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Bab2 Functions as an Ecdysone-Responsive Transcriptional Repressor during Drosophila Development
Drosophila development is governed by distinct ecdysone steroid pulses that initiate spatially and temporally defined gene expression programs. The translation of these signals into tissue-specific responses is crucial for metamorphosis, but the mechanisms that confer specificity to systemic ecdyson...
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Published in: | Cell reports (Cambridge) 2020-07, Vol.32 (4), p.107972-107972, Article 107972 |
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creator | Duan, Jianli Zhao, Yunpo Li, Haichao Habernig, Lukas Gordon, Michael D. Miao, Xuexia Engström, Ylva Büttner, Sabrina |
description | Drosophila development is governed by distinct ecdysone steroid pulses that initiate spatially and temporally defined gene expression programs. The translation of these signals into tissue-specific responses is crucial for metamorphosis, but the mechanisms that confer specificity to systemic ecdysone pulses are far from understood. Here, we identify Bric-à-brac 2 (Bab2) as an ecdysone-responsive transcriptional repressor that controls temporal gene expression during larval to pupal transition. Bab2 is necessary to terminate Salivary gland secretion (Sgs) gene expression, while premature Bab2 expression blocks Sgs genes and causes precocious salivary gland histolysis. The timely expression of bab2 is controlled by the ecdysone-responsive transcription factor Broad, and manipulation of EcR/USP/Broad signaling induces inappropriate Bab2 expression and termination of Sgs gene expression. Bab2 directly binds to Sgs loci in vitro and represses all Sgs genes in vivo. Our work characterizes Bab2 as a temporal regulator of somatic gene expression in response to systemic ecdysone signaling.
[Display omitted]
•Bab2 controls developmental stage-specific gene expression programs•Bab2 terminates gene expression downstream of EcR/USP and Broad in salivary glands•Bab2 directly binds to glue gene promoter sequences•High levels of Bab2 drive premature salivary gland degeneration
The steroid hormone ecdysone governs Drosophila development via initiation of spatially and temporally defined gene expression programs. Duan et al. establish Bab2 as an ecdysone-responsive suppressor of gene expression in Drosophila salivary glands, downstream of the early transcription factor Broad, following the larval-prepupal ecdysone pulse. |
doi_str_mv | 10.1016/j.celrep.2020.107972 |
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[Display omitted]
•Bab2 controls developmental stage-specific gene expression programs•Bab2 terminates gene expression downstream of EcR/USP and Broad in salivary glands•Bab2 directly binds to glue gene promoter sequences•High levels of Bab2 drive premature salivary gland degeneration
The steroid hormone ecdysone governs Drosophila development via initiation of spatially and temporally defined gene expression programs. Duan et al. establish Bab2 as an ecdysone-responsive suppressor of gene expression in Drosophila salivary glands, downstream of the early transcription factor Broad, following the larval-prepupal ecdysone pulse.</description><identifier>ISSN: 2211-1247</identifier><identifier>EISSN: 2211-1247</identifier><identifier>DOI: 10.1016/j.celrep.2020.107972</identifier><identifier>PMID: 32726635</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Bab2 ; Broad ; DNA-Binding Proteins - metabolism ; Drosophila ; Drosophila melanogaster - embryology ; Drosophila melanogaster - genetics ; Drosophila Proteins - genetics ; Drosophila Proteins - metabolism ; ecdysone ; Ecdysone - physiology ; EcR/USP ; Gene Expression Regulation, Developmental - genetics ; glue genes ; Larva - metabolism ; Metamorphosis, Biological - genetics ; salivary gland ; Sgs genes ; steroid hormone ; Transcription Factors - genetics ; Transcription Factors - metabolism ; Transcription, Genetic - genetics ; transcriptional regulation</subject><ispartof>Cell reports (Cambridge), 2020-07, Vol.32 (4), p.107972-107972, Article 107972</ispartof><rights>2020 The Author(s)</rights><rights>Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c511t-bbf94e719aaecbdb9014e4e82dd041f77696c207e67634c4a1f93c3050d6159b3</citedby><cites>FETCH-LOGICAL-c511t-bbf94e719aaecbdb9014e4e82dd041f77696c207e67634c4a1f93c3050d6159b3</cites><orcidid>0000-0002-7942-3406 ; 0000-0003-3244-0126 ; 0000-0002-1359-4640 ; 0000-0002-5440-986X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,777,781,882,27905,27906</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32726635$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-185457$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Duan, Jianli</creatorcontrib><creatorcontrib>Zhao, Yunpo</creatorcontrib><creatorcontrib>Li, Haichao</creatorcontrib><creatorcontrib>Habernig, Lukas</creatorcontrib><creatorcontrib>Gordon, Michael D.</creatorcontrib><creatorcontrib>Miao, Xuexia</creatorcontrib><creatorcontrib>Engström, Ylva</creatorcontrib><creatorcontrib>Büttner, Sabrina</creatorcontrib><title>Bab2 Functions as an Ecdysone-Responsive Transcriptional Repressor during Drosophila Development</title><title>Cell reports (Cambridge)</title><addtitle>Cell Rep</addtitle><description>Drosophila development is governed by distinct ecdysone steroid pulses that initiate spatially and temporally defined gene expression programs. The translation of these signals into tissue-specific responses is crucial for metamorphosis, but the mechanisms that confer specificity to systemic ecdysone pulses are far from understood. Here, we identify Bric-à-brac 2 (Bab2) as an ecdysone-responsive transcriptional repressor that controls temporal gene expression during larval to pupal transition. Bab2 is necessary to terminate Salivary gland secretion (Sgs) gene expression, while premature Bab2 expression blocks Sgs genes and causes precocious salivary gland histolysis. The timely expression of bab2 is controlled by the ecdysone-responsive transcription factor Broad, and manipulation of EcR/USP/Broad signaling induces inappropriate Bab2 expression and termination of Sgs gene expression. Bab2 directly binds to Sgs loci in vitro and represses all Sgs genes in vivo. Our work characterizes Bab2 as a temporal regulator of somatic gene expression in response to systemic ecdysone signaling.
[Display omitted]
•Bab2 controls developmental stage-specific gene expression programs•Bab2 terminates gene expression downstream of EcR/USP and Broad in salivary glands•Bab2 directly binds to glue gene promoter sequences•High levels of Bab2 drive premature salivary gland degeneration
The steroid hormone ecdysone governs Drosophila development via initiation of spatially and temporally defined gene expression programs. Duan et al. establish Bab2 as an ecdysone-responsive suppressor of gene expression in Drosophila salivary glands, downstream of the early transcription factor Broad, following the larval-prepupal ecdysone pulse.</description><subject>Animals</subject><subject>Bab2</subject><subject>Broad</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>Drosophila</subject><subject>Drosophila melanogaster - embryology</subject><subject>Drosophila melanogaster - genetics</subject><subject>Drosophila Proteins - genetics</subject><subject>Drosophila Proteins - metabolism</subject><subject>ecdysone</subject><subject>Ecdysone - physiology</subject><subject>EcR/USP</subject><subject>Gene Expression Regulation, Developmental - genetics</subject><subject>glue genes</subject><subject>Larva - metabolism</subject><subject>Metamorphosis, Biological - genetics</subject><subject>salivary gland</subject><subject>Sgs genes</subject><subject>steroid hormone</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><subject>Transcription, Genetic - genetics</subject><subject>transcriptional regulation</subject><issn>2211-1247</issn><issn>2211-1247</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNp9kV1rFDEUhgdRbKn9ByJz6YWz5mTysbkRarfVQkEo1duYjzM1y-xkTGZW-u_NdmrRG0Mgh5fnvCect6peA1kBAfF-u3LYJxxXlNCDJJWkz6pjSgEaoEw-_6s-qk5z3pJyBAFQ7GV11FJJhWj5cfX9o7G0vpwHN4U45NqUO9QXzt_nOGBzg3kscthjfZvMkF0K4wE0fX2DY8KcY6r9nMJwV29SzHH8EXpTb3CPfRx3OEyvqhed6TOePr4n1dfLi9vzz831l09X52fXjeMAU2NtpxhKUMags94qAgwZrqn3hEEnpVDCUSJRSNEyxwx0qnUt4cQL4Mq2J9XV4uuj2eoxhZ1J9zqaoB-EmO60SVNwPWouiQRjBVFMMpDGAONdRxSuybqIWLzeLV75F46z_cdtE76dPbjlWcOaMy4L_nbBxxR_zpgnvQu55NObAeOcNWVUEc7LNwvKFtSVZeWE3ZM3EH1IVm_1kqw-JKuXZEvbm8cJs92hf2r6k2MBPiwAlhXvAyadXcDBoQ8J3VR2EP4_4TeJPLWq</recordid><startdate>20200728</startdate><enddate>20200728</enddate><creator>Duan, Jianli</creator><creator>Zhao, Yunpo</creator><creator>Li, Haichao</creator><creator>Habernig, Lukas</creator><creator>Gordon, Michael D.</creator><creator>Miao, Xuexia</creator><creator>Engström, Ylva</creator><creator>Büttner, Sabrina</creator><general>Elsevier Inc</general><general>Elsevier</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>ABAVF</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>D8T</scope><scope>DG7</scope><scope>ZZAVC</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-7942-3406</orcidid><orcidid>https://orcid.org/0000-0003-3244-0126</orcidid><orcidid>https://orcid.org/0000-0002-1359-4640</orcidid><orcidid>https://orcid.org/0000-0002-5440-986X</orcidid></search><sort><creationdate>20200728</creationdate><title>Bab2 Functions as an Ecdysone-Responsive Transcriptional Repressor during Drosophila Development</title><author>Duan, Jianli ; Zhao, Yunpo ; Li, Haichao ; Habernig, Lukas ; Gordon, Michael D. ; Miao, Xuexia ; Engström, Ylva ; Büttner, Sabrina</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c511t-bbf94e719aaecbdb9014e4e82dd041f77696c207e67634c4a1f93c3050d6159b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>Bab2</topic><topic>Broad</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>Drosophila</topic><topic>Drosophila melanogaster - embryology</topic><topic>Drosophila melanogaster - genetics</topic><topic>Drosophila Proteins - genetics</topic><topic>Drosophila Proteins - metabolism</topic><topic>ecdysone</topic><topic>Ecdysone - physiology</topic><topic>EcR/USP</topic><topic>Gene Expression Regulation, Developmental - genetics</topic><topic>glue genes</topic><topic>Larva - metabolism</topic><topic>Metamorphosis, Biological - genetics</topic><topic>salivary gland</topic><topic>Sgs genes</topic><topic>steroid hormone</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><topic>Transcription, Genetic - genetics</topic><topic>transcriptional regulation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Duan, Jianli</creatorcontrib><creatorcontrib>Zhao, Yunpo</creatorcontrib><creatorcontrib>Li, Haichao</creatorcontrib><creatorcontrib>Habernig, Lukas</creatorcontrib><creatorcontrib>Gordon, Michael D.</creatorcontrib><creatorcontrib>Miao, Xuexia</creatorcontrib><creatorcontrib>Engström, Ylva</creatorcontrib><creatorcontrib>Büttner, Sabrina</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><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>SWEPUB Stockholms universitet full text</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Freely available online</collection><collection>SWEPUB Stockholms universitet</collection><collection>SwePub Articles full text</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Cell reports (Cambridge)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Duan, Jianli</au><au>Zhao, Yunpo</au><au>Li, Haichao</au><au>Habernig, Lukas</au><au>Gordon, Michael D.</au><au>Miao, Xuexia</au><au>Engström, Ylva</au><au>Büttner, Sabrina</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Bab2 Functions as an Ecdysone-Responsive Transcriptional Repressor during Drosophila Development</atitle><jtitle>Cell reports (Cambridge)</jtitle><addtitle>Cell Rep</addtitle><date>2020-07-28</date><risdate>2020</risdate><volume>32</volume><issue>4</issue><spage>107972</spage><epage>107972</epage><pages>107972-107972</pages><artnum>107972</artnum><issn>2211-1247</issn><eissn>2211-1247</eissn><abstract>Drosophila development is governed by distinct ecdysone steroid pulses that initiate spatially and temporally defined gene expression programs. The translation of these signals into tissue-specific responses is crucial for metamorphosis, but the mechanisms that confer specificity to systemic ecdysone pulses are far from understood. Here, we identify Bric-à-brac 2 (Bab2) as an ecdysone-responsive transcriptional repressor that controls temporal gene expression during larval to pupal transition. Bab2 is necessary to terminate Salivary gland secretion (Sgs) gene expression, while premature Bab2 expression blocks Sgs genes and causes precocious salivary gland histolysis. The timely expression of bab2 is controlled by the ecdysone-responsive transcription factor Broad, and manipulation of EcR/USP/Broad signaling induces inappropriate Bab2 expression and termination of Sgs gene expression. Bab2 directly binds to Sgs loci in vitro and represses all Sgs genes in vivo. Our work characterizes Bab2 as a temporal regulator of somatic gene expression in response to systemic ecdysone signaling.
[Display omitted]
•Bab2 controls developmental stage-specific gene expression programs•Bab2 terminates gene expression downstream of EcR/USP and Broad in salivary glands•Bab2 directly binds to glue gene promoter sequences•High levels of Bab2 drive premature salivary gland degeneration
The steroid hormone ecdysone governs Drosophila development via initiation of spatially and temporally defined gene expression programs. Duan et al. establish Bab2 as an ecdysone-responsive suppressor of gene expression in Drosophila salivary glands, downstream of the early transcription factor Broad, following the larval-prepupal ecdysone pulse.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>32726635</pmid><doi>10.1016/j.celrep.2020.107972</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-7942-3406</orcidid><orcidid>https://orcid.org/0000-0003-3244-0126</orcidid><orcidid>https://orcid.org/0000-0002-1359-4640</orcidid><orcidid>https://orcid.org/0000-0002-5440-986X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Bab2 Broad DNA-Binding Proteins - metabolism Drosophila Drosophila melanogaster - embryology Drosophila melanogaster - genetics Drosophila Proteins - genetics Drosophila Proteins - metabolism ecdysone Ecdysone - physiology EcR/USP Gene Expression Regulation, Developmental - genetics glue genes Larva - metabolism Metamorphosis, Biological - genetics salivary gland Sgs genes steroid hormone Transcription Factors - genetics Transcription Factors - metabolism Transcription, Genetic - genetics transcriptional regulation |
title | Bab2 Functions as an Ecdysone-Responsive Transcriptional Repressor during Drosophila Development |
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