Differential expression patterns of three aromatase genes and of four estrogen receptors genes in the testes of trout (Oncorhynchus mykiss)
SUMMARY Estrogens are implicated in male gonad function, although their physiological roles remain uncertain. In the present study, we take advantage of the original model of spatio‐temporal organization of trout spermatogenesis to revisit the synthesis and action sites of estrogens in fish testis....
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Veröffentlicht in: | Molecular reproduction and development 2015-09, Vol.82 (9), p.694-708 |
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description | SUMMARY
Estrogens are implicated in male gonad function, although their physiological roles remain uncertain. In the present study, we take advantage of the original model of spatio‐temporal organization of trout spermatogenesis to revisit the synthesis and action sites of estrogens in fish testis. Within this system, somatic cell and germ cell development are synchronized due to a strict seasonal spermatogenetic cycle and the cystic organization of gonads. We evaluated the expression patterns and regulation of three aromatase isoforms (cyp19a, cyp19b‐I, and cyp19b‐II) and four estrogen receptors (esr1a, esr1b, esr2a, and esr2b) by quantitative reverse‐transcriptase PCR during testicular maturation and in isolated germ cell populations. Our data demonstrated a reciprocal relationship between cyp19a and cyp19b (I and II) expression during testicular development (cyp19a decreased while cyp19b increased with maturation). Furthermore, cyp19b is significantly expressed in late germ cells. At the protein level, aromatase was immunohistochemically identified in interstitial tissue and in germ cells. Remarkable elevation of esr1a and esr2a was observed during the final stage of spermiation, while esr1b was expressed in an early stage of spermatogenetic development. Estrogen implants reduced testicular cyp19a transcript abundance while up‐regulating cyp19b levels, whereas androgens up‐regulated testicular esr1a, esr2a, and esr2b. Together, the distinct spatio‐temporal expression profiles and regulation of aromatases and estrogen receptors suggest that estrogens have discrete physiological functions during an early step of spermatogenesis and in the final stages of germ cell maturation and/or excretion. Mol. Reprod. Dev. 82: 694–708, 2015. © 2015 Wiley Periodicals, Inc. |
doi_str_mv | 10.1002/mrd.22509 |
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Estrogens are implicated in male gonad function, although their physiological roles remain uncertain. In the present study, we take advantage of the original model of spatio‐temporal organization of trout spermatogenesis to revisit the synthesis and action sites of estrogens in fish testis. Within this system, somatic cell and germ cell development are synchronized due to a strict seasonal spermatogenetic cycle and the cystic organization of gonads. We evaluated the expression patterns and regulation of three aromatase isoforms (cyp19a, cyp19b‐I, and cyp19b‐II) and four estrogen receptors (esr1a, esr1b, esr2a, and esr2b) by quantitative reverse‐transcriptase PCR during testicular maturation and in isolated germ cell populations. Our data demonstrated a reciprocal relationship between cyp19a and cyp19b (I and II) expression during testicular development (cyp19a decreased while cyp19b increased with maturation). Furthermore, cyp19b is significantly expressed in late germ cells. At the protein level, aromatase was immunohistochemically identified in interstitial tissue and in germ cells. Remarkable elevation of esr1a and esr2a was observed during the final stage of spermiation, while esr1b was expressed in an early stage of spermatogenetic development. Estrogen implants reduced testicular cyp19a transcript abundance while up‐regulating cyp19b levels, whereas androgens up‐regulated testicular esr1a, esr2a, and esr2b. Together, the distinct spatio‐temporal expression profiles and regulation of aromatases and estrogen receptors suggest that estrogens have discrete physiological functions during an early step of spermatogenesis and in the final stages of germ cell maturation and/or excretion. Mol. Reprod. Dev. 82: 694–708, 2015. © 2015 Wiley Periodicals, Inc.</description><identifier>ISSN: 1040-452X</identifier><identifier>EISSN: 1098-2795</identifier><identifier>DOI: 10.1002/mrd.22509</identifier><identifier>PMID: 26018767</identifier><identifier>CODEN: MREDEE</identifier><language>eng</language><publisher>United States: Blackwell Publishing Ltd</publisher><subject>Animals ; Aromatase - analysis ; Aromatase - genetics ; Aromatase - metabolism ; Estradiol - pharmacology ; Fish Proteins - analysis ; Fish Proteins - genetics ; Fish Proteins - metabolism ; Gene Expression - drug effects ; Gene Expression - genetics ; Life Sciences ; Male ; Oncorhynchus mykiss ; Oncorhynchus mykiss - genetics ; Receptors, Estrogen - analysis ; Receptors, Estrogen - genetics ; Receptors, Estrogen - metabolism ; Reproductive Biology ; Testis - enzymology ; Testis - metabolism</subject><ispartof>Molecular reproduction and development, 2015-09, Vol.82 (9), p.694-708</ispartof><rights>2015 Wiley Periodicals, Inc.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4949-54882dc4922e73a1096a1ae43f8c984d5e252de4b0abf3b3a702efbda82e67b63</citedby><orcidid>0000-0003-0747-0024</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fmrd.22509$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fmrd.22509$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,776,780,881,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26018767$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01222887$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Delalande, Christelle</creatorcontrib><creatorcontrib>Goupil, Anne-Sophie</creatorcontrib><creatorcontrib>Lareyre, Jean-Jacques</creatorcontrib><creatorcontrib>Le Gac, Florence</creatorcontrib><title>Differential expression patterns of three aromatase genes and of four estrogen receptors genes in the testes of trout (Oncorhynchus mykiss)</title><title>Molecular reproduction and development</title><addtitle>Mol. Reprod. Dev</addtitle><description>SUMMARY
Estrogens are implicated in male gonad function, although their physiological roles remain uncertain. In the present study, we take advantage of the original model of spatio‐temporal organization of trout spermatogenesis to revisit the synthesis and action sites of estrogens in fish testis. Within this system, somatic cell and germ cell development are synchronized due to a strict seasonal spermatogenetic cycle and the cystic organization of gonads. We evaluated the expression patterns and regulation of three aromatase isoforms (cyp19a, cyp19b‐I, and cyp19b‐II) and four estrogen receptors (esr1a, esr1b, esr2a, and esr2b) by quantitative reverse‐transcriptase PCR during testicular maturation and in isolated germ cell populations. Our data demonstrated a reciprocal relationship between cyp19a and cyp19b (I and II) expression during testicular development (cyp19a decreased while cyp19b increased with maturation). Furthermore, cyp19b is significantly expressed in late germ cells. At the protein level, aromatase was immunohistochemically identified in interstitial tissue and in germ cells. Remarkable elevation of esr1a and esr2a was observed during the final stage of spermiation, while esr1b was expressed in an early stage of spermatogenetic development. Estrogen implants reduced testicular cyp19a transcript abundance while up‐regulating cyp19b levels, whereas androgens up‐regulated testicular esr1a, esr2a, and esr2b. Together, the distinct spatio‐temporal expression profiles and regulation of aromatases and estrogen receptors suggest that estrogens have discrete physiological functions during an early step of spermatogenesis and in the final stages of germ cell maturation and/or excretion. Mol. Reprod. Dev. 82: 694–708, 2015. © 2015 Wiley Periodicals, Inc.</description><subject>Animals</subject><subject>Aromatase - analysis</subject><subject>Aromatase - genetics</subject><subject>Aromatase - metabolism</subject><subject>Estradiol - pharmacology</subject><subject>Fish Proteins - analysis</subject><subject>Fish Proteins - genetics</subject><subject>Fish Proteins - metabolism</subject><subject>Gene Expression - drug effects</subject><subject>Gene Expression - genetics</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Oncorhynchus mykiss</subject><subject>Oncorhynchus mykiss - genetics</subject><subject>Receptors, Estrogen - analysis</subject><subject>Receptors, Estrogen - genetics</subject><subject>Receptors, Estrogen - metabolism</subject><subject>Reproductive Biology</subject><subject>Testis - enzymology</subject><subject>Testis - metabolism</subject><issn>1040-452X</issn><issn>1098-2795</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkstu1TAQhiMEoqWw4AWQJTbtIq1vie1l1dKW6tAKBIKd5SQTjtvEDnYCPc_AS-M0h7Ngxcq_Zr5_5Llk2WuCjwnG9KQPzTGlBVZPsn2ClcypUMXTWXOc84J-28texHiHMVZK4ufZHi0xkaIU-9nvc9u2EMCN1nQIHoYAMVrv0GDGEYKLyLdoXAcAZILvzWgioO_gICLjmjnZ-ikgiGPwKYwC1DCMPsQtZF1yAxoTAEut4KcRHd662of1xtXrKaJ-c29jPHqZPWtNF-HV9j3Ivly8-3x2la9uL9-fna7ymiuu8oJLSZukKQXBTGq4NMQAZ62sleRNAbSgDfAKm6plFTMCU2irxkgKpahKdpAdLXXXptNDsL0JG-2N1VenKz3HMKGUSil-ksQeLuwQ_I8pdaF7G2voOuPAT1ETwaikabLiP1DCFGekmNG3_6B3aYouNT1TlCuBRZGoN1tqqnpodl_9u70EnCzAL9vBZpcnWM9nodNZ6Mez0B8-nT-K5MgXh037eNg5TLjXqZ4o9NebS33Nibz5eC31BfsDvVS5bw</recordid><startdate>201509</startdate><enddate>201509</enddate><creator>Delalande, Christelle</creator><creator>Goupil, Anne-Sophie</creator><creator>Lareyre, Jean-Jacques</creator><creator>Le Gac, Florence</creator><general>Blackwell Publishing Ltd</general><general>Wiley Subscription Services, Inc</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>7QP</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0003-0747-0024</orcidid></search><sort><creationdate>201509</creationdate><title>Differential expression patterns of three aromatase genes and of four estrogen receptors genes in the testes of trout (Oncorhynchus mykiss)</title><author>Delalande, Christelle ; Goupil, Anne-Sophie ; Lareyre, Jean-Jacques ; Le Gac, Florence</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4949-54882dc4922e73a1096a1ae43f8c984d5e252de4b0abf3b3a702efbda82e67b63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Aromatase - analysis</topic><topic>Aromatase - genetics</topic><topic>Aromatase - metabolism</topic><topic>Estradiol - pharmacology</topic><topic>Fish Proteins - analysis</topic><topic>Fish Proteins - genetics</topic><topic>Fish Proteins - metabolism</topic><topic>Gene Expression - drug effects</topic><topic>Gene Expression - genetics</topic><topic>Life Sciences</topic><topic>Male</topic><topic>Oncorhynchus mykiss</topic><topic>Oncorhynchus mykiss - genetics</topic><topic>Receptors, Estrogen - analysis</topic><topic>Receptors, Estrogen - genetics</topic><topic>Receptors, Estrogen - metabolism</topic><topic>Reproductive Biology</topic><topic>Testis - enzymology</topic><topic>Testis - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Delalande, Christelle</creatorcontrib><creatorcontrib>Goupil, Anne-Sophie</creatorcontrib><creatorcontrib>Lareyre, Jean-Jacques</creatorcontrib><creatorcontrib>Le Gac, Florence</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</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>Delalande, Christelle</au><au>Goupil, Anne-Sophie</au><au>Lareyre, Jean-Jacques</au><au>Le Gac, Florence</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Differential expression patterns of three aromatase genes and of four estrogen receptors genes in the testes of trout (Oncorhynchus mykiss)</atitle><jtitle>Molecular reproduction and development</jtitle><addtitle>Mol. Reprod. Dev</addtitle><date>2015-09</date><risdate>2015</risdate><volume>82</volume><issue>9</issue><spage>694</spage><epage>708</epage><pages>694-708</pages><issn>1040-452X</issn><eissn>1098-2795</eissn><coden>MREDEE</coden><abstract>SUMMARY
Estrogens are implicated in male gonad function, although their physiological roles remain uncertain. In the present study, we take advantage of the original model of spatio‐temporal organization of trout spermatogenesis to revisit the synthesis and action sites of estrogens in fish testis. Within this system, somatic cell and germ cell development are synchronized due to a strict seasonal spermatogenetic cycle and the cystic organization of gonads. We evaluated the expression patterns and regulation of three aromatase isoforms (cyp19a, cyp19b‐I, and cyp19b‐II) and four estrogen receptors (esr1a, esr1b, esr2a, and esr2b) by quantitative reverse‐transcriptase PCR during testicular maturation and in isolated germ cell populations. Our data demonstrated a reciprocal relationship between cyp19a and cyp19b (I and II) expression during testicular development (cyp19a decreased while cyp19b increased with maturation). Furthermore, cyp19b is significantly expressed in late germ cells. At the protein level, aromatase was immunohistochemically identified in interstitial tissue and in germ cells. Remarkable elevation of esr1a and esr2a was observed during the final stage of spermiation, while esr1b was expressed in an early stage of spermatogenetic development. Estrogen implants reduced testicular cyp19a transcript abundance while up‐regulating cyp19b levels, whereas androgens up‐regulated testicular esr1a, esr2a, and esr2b. Together, the distinct spatio‐temporal expression profiles and regulation of aromatases and estrogen receptors suggest that estrogens have discrete physiological functions during an early step of spermatogenesis and in the final stages of germ cell maturation and/or excretion. Mol. Reprod. Dev. 82: 694–708, 2015. © 2015 Wiley Periodicals, Inc.</abstract><cop>United States</cop><pub>Blackwell Publishing Ltd</pub><pmid>26018767</pmid><doi>10.1002/mrd.22509</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0003-0747-0024</orcidid></addata></record> |
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subjects | Animals Aromatase - analysis Aromatase - genetics Aromatase - metabolism Estradiol - pharmacology Fish Proteins - analysis Fish Proteins - genetics Fish Proteins - metabolism Gene Expression - drug effects Gene Expression - genetics Life Sciences Male Oncorhynchus mykiss Oncorhynchus mykiss - genetics Receptors, Estrogen - analysis Receptors, Estrogen - genetics Receptors, Estrogen - metabolism Reproductive Biology Testis - enzymology Testis - metabolism |
title | Differential expression patterns of three aromatase genes and of four estrogen receptors genes in the testes of trout (Oncorhynchus mykiss) |
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