Cooperative binding of AP-1 and TEAD4 modulates the balance between vascular smooth muscle and hemogenic cell fate
The transmission of extracellular signals into the nucleus involves inducible transcription factors, but how different signalling pathways act in a cell type-specific fashion is poorly understood. Here, we studied the regulatory role of the AP-1 transcription factor family in blood development using...
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Veröffentlicht in: | Development (Cambridge) 2016-12, Vol.143 (23), p.4324-4340 |
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creator | Obier, Nadine Cauchy, Pierre Assi, Salam A Gilmour, Jane Lie-A-Ling, Michael Lichtinger, Monika Hoogenkamp, Maarten Noailles, Laura Cockerill, Peter N Lacaud, Georges Kouskoff, Valerie Bonifer, Constanze |
description | The transmission of extracellular signals into the nucleus involves inducible transcription factors, but how different signalling pathways act in a cell type-specific fashion is poorly understood. Here, we studied the regulatory role of the AP-1 transcription factor family in blood development using embryonic stem cell differentiation coupled with genome-wide transcription factor binding and gene expression analyses. AP-1 factors respond to MAP kinase signalling and comprise dimers of FOS, ATF and JUN proteins. To examine genes regulated by AP-1 and to examine how it interacts with other inducible transcription factors, we abrogated its global DNA-binding activity using a dominant-negative FOS peptide. We show that FOS and JUN bind to and activate a specific set of vascular genes and that AP-1 inhibition shifts the balance between smooth muscle and hematopoietic differentiation towards blood. Furthermore, AP-1 is required for de novo binding of TEAD4, a transcription factor connected to Hippo signalling. Our bottom-up approach demonstrates that AP-1- and TEAD4-associated cis-regulatory elements form hubs for multiple signalling-responsive transcription factors and define the cistrome that regulates vascular and hematopoietic development by extrinsic signals. |
doi_str_mv | 10.1242/dev.139857 |
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Here, we studied the regulatory role of the AP-1 transcription factor family in blood development using embryonic stem cell differentiation coupled with genome-wide transcription factor binding and gene expression analyses. AP-1 factors respond to MAP kinase signalling and comprise dimers of FOS, ATF and JUN proteins. To examine genes regulated by AP-1 and to examine how it interacts with other inducible transcription factors, we abrogated its global DNA-binding activity using a dominant-negative FOS peptide. We show that FOS and JUN bind to and activate a specific set of vascular genes and that AP-1 inhibition shifts the balance between smooth muscle and hematopoietic differentiation towards blood. Furthermore, AP-1 is required for de novo binding of TEAD4, a transcription factor connected to Hippo signalling. Our bottom-up approach demonstrates that AP-1- and TEAD4-associated cis-regulatory elements form hubs for multiple signalling-responsive transcription factors and define the cistrome that regulates vascular and hematopoietic development by extrinsic signals.</description><identifier>ISSN: 0950-1991</identifier><identifier>EISSN: 1477-9129</identifier><identifier>DOI: 10.1242/dev.139857</identifier><identifier>PMID: 27802171</identifier><language>eng</language><publisher>England: The Company of Biologists Ltd</publisher><subject>Activating Transcription Factors - metabolism ; Animals ; Binding Sites - genetics ; Cell Differentiation - physiology ; Cell Line ; DNA-Binding Proteins - genetics ; DNA-Binding Proteins - metabolism ; Embryonic Stem Cells - cytology ; Gene Expression - genetics ; Gene Expression Profiling ; Mice ; Muscle Proteins - metabolism ; Muscle, Smooth, Vascular - cytology ; Muscle, Smooth, Vascular - metabolism ; Protein Binding ; Proto-Oncogene Proteins c-fos - metabolism ; Proto-Oncogene Proteins c-jun - metabolism ; Signal Transduction - physiology ; Stem Cells and Regeneration ; TEA Domain Transcription Factors ; Transcription Factor AP-1 - antagonists & inhibitors ; Transcription Factor AP-1 - metabolism ; Transcription Factors - metabolism</subject><ispartof>Development (Cambridge), 2016-12, Vol.143 (23), p.4324-4340</ispartof><rights>2016. 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Cauchy, Pierre ; Assi, Salam A ; Gilmour, Jane ; Lie-A-Ling, Michael ; Lichtinger, Monika ; Hoogenkamp, Maarten ; Noailles, Laura ; Cockerill, Peter N ; Lacaud, Georges ; Kouskoff, Valerie ; Bonifer, Constanze</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c477t-3fb267d689b8b851d80746f6ffa1f77b08fdfa4592d65b95ca2473dbdc09ff943</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Activating Transcription Factors - metabolism</topic><topic>Animals</topic><topic>Binding Sites - genetics</topic><topic>Cell Differentiation - physiology</topic><topic>Cell Line</topic><topic>DNA-Binding Proteins - genetics</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>Embryonic Stem Cells - cytology</topic><topic>Gene Expression - genetics</topic><topic>Gene Expression Profiling</topic><topic>Mice</topic><topic>Muscle Proteins - metabolism</topic><topic>Muscle, Smooth, Vascular - cytology</topic><topic>Muscle, Smooth, Vascular - metabolism</topic><topic>Protein Binding</topic><topic>Proto-Oncogene Proteins c-fos - metabolism</topic><topic>Proto-Oncogene Proteins c-jun - metabolism</topic><topic>Signal Transduction - physiology</topic><topic>Stem Cells and Regeneration</topic><topic>TEA Domain Transcription Factors</topic><topic>Transcription Factor AP-1 - antagonists & inhibitors</topic><topic>Transcription Factor AP-1 - metabolism</topic><topic>Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Obier, Nadine</creatorcontrib><creatorcontrib>Cauchy, Pierre</creatorcontrib><creatorcontrib>Assi, Salam A</creatorcontrib><creatorcontrib>Gilmour, Jane</creatorcontrib><creatorcontrib>Lie-A-Ling, Michael</creatorcontrib><creatorcontrib>Lichtinger, Monika</creatorcontrib><creatorcontrib>Hoogenkamp, Maarten</creatorcontrib><creatorcontrib>Noailles, Laura</creatorcontrib><creatorcontrib>Cockerill, Peter N</creatorcontrib><creatorcontrib>Lacaud, Georges</creatorcontrib><creatorcontrib>Kouskoff, Valerie</creatorcontrib><creatorcontrib>Bonifer, Constanze</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Development (Cambridge)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Obier, Nadine</au><au>Cauchy, Pierre</au><au>Assi, Salam A</au><au>Gilmour, Jane</au><au>Lie-A-Ling, Michael</au><au>Lichtinger, Monika</au><au>Hoogenkamp, Maarten</au><au>Noailles, Laura</au><au>Cockerill, Peter N</au><au>Lacaud, Georges</au><au>Kouskoff, Valerie</au><au>Bonifer, Constanze</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cooperative binding of AP-1 and TEAD4 modulates the balance between vascular smooth muscle and hemogenic cell fate</atitle><jtitle>Development (Cambridge)</jtitle><addtitle>Development</addtitle><date>2016-12-01</date><risdate>2016</risdate><volume>143</volume><issue>23</issue><spage>4324</spage><epage>4340</epage><pages>4324-4340</pages><issn>0950-1991</issn><eissn>1477-9129</eissn><abstract>The transmission of extracellular signals into the nucleus involves inducible transcription factors, but how different signalling pathways act in a cell type-specific fashion is poorly understood. 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subjects | Activating Transcription Factors - metabolism Animals Binding Sites - genetics Cell Differentiation - physiology Cell Line DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism Embryonic Stem Cells - cytology Gene Expression - genetics Gene Expression Profiling Mice Muscle Proteins - metabolism Muscle, Smooth, Vascular - cytology Muscle, Smooth, Vascular - metabolism Protein Binding Proto-Oncogene Proteins c-fos - metabolism Proto-Oncogene Proteins c-jun - metabolism Signal Transduction - physiology Stem Cells and Regeneration TEA Domain Transcription Factors Transcription Factor AP-1 - antagonists & inhibitors Transcription Factor AP-1 - metabolism Transcription Factors - metabolism |
title | Cooperative binding of AP-1 and TEAD4 modulates the balance between vascular smooth muscle and hemogenic cell fate |
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