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Involvement of estrogens in the process of sex differentiation in two fish species: the rainbow trout (Oncorhynchus mykiss) and a tilapia (Oreochromis niloticus)
In order to study the physiological implication of sex steroid hormones in gonadal sex differentiation in fish, we first investigated the potential role of estrogens using two fish models: the rainbow trout (Oncorhynchus mykiss) and a tilapia species (Oreochromis niloticus). All experiments were car...
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Published in: | Molecular reproduction and development 1999-10, Vol.54 (2), p.154-162 |
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description | In order to study the physiological implication of sex steroid hormones in gonadal sex differentiation in fish, we first investigated the potential role of estrogens using two fish models: the rainbow trout (Oncorhynchus mykiss) and a tilapia species (Oreochromis niloticus). All experiments were carried out on genetically all‐male (XY) and all‐female (XX) populations. In vivo treatments with an aromatase inhibitor (ATD, 1,4,6‐ androstatriene‐3–17‐dione) result in 100% masculinization of an all‐female population in rainbow trout (dosage 50 mg/kg of food) and 75.3% in tilapia (dosage 150 mg/kg of food). In tilapia, the effectiveness of the aromatase inhibition by ATD is demonstrated by the marked decrease of the gonadal aromatase activity in treated animals versus control. No masculinization is obtained following treatment with an estrogen receptor antagonist (tamoxifen) in both species. Aromatase and estrogen receptor gene expression was studied in rainbow trout by semi‐quantitative RT‐PCR in gonads sampled before, during and after sex‐differentiation. Aromatase mRNA is specifically detected in female gonads, 3 weeks before the first sign of histological sex‐differentiation, i.e., first female meiosis. Aromatase expression in male gonads is at least a few hundred times less than in female gonads. Estrogen receptor gene is expressed in both male and female gonads at all stages with no dimorphic expression between sexes. Specific aromatase gene expression before ovarian differentiation was also demonstrated using virtual Northern blot, with no expression detected in male differentiating gonads. From these results it can be concluded that estrogen synthesis is crucial for ovarian differentiation, and transcription of the aromatase gene can be proposed as a key step in that process in fish. Mol. Reprod. Dev. 54:154–162, 1999. © 1999 Wiley‐Liss, Inc. |
doi_str_mv | 10.1002/(SICI)1098-2795(199910)54:2<154::AID-MRD7>3.0.CO;2-5 |
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All experiments were carried out on genetically all‐male (XY) and all‐female (XX) populations. In vivo treatments with an aromatase inhibitor (ATD, 1,4,6‐ androstatriene‐3–17‐dione) result in 100% masculinization of an all‐female population in rainbow trout (dosage 50 mg/kg of food) and 75.3% in tilapia (dosage 150 mg/kg of food). In tilapia, the effectiveness of the aromatase inhibition by ATD is demonstrated by the marked decrease of the gonadal aromatase activity in treated animals versus control. No masculinization is obtained following treatment with an estrogen receptor antagonist (tamoxifen) in both species. Aromatase and estrogen receptor gene expression was studied in rainbow trout by semi‐quantitative RT‐PCR in gonads sampled before, during and after sex‐differentiation. Aromatase mRNA is specifically detected in female gonads, 3 weeks before the first sign of histological sex‐differentiation, i.e., first female meiosis. Aromatase expression in male gonads is at least a few hundred times less than in female gonads. Estrogen receptor gene is expressed in both male and female gonads at all stages with no dimorphic expression between sexes. Specific aromatase gene expression before ovarian differentiation was also demonstrated using virtual Northern blot, with no expression detected in male differentiating gonads. From these results it can be concluded that estrogen synthesis is crucial for ovarian differentiation, and transcription of the aromatase gene can be proposed as a key step in that process in fish. Mol. Reprod. Dev. 54:154–162, 1999. © 1999 Wiley‐Liss, Inc.</description><identifier>ISSN: 1040-452X</identifier><identifier>EISSN: 1098-2795</identifier><identifier>DOI: 10.1002/(SICI)1098-2795(199910)54:2<154::AID-MRD7>3.0.CO;2-5</identifier><identifier>PMID: 10471475</identifier><identifier>CODEN: MREDEE</identifier><language>eng</language><publisher>New York: John Wiley & Sons, Inc</publisher><subject>Animals ; aromatase ; Aromatase - drug effects ; Aromatase - genetics ; Aromatase - metabolism ; Biological and medical sciences ; Blotting, Northern ; Cell differentiation, maturation, development, hematopoiesis ; Cell physiology ; DNA, Complementary - analysis ; Dose-Response Relationship, Drug ; Egg Proteins - pharmacology ; enzyme inhibitors ; estrogen receptor ; estrogen receptors ; estrogens ; Estrogens - physiology ; Female ; fish ; Fundamental and applied biological sciences. Psychology ; Gene Expression ; gonads ; Gonads - anatomy & histology ; Gonads - drug effects ; Life Sciences ; Male ; masculinizing effect ; Molecular and cellular biology ; Oncorhynchus mykiss ; Oncorhynchus mykiss - physiology ; Ovary - anatomy & histology ; Receptors, Estrogen - physiology ; Reproductive Biology ; Reverse Transcriptase Polymerase Chain Reaction ; Sequence Analysis, DNA ; sex differentiation ; Sex Differentiation - drug effects ; Sex Differentiation - physiology ; sexual development ; steroids ; Tamoxifen - pharmacology ; tilapia (common name) ; Tilapia - physiology</subject><ispartof>Molecular reproduction and development, 1999-10, Vol.54 (2), p.154-162</ispartof><rights>Copyright © 1999 Wiley‐Liss, Inc.</rights><rights>1999 INIST-CNRS</rights><rights>Copyright 1999 Wiley-Liss, Inc.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c4677-81fe1dc6670665d87286374f74b13ca7279978388dc5a037e12988feef457e943</cites><orcidid>0000-0001-5464-6219</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=1985975$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/10471475$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-02697875$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Guiguen, Y</creatorcontrib><creatorcontrib>Baroiller, J.F</creatorcontrib><creatorcontrib>Ricordel, M.J</creatorcontrib><creatorcontrib>Iseki, K</creatorcontrib><creatorcontrib>McMeel, O.M</creatorcontrib><creatorcontrib>Martin, S.A.M</creatorcontrib><creatorcontrib>Fostier, A</creatorcontrib><title>Involvement of estrogens in the process of sex differentiation in two fish species: the rainbow trout (Oncorhynchus mykiss) and a tilapia (Oreochromis niloticus)</title><title>Molecular reproduction and development</title><addtitle>Mol. Reprod. Dev</addtitle><description>In order to study the physiological implication of sex steroid hormones in gonadal sex differentiation in fish, we first investigated the potential role of estrogens using two fish models: the rainbow trout (Oncorhynchus mykiss) and a tilapia species (Oreochromis niloticus). All experiments were carried out on genetically all‐male (XY) and all‐female (XX) populations. In vivo treatments with an aromatase inhibitor (ATD, 1,4,6‐ androstatriene‐3–17‐dione) result in 100% masculinization of an all‐female population in rainbow trout (dosage 50 mg/kg of food) and 75.3% in tilapia (dosage 150 mg/kg of food). In tilapia, the effectiveness of the aromatase inhibition by ATD is demonstrated by the marked decrease of the gonadal aromatase activity in treated animals versus control. No masculinization is obtained following treatment with an estrogen receptor antagonist (tamoxifen) in both species. Aromatase and estrogen receptor gene expression was studied in rainbow trout by semi‐quantitative RT‐PCR in gonads sampled before, during and after sex‐differentiation. Aromatase mRNA is specifically detected in female gonads, 3 weeks before the first sign of histological sex‐differentiation, i.e., first female meiosis. Aromatase expression in male gonads is at least a few hundred times less than in female gonads. Estrogen receptor gene is expressed in both male and female gonads at all stages with no dimorphic expression between sexes. Specific aromatase gene expression before ovarian differentiation was also demonstrated using virtual Northern blot, with no expression detected in male differentiating gonads. From these results it can be concluded that estrogen synthesis is crucial for ovarian differentiation, and transcription of the aromatase gene can be proposed as a key step in that process in fish. Mol. Reprod. Dev. 54:154–162, 1999. © 1999 Wiley‐Liss, Inc.</description><subject>Animals</subject><subject>aromatase</subject><subject>Aromatase - drug effects</subject><subject>Aromatase - genetics</subject><subject>Aromatase - metabolism</subject><subject>Biological and medical sciences</subject><subject>Blotting, Northern</subject><subject>Cell differentiation, maturation, development, hematopoiesis</subject><subject>Cell physiology</subject><subject>DNA, Complementary - analysis</subject><subject>Dose-Response Relationship, Drug</subject><subject>Egg Proteins - pharmacology</subject><subject>enzyme inhibitors</subject><subject>estrogen receptor</subject><subject>estrogen receptors</subject><subject>estrogens</subject><subject>Estrogens - physiology</subject><subject>Female</subject><subject>fish</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Expression</subject><subject>gonads</subject><subject>Gonads - anatomy & histology</subject><subject>Gonads - drug effects</subject><subject>Life Sciences</subject><subject>Male</subject><subject>masculinizing effect</subject><subject>Molecular and cellular biology</subject><subject>Oncorhynchus mykiss</subject><subject>Oncorhynchus mykiss - physiology</subject><subject>Ovary - anatomy & histology</subject><subject>Receptors, Estrogen - physiology</subject><subject>Reproductive Biology</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>Sequence Analysis, DNA</subject><subject>sex differentiation</subject><subject>Sex Differentiation - drug effects</subject><subject>Sex Differentiation - physiology</subject><subject>sexual development</subject><subject>steroids</subject><subject>Tamoxifen - pharmacology</subject><subject>tilapia (common name)</subject><subject>Tilapia - physiology</subject><issn>1040-452X</issn><issn>1098-2795</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1999</creationdate><recordtype>article</recordtype><recordid>eNqFkdFu0zAUhiMEYmPwCuALhNaLFNuJY3tMSFMHW1GhgnUCcXPkuc7qLY2Lna7r4_CmOE1VkEDiJontz19-nT9JjgnuE4zp68OL4WDYI1iKlHLJDomUkuAey4_oMYnPo5Phafrxyyl_m_VxfzB-Q1P2INnfXXjYfuc4zRn9tpc8CeEGYyylwI-TvXjASc7ZfvJzWN-56s7MTd0gVyITGu-uTR2QrVEzM2jhnTYhtGfB3KOpLUvjI2xVY129oVYOlTbMUFgYbU042tzzytZXboWibtmgw3GtnZ-taz1bBjRf39oQekjVU6RQYyu1sCoy3jg9825uA6pt5Rqrl6H3NHlUqiqYZ9v3QXL5_t1kcJ6OxmfDwcko1XnBeSpIachUFwXHRcGmglNRZDwveX5FMq14HInkIhNiqpnCGTeESiFKY8qccSPz7CDpdd6ZqmDh7Vz5NThl4fxkBO0epkU0cHZHIvuqY-N0fizjzCBm1qaqVG3cMgDHmMSOaAQnHai9C8GbcmcmGNqaAdqaoW0N2tagqxlYDhSiAiDWDG3NkAGGwThus6h9vv3_8mpupn9Iu14j8HILqKBVVXpVaxt-c1IwucG28Va2Muu_sv0n2j-SbdZRm3ZaGxpzv9MqfwsFzziDr5_OoPg8-j75kA-gHeeLji-VA3XtY9LLC4pJhqlkVOQi-wXlXehP</recordid><startdate>199910</startdate><enddate>199910</enddate><creator>Guiguen, Y</creator><creator>Baroiller, J.F</creator><creator>Ricordel, M.J</creator><creator>Iseki, K</creator><creator>McMeel, O.M</creator><creator>Martin, S.A.M</creator><creator>Fostier, A</creator><general>John Wiley & Sons, Inc</general><general>Wiley-Liss</general><general>Wiley</general><scope>FBQ</scope><scope>BSCLL</scope><scope>IQODW</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>1XC</scope><orcidid>https://orcid.org/0000-0001-5464-6219</orcidid></search><sort><creationdate>199910</creationdate><title>Involvement of estrogens in the process of sex differentiation in two fish species: the rainbow trout (Oncorhynchus mykiss) and a tilapia (Oreochromis niloticus)</title><author>Guiguen, Y ; Baroiller, J.F ; Ricordel, M.J ; Iseki, K ; McMeel, O.M ; Martin, S.A.M ; Fostier, A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4677-81fe1dc6670665d87286374f74b13ca7279978388dc5a037e12988feef457e943</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1999</creationdate><topic>Animals</topic><topic>aromatase</topic><topic>Aromatase - drug effects</topic><topic>Aromatase - genetics</topic><topic>Aromatase - metabolism</topic><topic>Biological and medical sciences</topic><topic>Blotting, Northern</topic><topic>Cell differentiation, maturation, development, hematopoiesis</topic><topic>Cell physiology</topic><topic>DNA, Complementary - analysis</topic><topic>Dose-Response Relationship, Drug</topic><topic>Egg Proteins - pharmacology</topic><topic>enzyme inhibitors</topic><topic>estrogen receptor</topic><topic>estrogen receptors</topic><topic>estrogens</topic><topic>Estrogens - physiology</topic><topic>Female</topic><topic>fish</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Expression</topic><topic>gonads</topic><topic>Gonads - anatomy & histology</topic><topic>Gonads - drug effects</topic><topic>Life Sciences</topic><topic>Male</topic><topic>masculinizing effect</topic><topic>Molecular and cellular biology</topic><topic>Oncorhynchus mykiss</topic><topic>Oncorhynchus mykiss - physiology</topic><topic>Ovary - anatomy & histology</topic><topic>Receptors, Estrogen - physiology</topic><topic>Reproductive Biology</topic><topic>Reverse Transcriptase Polymerase Chain Reaction</topic><topic>Sequence Analysis, DNA</topic><topic>sex differentiation</topic><topic>Sex Differentiation - drug effects</topic><topic>Sex Differentiation - physiology</topic><topic>sexual development</topic><topic>steroids</topic><topic>Tamoxifen - pharmacology</topic><topic>tilapia (common name)</topic><topic>Tilapia - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Guiguen, Y</creatorcontrib><creatorcontrib>Baroiller, J.F</creatorcontrib><creatorcontrib>Ricordel, M.J</creatorcontrib><creatorcontrib>Iseki, K</creatorcontrib><creatorcontrib>McMeel, O.M</creatorcontrib><creatorcontrib>Martin, S.A.M</creatorcontrib><creatorcontrib>Fostier, A</creatorcontrib><collection>AGRIS</collection><collection>Istex</collection><collection>Pascal-Francis</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>Hyper Article en Ligne (HAL)</collection><jtitle>Molecular reproduction and development</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Guiguen, Y</au><au>Baroiller, J.F</au><au>Ricordel, M.J</au><au>Iseki, K</au><au>McMeel, O.M</au><au>Martin, S.A.M</au><au>Fostier, A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Involvement of estrogens in the process of sex differentiation in two fish species: the rainbow trout (Oncorhynchus mykiss) and a tilapia (Oreochromis niloticus)</atitle><jtitle>Molecular reproduction and development</jtitle><addtitle>Mol. Reprod. Dev</addtitle><date>1999-10</date><risdate>1999</risdate><volume>54</volume><issue>2</issue><spage>154</spage><epage>162</epage><pages>154-162</pages><issn>1040-452X</issn><eissn>1098-2795</eissn><coden>MREDEE</coden><abstract>In order to study the physiological implication of sex steroid hormones in gonadal sex differentiation in fish, we first investigated the potential role of estrogens using two fish models: the rainbow trout (Oncorhynchus mykiss) and a tilapia species (Oreochromis niloticus). All experiments were carried out on genetically all‐male (XY) and all‐female (XX) populations. In vivo treatments with an aromatase inhibitor (ATD, 1,4,6‐ androstatriene‐3–17‐dione) result in 100% masculinization of an all‐female population in rainbow trout (dosage 50 mg/kg of food) and 75.3% in tilapia (dosage 150 mg/kg of food). In tilapia, the effectiveness of the aromatase inhibition by ATD is demonstrated by the marked decrease of the gonadal aromatase activity in treated animals versus control. No masculinization is obtained following treatment with an estrogen receptor antagonist (tamoxifen) in both species. Aromatase and estrogen receptor gene expression was studied in rainbow trout by semi‐quantitative RT‐PCR in gonads sampled before, during and after sex‐differentiation. Aromatase mRNA is specifically detected in female gonads, 3 weeks before the first sign of histological sex‐differentiation, i.e., first female meiosis. Aromatase expression in male gonads is at least a few hundred times less than in female gonads. Estrogen receptor gene is expressed in both male and female gonads at all stages with no dimorphic expression between sexes. Specific aromatase gene expression before ovarian differentiation was also demonstrated using virtual Northern blot, with no expression detected in male differentiating gonads. From these results it can be concluded that estrogen synthesis is crucial for ovarian differentiation, and transcription of the aromatase gene can be proposed as a key step in that process in fish. Mol. Reprod. Dev. 54:154–162, 1999. © 1999 Wiley‐Liss, Inc.</abstract><cop>New York</cop><pub>John Wiley & Sons, Inc</pub><pmid>10471475</pmid><doi>10.1002/(SICI)1098-2795(199910)54:2<154::AID-MRD7>3.0.CO;2-5</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0001-5464-6219</orcidid></addata></record> |
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subjects | Animals aromatase Aromatase - drug effects Aromatase - genetics Aromatase - metabolism Biological and medical sciences Blotting, Northern Cell differentiation, maturation, development, hematopoiesis Cell physiology DNA, Complementary - analysis Dose-Response Relationship, Drug Egg Proteins - pharmacology enzyme inhibitors estrogen receptor estrogen receptors estrogens Estrogens - physiology Female fish Fundamental and applied biological sciences. Psychology Gene Expression gonads Gonads - anatomy & histology Gonads - drug effects Life Sciences Male masculinizing effect Molecular and cellular biology Oncorhynchus mykiss Oncorhynchus mykiss - physiology Ovary - anatomy & histology Receptors, Estrogen - physiology Reproductive Biology Reverse Transcriptase Polymerase Chain Reaction Sequence Analysis, DNA sex differentiation Sex Differentiation - drug effects Sex Differentiation - physiology sexual development steroids Tamoxifen - pharmacology tilapia (common name) Tilapia - physiology |
title | Involvement of estrogens in the process of sex differentiation in two fish species: the rainbow trout (Oncorhynchus mykiss) and a tilapia (Oreochromis niloticus) |
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