniqKey="Oksenberg N" first="Nir" last="Oksenberg">Nir Oksenberg</name><affiliation><nlm:affiliation>Institute for Human Genetics, University of California San Francisco, San Francisco, California, United States of America; Department of Bioengineering and Therapeutic Sciences, University of California San Francisco, San Francisco, California, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Truty, Rebecca M" sort="Truty, Rebecca M" uniqKey="Truty R" first="Rebecca M" last="Truty">Rebecca M. Truty</name><affiliation><nlm:affiliation>Gladstone Institute of Cardiovascular Disease, San Francisco, California, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Kostka, Dennis" sort="Kostka, Dennis" uniqKey="Kostka D" first="Dennis" last="Kostka">Dennis Kostka</name><affiliation><nlm:affiliation>Department of Developmental Biology and Department of Computational and Systems Biology, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Murphy, Karl K" sort="Murphy, Karl K" uniqKey="Murphy K" first="Karl K" last="Murphy">Karl K. Murphy</name><affiliation><nlm:affiliation>Institute for Human Genetics, University of California San Francisco, San Francisco, California, United States of America; Department of Bioengineering and Therapeutic Sciences, University of California San Francisco, San Francisco, California, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Ahituv, Nadav" sort="Ahituv, Nadav" uniqKey="Ahituv N" first="Nadav" last="Ahituv">Nadav Ahituv</name><affiliation><nlm:affiliation>Institute for Human Genetics, University of California San Francisco, San Francisco, California, United States of America; Department of Bioengineering and Therapeutic Sciences, University of California San Francisco, San Francisco, California, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Pollard, Katherine S" sort="Pollard, Katherine S" uniqKey="Pollard K" first="Katherine S" last="Pollard">Katherine S. Pollard</name><affiliation><nlm:affiliation>Gladstone Institute of Cardiovascular Disease, San Francisco, California, United States of America; Institute for Human Genetics, University of California San Francisco, San Francisco, California, United States of America; Department of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, California, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Capra, John A" sort="Capra, John A" uniqKey="Capra J" first="John A" last="Capra">John A. Capra</name><affiliation><nlm:affiliation>Center for Human Genetics Research and Department of Biomedical Informatics, Vanderbilt University, Nashville, Tennessee, United States of America.</nlm:affiliation></affiliation></author></analytic><series><title level="j">PLoS computational biology</title><idno type="eISSN">1553-7358</idno><imprint><date when="2014" type="published">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Artificial Intelligence</term><term>Databases, Genetic</term><term>Enhancer Elements, Genetic (genetics)</term><term>Genome-Wide Association Study</term><term>Genomics (methods)</term><term>Histones (genetics)</term><term>Humans</term><term>Mice</term><term>Mice, Transgenic</term><term>Models, Statistical</term><term>Organ Specificity (genetics)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Histones</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Enhancer Elements, Genetic</term><term>Organ Specificity</term></keywords><keywords scheme="MESH" qualifier="methods" xml:lang="en"><term>Genomics</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Artificial Intelligence</term><term>Databases, Genetic</term><term>Genome-Wide Association Study</term><term>Humans</term><term>Mice</term><term>Mice, Transgenic</term><term>Models, Statistical</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Gene-regulatory enhancers have been identified using various approaches, including evolutionary conservation, regulatory protein binding, chromatin modifications, and DNA sequence motifs. To integrate these different approaches, we developed EnhancerFinder, a two-step method for distinguishing developmental enhancers from the genomic background and then predicting their tissue specificity. EnhancerFinder uses a multiple kernel learning approach to integrate DNA sequence motifs, evolutionary patterns, and diverse functional genomics datasets from a variety of cell types. In contrast with prediction approaches that define enhancers based on histone marks or p300 sites from a single cell line, we trained EnhancerFinder on hundreds of experimentally verified human developmental enhancers from the VISTA Enhancer Browser. We comprehensively evaluated EnhancerFinder using cross validation and found that our integrative method improves the identification of enhancers over approaches that consider a single type of data, such as sequence motifs, evolutionary conservation, or the binding of enhancer-associated proteins. We find that VISTA enhancers active in embryonic heart are easier to identify than enhancers active in several other embryonic tissues, likely due to their uniquely high GC content. We applied EnhancerFinder to the entire human genome and predicted 84,301 developmental enhancers and their tissue specificity. These predictions provide specific functional annotations for large amounts of human non-coding DNA, and are significantly enriched near genes with annotated roles in their predicted tissues and lead SNPs from genome-wide association studies. We demonstrate the utility of EnhancerFinder predictions through in vivo validation of novel embryonic gene regulatory enhancers from three developmental transcription factor loci. Our genome-wide developmental enhancer predictions are freely available as a UCSC Genome Browser track, which we hope will enable researchers to further investigate questions in developmental biology.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">24967590</PMID><DateCreated><Year>2014</Year><Month>06</Month><Day>27</Day></DateCreated><DateCompleted><Year>2015</Year><Month>10</Month><Day>20</Day></DateCompleted><DateRevised><Year>2017</Year><Month>02</Month><Day>20</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">1553-7358</ISSN><JournalIssue CitedMedium="Internet"><Volume>10</Volume><Issue>6</Issue><PubDate><Year>2014</Year><Month>Jun</Month></PubDate></JournalIssue><Title>PLoS computational biology</Title><ISOAbbreviation>PLoS Comput. Biol.</ISOAbbreviation></Journal><ArticleTitle>Integrating diverse datasets improves developmental enhancer prediction.</ArticleTitle><Pagination><MedlinePgn>e1003677</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.pcbi.1003677</ELocationID><Abstract><AbstractText>Gene-regulatory enhancers have been identified using various approaches, including evolutionary conservation, regulatory protein binding, chromatin modifications, and DNA sequence motifs. To integrate these different approaches, we developed EnhancerFinder, a two-step method for distinguishing developmental enhancers from the genomic background and then predicting their tissue specificity. EnhancerFinder uses a multiple kernel learning approach to integrate DNA sequence motifs, evolutionary patterns, and diverse functional genomics datasets from a variety of cell types. In contrast with prediction approaches that define enhancers based on histone marks or p300 sites from a single cell line, we trained EnhancerFinder on hundreds of experimentally verified human developmental enhancers from the VISTA Enhancer Browser. We comprehensively evaluated EnhancerFinder using cross validation and found that our integrative method improves the identification of enhancers over approaches that consider a single type of data, such as sequence motifs, evolutionary conservation, or the binding of enhancer-associated proteins. We find that VISTA enhancers active in embryonic heart are easier to identify than enhancers active in several other embryonic tissues, likely due to their uniquely high GC content. We applied EnhancerFinder to the entire human genome and predicted 84,301 developmental enhancers and their tissue specificity. These predictions provide specific functional annotations for large amounts of human non-coding DNA, and are significantly enriched near genes with annotated roles in their predicted tissues and lead SNPs from genome-wide association studies. We demonstrate the utility of EnhancerFinder predictions through in vivo validation of novel embryonic gene regulatory enhancers from three developmental transcription factor loci. Our genome-wide developmental enhancer predictions are freely available as a UCSC Genome Browser track, which we hope will enable researchers to further investigate questions in developmental biology.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Erwin</LastName><ForeName>Genevieve D</ForeName><Initials>GD</Initials><AffiliationInfo><Affiliation>Gladstone Institute of Cardiovascular Disease, San Francisco, California, United States of America; Institute for Human Genetics, University of California San Francisco, San Francisco, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Oksenberg</LastName><ForeName>Nir</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Institute for Human Genetics, University of California San Francisco, San Francisco, California, United States of America; Department of Bioengineering and Therapeutic Sciences, University of California San Francisco, San Francisco, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Truty</LastName><ForeName>Rebecca M</ForeName><Initials>RM</Initials><AffiliationInfo><Affiliation>Gladstone Institute of Cardiovascular Disease, San Francisco, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kostka</LastName><ForeName>Dennis</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Department of Developmental Biology and Department of Computational and Systems Biology, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Murphy</LastName><ForeName>Karl K</ForeName><Initials>KK</Initials><AffiliationInfo><Affiliation>Institute for Human Genetics, University of California San Francisco, San Francisco, California, United States of America; Department of Bioengineering and Therapeutic Sciences, University of California San Francisco, San Francisco, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ahituv</LastName><ForeName>Nadav</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Institute for Human Genetics, University of California San Francisco, San Francisco, California, United States of America; Department of Bioengineering and Therapeutic Sciences, University of California San Francisco, San Francisco, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pollard</LastName><ForeName>Katherine S</ForeName><Initials>KS</Initials><AffiliationInfo><Affiliation>Gladstone Institute of Cardiovascular Disease, San Francisco, California, United States of America; Institute for Human Genetics, University of California San Francisco, San Francisco, California, United States of America; Department of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Capra</LastName><ForeName>John A</ForeName><Initials>JA</Initials><AffiliationInfo><Affiliation>Center for Human Genetics Research and Department of Biomedical Informatics, Vanderbilt University, Nashville, Tennessee, United States of America.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>HL098179</GrantID><Acronym>HL</Acronym><Agency>NHLBI NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>HD059862</GrantID><Acronym>HD</Acronym><Agency>NICHD NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>HG005058</GrantID><Acronym>HG</Acronym><Agency>NHGRI NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>T32 GM067547</GrantID><Acronym>GM</Acronym><Agency>NIGMS NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>U01 HL098188</GrantID><Acronym>HL</Acronym><Agency>NHLBI NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>DK090382</GrantID><Acronym>DK</Acronym><Agency>NIDDK NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>GM61390</GrantID><Acronym>GM</Acronym><Agency>NIGMS NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>HG006768</GrantID><Acronym>HG</Acronym><Agency>NHGRI NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>NS079231</GrantID><Acronym>NS</Acronym><Agency>NINDS NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>GM082901</GrantID><Acronym>GM</Acronym><Agency>NIGMS NIH HHS</Agency><Country>United States</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D052061">Research Support, N.I.H., Extramural</PublicationType><PublicationType UI="D013485">Research 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