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Expression and estrogen-dependent regulation of the zebrafish brain aromatase gene
Compared with adult mammals, the brain of teleost fish is characterized by an extremely high capacity to aromatize androgens into estrogens, and this metabolic activity results from the expression of a specific brain aromatase (AroB) generated by the cyp19b gene. In this study, we first generated an...
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Published in: | Journal of comparative neurology (1911) 2005-05, Vol.485 (4), p.304-320 |
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container_title | Journal of comparative neurology (1911) |
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creator | Menuet, Arnaud Pellegrini, Elisabeth Brion, François Gueguen, Marie-Madeleine Anglade, Isabelle Pakdel, Farzad Kah, Olivier |
description | Compared with adult mammals, the brain of teleost fish is characterized by an extremely high capacity to aromatize androgens into estrogens, and this metabolic activity results from the expression of a specific brain aromatase (AroB) generated by the cyp19b gene. In this study, we first generated antibodies to zebrafish AroB and used them to map AroB‐positive structures in the brain of adult zebrafish. We show that AroB is exclusively expressed in radial glial cells, mainly in the olfactory bulbs, telencephalon, preoptic area, and hypothalamus. Second, we investigated in vivo and in vitro the mechanisms involved in the estradiol (E2) regulation of the cyp19b gene. By means of whole‐mount hybridization and immunohistochemistry on zebrafish embryos and larvae, we confirmed the E2‐dependent upregulation of the cyp19b gene, and we show that E2 triggers AroB expression in radial glial cells mainly in the preoptic area and mediobasal hypothalamus of 48 hpf (hours post fertilization) and 108 hpf larvae. In addition, an in vitro analysis of 0.5 kb of the promoter region of the cyp19b gene demonstrated that this E2‐dependent regulation involves a direct transcriptional action of estrogen receptors requiring estrogen‐responsive elements. However, the data obtained on different cell lines demonstrate that a glial cell context is necessary for full E2 induction. The correlation between our in vivo and in vitro data suggests that the E2‐dependent upregulation of AroB is favored by a glial cell context. J. Comp. Neurol. 485:304–320, 2005. © 2005 Wiley‐Liss, Inc. |
doi_str_mv | 10.1002/cne.20497 |
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In this study, we first generated antibodies to zebrafish AroB and used them to map AroB‐positive structures in the brain of adult zebrafish. We show that AroB is exclusively expressed in radial glial cells, mainly in the olfactory bulbs, telencephalon, preoptic area, and hypothalamus. Second, we investigated in vivo and in vitro the mechanisms involved in the estradiol (E2) regulation of the cyp19b gene. By means of whole‐mount hybridization and immunohistochemistry on zebrafish embryos and larvae, we confirmed the E2‐dependent upregulation of the cyp19b gene, and we show that E2 triggers AroB expression in radial glial cells mainly in the preoptic area and mediobasal hypothalamus of 48 hpf (hours post fertilization) and 108 hpf larvae. In addition, an in vitro analysis of 0.5 kb of the promoter region of the cyp19b gene demonstrated that this E2‐dependent regulation involves a direct transcriptional action of estrogen receptors requiring estrogen‐responsive elements. However, the data obtained on different cell lines demonstrate that a glial cell context is necessary for full E2 induction. The correlation between our in vivo and in vitro data suggests that the E2‐dependent upregulation of AroB is favored by a glial cell context. J. Comp. Neurol. 485:304–320, 2005. © 2005 Wiley‐Liss, Inc.</description><identifier>ISSN: 0021-9967</identifier><identifier>EISSN: 1096-9861</identifier><identifier>DOI: 10.1002/cne.20497</identifier><identifier>PMID: 15803511</identifier><language>eng</language><publisher>Hoboken: Wiley Subscription Services, Inc., A Wiley Company</publisher><subject>Animals ; Aromatase ; Aromatase - biosynthesis ; Aromatase - genetics ; Biochemistry, Molecular Biology ; Brain ; Brain - drug effects ; Brain - embryology ; Brain - enzymology ; Cell Line ; Cricetinae ; Dose-Response Relationship, Drug ; Estradiol ; Estradiol - analogs & derivatives ; Estradiol - pharmacology ; estrogen receptor ; Estrogens ; Estrogens - pharmacology ; Female ; Gene Expression Regulation, Enzymologic ; Gene Expression Regulation, Enzymologic - drug effects ; Gene Expression Regulation, Enzymologic - physiology ; Humans ; Life Sciences ; Male ; Mice ; Molecular biology ; radial glia ; Rats ; Reproductive Biology ; teleost fish ; Zebrafish ; Zebrafish - embryology ; Zebrafish - genetics ; Zebrafish - metabolism</subject><ispartof>Journal of comparative neurology (1911), 2005-05, Vol.485 (4), p.304-320</ispartof><rights>Copyright © 2005 Wiley‐Liss, Inc.</rights><rights>(c) 2005 Wiley-Liss, Inc.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4267-47443988c4211ef4b27c5ca41c5660c389b12bd915c12b4907c4a835be7ba02f3</citedby><cites>FETCH-LOGICAL-c4267-47443988c4211ef4b27c5ca41c5660c389b12bd915c12b4907c4a835be7ba02f3</cites><orcidid>0000-0003-4821-0966 ; 0000-0003-2341-4196 ; 0000-0002-3067-3156</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/15803511$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-00294769$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Menuet, Arnaud</creatorcontrib><creatorcontrib>Pellegrini, Elisabeth</creatorcontrib><creatorcontrib>Brion, François</creatorcontrib><creatorcontrib>Gueguen, Marie-Madeleine</creatorcontrib><creatorcontrib>Anglade, Isabelle</creatorcontrib><creatorcontrib>Pakdel, Farzad</creatorcontrib><creatorcontrib>Kah, Olivier</creatorcontrib><title>Expression and estrogen-dependent regulation of the zebrafish brain aromatase gene</title><title>Journal of comparative neurology (1911)</title><addtitle>J. Comp. Neurol</addtitle><description>Compared with adult mammals, the brain of teleost fish is characterized by an extremely high capacity to aromatize androgens into estrogens, and this metabolic activity results from the expression of a specific brain aromatase (AroB) generated by the cyp19b gene. In this study, we first generated antibodies to zebrafish AroB and used them to map AroB‐positive structures in the brain of adult zebrafish. We show that AroB is exclusively expressed in radial glial cells, mainly in the olfactory bulbs, telencephalon, preoptic area, and hypothalamus. Second, we investigated in vivo and in vitro the mechanisms involved in the estradiol (E2) regulation of the cyp19b gene. By means of whole‐mount hybridization and immunohistochemistry on zebrafish embryos and larvae, we confirmed the E2‐dependent upregulation of the cyp19b gene, and we show that E2 triggers AroB expression in radial glial cells mainly in the preoptic area and mediobasal hypothalamus of 48 hpf (hours post fertilization) and 108 hpf larvae. In addition, an in vitro analysis of 0.5 kb of the promoter region of the cyp19b gene demonstrated that this E2‐dependent regulation involves a direct transcriptional action of estrogen receptors requiring estrogen‐responsive elements. However, the data obtained on different cell lines demonstrate that a glial cell context is necessary for full E2 induction. The correlation between our in vivo and in vitro data suggests that the E2‐dependent upregulation of AroB is favored by a glial cell context. J. Comp. Neurol. 485:304–320, 2005. © 2005 Wiley‐Liss, Inc.</description><subject>Animals</subject><subject>Aromatase</subject><subject>Aromatase - biosynthesis</subject><subject>Aromatase - genetics</subject><subject>Biochemistry, Molecular Biology</subject><subject>Brain</subject><subject>Brain - drug effects</subject><subject>Brain - embryology</subject><subject>Brain - enzymology</subject><subject>Cell Line</subject><subject>Cricetinae</subject><subject>Dose-Response Relationship, Drug</subject><subject>Estradiol</subject><subject>Estradiol - analogs & derivatives</subject><subject>Estradiol - pharmacology</subject><subject>estrogen receptor</subject><subject>Estrogens</subject><subject>Estrogens - pharmacology</subject><subject>Female</subject><subject>Gene Expression Regulation, Enzymologic</subject><subject>Gene Expression Regulation, Enzymologic - drug effects</subject><subject>Gene Expression Regulation, Enzymologic - physiology</subject><subject>Humans</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Mice</subject><subject>Molecular biology</subject><subject>radial glia</subject><subject>Rats</subject><subject>Reproductive Biology</subject><subject>teleost fish</subject><subject>Zebrafish</subject><subject>Zebrafish - embryology</subject><subject>Zebrafish - genetics</subject><subject>Zebrafish - metabolism</subject><issn>0021-9967</issn><issn>1096-9861</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2005</creationdate><recordtype>article</recordtype><recordid>eNqFkU9P4zAQxS3ECkp3D3wBlBPSHgKe-F98RFWhSFUXIVZ7tBxnQgNpUuyUBT49Li1wQpxGY__eG48fIYdAT4DS7NS1eJJRrtUOGQDVMtW5hF0yiHeQai3VPjkI4Y5SqjXL98g-iJwyATAg1-OnpccQ6q5NbFsmGHrf3WKblrjEtsS2Tzzerhrbr4muSvo5Ji9YeFvVYZ7EWkeh7xa2twGTqMSf5Edlm4C_tnVI_p6Pb0aTdPrn4nJ0Nk0dz6RKueKc6TyPHQBWvMiUE85ycEJK6liuC8iKUoNwsXJNleM2Z6JAVViaVWxIfm9857YxS18vrH82na3N5Gxq1mdxfc2V1I8Q2eMNu_TdwyouaRZ1cNg0tsVuFYxUChhI9i0IimXxz_PP6c53IXisPp4A1KxTMTEV85ZKZI-2pqtigeUnuY0hAqcb4H_d4PPXTmY0G79bphtFHXp8-lBYfx93YUqYf7MLI5i8GolJbNgrx3qjzw</recordid><startdate>20050516</startdate><enddate>20050516</enddate><creator>Menuet, Arnaud</creator><creator>Pellegrini, Elisabeth</creator><creator>Brion, François</creator><creator>Gueguen, Marie-Madeleine</creator><creator>Anglade, Isabelle</creator><creator>Pakdel, Farzad</creator><creator>Kah, Olivier</creator><general>Wiley Subscription Services, Inc., A Wiley Company</general><general>Wiley</general><scope>BSCLL</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>7TK</scope><scope>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0003-4821-0966</orcidid><orcidid>https://orcid.org/0000-0003-2341-4196</orcidid><orcidid>https://orcid.org/0000-0002-3067-3156</orcidid></search><sort><creationdate>20050516</creationdate><title>Expression and estrogen-dependent regulation of the zebrafish brain aromatase gene</title><author>Menuet, Arnaud ; Pellegrini, Elisabeth ; Brion, François ; Gueguen, Marie-Madeleine ; Anglade, Isabelle ; Pakdel, Farzad ; Kah, Olivier</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4267-47443988c4211ef4b27c5ca41c5660c389b12bd915c12b4907c4a835be7ba02f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2005</creationdate><topic>Animals</topic><topic>Aromatase</topic><topic>Aromatase - biosynthesis</topic><topic>Aromatase - genetics</topic><topic>Biochemistry, Molecular Biology</topic><topic>Brain</topic><topic>Brain - drug effects</topic><topic>Brain - embryology</topic><topic>Brain - enzymology</topic><topic>Cell Line</topic><topic>Cricetinae</topic><topic>Dose-Response Relationship, Drug</topic><topic>Estradiol</topic><topic>Estradiol - analogs & derivatives</topic><topic>Estradiol - pharmacology</topic><topic>estrogen receptor</topic><topic>Estrogens</topic><topic>Estrogens - pharmacology</topic><topic>Female</topic><topic>Gene Expression Regulation, Enzymologic</topic><topic>Gene Expression Regulation, Enzymologic - drug effects</topic><topic>Gene Expression Regulation, Enzymologic - physiology</topic><topic>Humans</topic><topic>Life Sciences</topic><topic>Male</topic><topic>Mice</topic><topic>Molecular biology</topic><topic>radial glia</topic><topic>Rats</topic><topic>Reproductive Biology</topic><topic>teleost fish</topic><topic>Zebrafish</topic><topic>Zebrafish - embryology</topic><topic>Zebrafish - genetics</topic><topic>Zebrafish - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Menuet, Arnaud</creatorcontrib><creatorcontrib>Pellegrini, Elisabeth</creatorcontrib><creatorcontrib>Brion, François</creatorcontrib><creatorcontrib>Gueguen, Marie-Madeleine</creatorcontrib><creatorcontrib>Anglade, Isabelle</creatorcontrib><creatorcontrib>Pakdel, Farzad</creatorcontrib><creatorcontrib>Kah, Olivier</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Journal of comparative neurology (1911)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Menuet, Arnaud</au><au>Pellegrini, Elisabeth</au><au>Brion, François</au><au>Gueguen, Marie-Madeleine</au><au>Anglade, Isabelle</au><au>Pakdel, Farzad</au><au>Kah, Olivier</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Expression and estrogen-dependent regulation of the zebrafish brain aromatase gene</atitle><jtitle>Journal of comparative neurology (1911)</jtitle><addtitle>J. Comp. Neurol</addtitle><date>2005-05-16</date><risdate>2005</risdate><volume>485</volume><issue>4</issue><spage>304</spage><epage>320</epage><pages>304-320</pages><issn>0021-9967</issn><eissn>1096-9861</eissn><abstract>Compared with adult mammals, the brain of teleost fish is characterized by an extremely high capacity to aromatize androgens into estrogens, and this metabolic activity results from the expression of a specific brain aromatase (AroB) generated by the cyp19b gene. In this study, we first generated antibodies to zebrafish AroB and used them to map AroB‐positive structures in the brain of adult zebrafish. We show that AroB is exclusively expressed in radial glial cells, mainly in the olfactory bulbs, telencephalon, preoptic area, and hypothalamus. Second, we investigated in vivo and in vitro the mechanisms involved in the estradiol (E2) regulation of the cyp19b gene. By means of whole‐mount hybridization and immunohistochemistry on zebrafish embryos and larvae, we confirmed the E2‐dependent upregulation of the cyp19b gene, and we show that E2 triggers AroB expression in radial glial cells mainly in the preoptic area and mediobasal hypothalamus of 48 hpf (hours post fertilization) and 108 hpf larvae. In addition, an in vitro analysis of 0.5 kb of the promoter region of the cyp19b gene demonstrated that this E2‐dependent regulation involves a direct transcriptional action of estrogen receptors requiring estrogen‐responsive elements. However, the data obtained on different cell lines demonstrate that a glial cell context is necessary for full E2 induction. The correlation between our in vivo and in vitro data suggests that the E2‐dependent upregulation of AroB is favored by a glial cell context. J. Comp. 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subjects | Animals Aromatase Aromatase - biosynthesis Aromatase - genetics Biochemistry, Molecular Biology Brain Brain - drug effects Brain - embryology Brain - enzymology Cell Line Cricetinae Dose-Response Relationship, Drug Estradiol Estradiol - analogs & derivatives Estradiol - pharmacology estrogen receptor Estrogens Estrogens - pharmacology Female Gene Expression Regulation, Enzymologic Gene Expression Regulation, Enzymologic - drug effects Gene Expression Regulation, Enzymologic - physiology Humans Life Sciences Male Mice Molecular biology radial glia Rats Reproductive Biology teleost fish Zebrafish Zebrafish - embryology Zebrafish - genetics Zebrafish - metabolism |
title | Expression and estrogen-dependent regulation of the zebrafish brain aromatase gene |
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