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Article: Collaborative regulation of development but independent control of metabolism by two epidermis-specific transcription factors in Caenorhabditis elegans

TitleCollaborative regulation of development but independent control of metabolism by two epidermis-specific transcription factors in Caenorhabditis elegans
Authors
KeywordsC. elegans
Cell Differentiation
Chromatin Immunoprecipitation (ChIP)
Epithelium
Gene Expression
Issue Date2013
PublisherAmerican Society for Biochemistry and Molecular Biology, Inc. The Journal's web site is located at http://www.jbc.org/
Citation
Journal of Biological Chemistry, 2013, v. 288 n. 46, p. 33411-33426 How to Cite?
AbstractCell fate specification is typically initiated by a master regulator, which is relayed by tissue-specific regulatory proteins (usually transcription factors) for further enforcement of cell identities, but how the factors are coordinated among each other to 'finish up' the specification remains poorly understood. Caenorhabditis elegans epidermis specification is initiated by a master regulator, ELT-1, that activates its targets, NHR-25 and ELT-3, two epidermis-specific transcription factors that are important for development but not for initial specification of epidermis, thus providing a unique paradigm for illustrating how the tissue-specific regulatory proteins work together to enforce cell fate specification. Here we addressed the question through contrasting genome-wide in vivo binding targets between NHR-25 and ELT-3. We demonstrate that the two factors bind discrete but conserved DNA motifs, most of which remain in proximity, suggesting formation of a complex between the two. In agreement with this, gene ontology analysis of putative target genes suggested differential regulation of metabolism but coordinated control of epidermal development between the two factors, which is supported by quantitative analysis of expression of their specific or common targets in the presence or absence of either protein. Functional validation of a subset of the target genes showed both activating and inhibitory roles of NHR-25 and ELT-3 in regulating their targets. We further demonstrated differential control of specification of AB and C lineage-derived epidermis. The results allow us to assemble a comprehensive gene network underlying C. elegans epidermis development that is likely to be widely used across species and provides insights into how tissue-specific transcription factors coordinate with one another to enforce cell fate specification initiated by its master regulator.
Persistent Identifierhttp://hdl.handle.net/10722/210600
ISSN
2015 Impact Factor: 4.258
2015 SCImago Journal Rankings: 3.151
PubMed Central ID

 

DC FieldValueLanguage
dc.contributor.authorShao, J-
dc.contributor.authorHe, K-
dc.contributor.authorWang, H-
dc.contributor.authorHo, WS-
dc.contributor.authorRen, X-
dc.contributor.authorAn, X-
dc.contributor.authorWong, MK-
dc.contributor.authorYan, B-
dc.contributor.authorXie, D-
dc.contributor.authorStamatoyannopoulos, J-
dc.contributor.authorZhao, Z-
dc.date.accessioned2015-06-19T04:31:49Z-
dc.date.available2015-06-19T04:31:49Z-
dc.date.issued2013-
dc.identifier.citationJournal of Biological Chemistry, 2013, v. 288 n. 46, p. 33411-33426-
dc.identifier.issn0021-9258-
dc.identifier.urihttp://hdl.handle.net/10722/210600-
dc.description.abstractCell fate specification is typically initiated by a master regulator, which is relayed by tissue-specific regulatory proteins (usually transcription factors) for further enforcement of cell identities, but how the factors are coordinated among each other to 'finish up' the specification remains poorly understood. Caenorhabditis elegans epidermis specification is initiated by a master regulator, ELT-1, that activates its targets, NHR-25 and ELT-3, two epidermis-specific transcription factors that are important for development but not for initial specification of epidermis, thus providing a unique paradigm for illustrating how the tissue-specific regulatory proteins work together to enforce cell fate specification. Here we addressed the question through contrasting genome-wide in vivo binding targets between NHR-25 and ELT-3. We demonstrate that the two factors bind discrete but conserved DNA motifs, most of which remain in proximity, suggesting formation of a complex between the two. In agreement with this, gene ontology analysis of putative target genes suggested differential regulation of metabolism but coordinated control of epidermal development between the two factors, which is supported by quantitative analysis of expression of their specific or common targets in the presence or absence of either protein. Functional validation of a subset of the target genes showed both activating and inhibitory roles of NHR-25 and ELT-3 in regulating their targets. We further demonstrated differential control of specification of AB and C lineage-derived epidermis. The results allow us to assemble a comprehensive gene network underlying C. elegans epidermis development that is likely to be widely used across species and provides insights into how tissue-specific transcription factors coordinate with one another to enforce cell fate specification initiated by its master regulator.-
dc.languageeng-
dc.publisherAmerican Society for Biochemistry and Molecular Biology, Inc. The Journal's web site is located at http://www.jbc.org/-
dc.relation.ispartofJournal of Biological Chemistry-
dc.rightsJournal of Biological Chemistry. Copyright © American Society for Biochemistry and Molecular Biology, Inc.-
dc.rightsThis research was originally published in [Journal Name]. Author(s). Title. Journal Name. Year. Vol:pp-pp. © the American Society for Biochemistry and Molecular Biology-
dc.subjectC. elegans-
dc.subjectCell Differentiation-
dc.subjectChromatin Immunoprecipitation (ChIP)-
dc.subjectEpithelium-
dc.subjectGene Expression-
dc.titleCollaborative regulation of development but independent control of metabolism by two epidermis-specific transcription factors in Caenorhabditis elegans-
dc.typeArticle-
dc.description.naturelink_to_OA_fulltext-
dc.identifier.doi10.1074/jbc.M113.487975-
dc.identifier.pmid24097988-
dc.identifier.pmcidPMC3829187-
dc.identifier.volume288-
dc.identifier.issue46-
dc.identifier.spage33411-
dc.identifier.epage33426-
dc.publisher.placeUnited States-

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