Epigenetic control of gonadal aromatase (cyp19a1) in temperature-dependent sex determination of red-eared slider turtles
In the red-eared slider turtle (Trachemys scripta), a species with temperature-dependent sex determination (TSD), the expression of the aromatase gene during gonad development is strictly limited to the female-producing temperature. The underlying mechanism remains unknown. In this study, we identif...
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| description | In the red-eared slider turtle (Trachemys scripta), a species with temperature-dependent sex determination (TSD), the expression of the aromatase gene during gonad development is strictly limited to the female-producing temperature. The underlying mechanism remains unknown. In this study, we identified the upstream 5'-flanking region of the aromatase gene, gonad-specific promoter, and the temperature-dependent DNA methylation signatures during gonad development in the red-eared slider turtle. The 5'-flanking region of the slider aromatase exhibited sequence similarities to the aromatase genes of the American alligator, chicken, quail, and zebra finch. A putative TATA box was located 31 bp upstream of the gonad-specific transcription start site. DNA methylation at the CpG sites between the putative binding sites of the fork head domain factor (FOX) and vertebrate steroidogenic factor 1 (SF1) and adjacent TATA box in the promoter region were significantly lower in embryonic gonads at the female-producing temperature compared the male-producing temperature. A shift from male- to female-, but not from female- to male-, producing temperature changed the level of DNA methylation in gonads. Taken together these results indicate that the temperature, particularly female-producing temperature, allows demethylation at the specific CpG sites of the promoter region which leads the temperature-specific expression of aromatase during gonad development. |
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The underlying mechanism remains unknown. In this study, we identified the upstream 5'-flanking region of the aromatase gene, gonad-specific promoter, and the temperature-dependent DNA methylation signatures during gonad development in the red-eared slider turtle. The 5'-flanking region of the slider aromatase exhibited sequence similarities to the aromatase genes of the American alligator, chicken, quail, and zebra finch. A putative TATA box was located 31 bp upstream of the gonad-specific transcription start site. DNA methylation at the CpG sites between the putative binding sites of the fork head domain factor (FOX) and vertebrate steroidogenic factor 1 (SF1) and adjacent TATA box in the promoter region were significantly lower in embryonic gonads at the female-producing temperature compared the male-producing temperature. A shift from male- to female-, but not from female- to male-, producing temperature changed the level of DNA methylation in gonads. Taken together these results indicate that the temperature, particularly female-producing temperature, allows demethylation at the specific CpG sites of the promoter region which leads the temperature-specific expression of aromatase during gonad development.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0063599</identifier><identifier>PMID: 23762231</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>5' Flanking Region - genetics ; Alligators ; Animals ; Aquatic reptiles ; Aromatase ; Aromatase - genetics ; Aromatase - metabolism ; Base Pairing - genetics ; Base Sequence ; Binding Sites ; Biology ; Codon, Initiator - genetics ; Conserved Sequence - genetics ; CpG islands ; CpG Islands - genetics ; Cytochrome P-450 ; Demethylation ; Deoxyribonucleic acid ; DNA ; DNA methylation ; DNA Methylation - genetics ; Embryos ; Endocrinology ; Epigenesis, Genetic ; Epigenetic inheritance ; Epigenetics ; Female ; Gene expression ; Genes ; Genetic engineering ; Genomes ; Gonads ; Gonads - embryology ; Gonads - enzymology ; Hormones ; Male ; Mammals ; Methylation ; Molecular Sequence Data ; Organ Specificity - genetics ; Promoter Regions, Genetic - genetics ; Protein Biosynthesis - genetics ; Reptiles & amphibians ; Sequence Homology, Nucleic Acid ; Sex ; Sex determination ; Sex Determination Processes - genetics ; Steroidogenic factor 1 ; Tata box ; Temperature ; Temperature effects ; Trachemys scripta ; Transcription (Genetics) ; Transcription Factors - metabolism ; Transcription Initiation Site ; Turtles ; Turtles - embryology ; Turtles - genetics ; Vertebrates ; Zebra finch</subject><ispartof>PloS one, 2013-06, Vol.8 (6), p.e63599-e63599</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Matsumoto et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013 Matsumoto et al 2013 Matsumoto et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c593t-2f90ba0b21975e5df843777b35464d52c37606708839a966d8243bcbb4c6a56b3</citedby><cites>FETCH-LOGICAL-c593t-2f90ba0b21975e5df843777b35464d52c37606708839a966d8243bcbb4c6a56b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3676416/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3676416/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,2096,2915,23847,27905,27906,53772,53774,79349,79350</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23762231$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Shioda, Toshi</contributor><creatorcontrib>Matsumoto, Yuiko</creatorcontrib><creatorcontrib>Buemio, Alvin</creatorcontrib><creatorcontrib>Chu, Randy</creatorcontrib><creatorcontrib>Vafaee, Mozhgon</creatorcontrib><creatorcontrib>Crews, David</creatorcontrib><title>Epigenetic control of gonadal aromatase (cyp19a1) in temperature-dependent sex determination of red-eared slider turtles</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>In the red-eared slider turtle (Trachemys scripta), a species with temperature-dependent sex determination (TSD), the expression of the aromatase gene during gonad development is strictly limited to the female-producing temperature. The underlying mechanism remains unknown. In this study, we identified the upstream 5'-flanking region of the aromatase gene, gonad-specific promoter, and the temperature-dependent DNA methylation signatures during gonad development in the red-eared slider turtle. The 5'-flanking region of the slider aromatase exhibited sequence similarities to the aromatase genes of the American alligator, chicken, quail, and zebra finch. A putative TATA box was located 31 bp upstream of the gonad-specific transcription start site. DNA methylation at the CpG sites between the putative binding sites of the fork head domain factor (FOX) and vertebrate steroidogenic factor 1 (SF1) and adjacent TATA box in the promoter region were significantly lower in embryonic gonads at the female-producing temperature compared the male-producing temperature. A shift from male- to female-, but not from female- to male-, producing temperature changed the level of DNA methylation in gonads. Taken together these results indicate that the temperature, particularly female-producing temperature, allows demethylation at the specific CpG sites of the promoter region which leads the temperature-specific expression of aromatase during gonad development.</description><subject>5' Flanking Region - genetics</subject><subject>Alligators</subject><subject>Animals</subject><subject>Aquatic reptiles</subject><subject>Aromatase</subject><subject>Aromatase - genetics</subject><subject>Aromatase - metabolism</subject><subject>Base Pairing - genetics</subject><subject>Base Sequence</subject><subject>Binding Sites</subject><subject>Biology</subject><subject>Codon, Initiator - genetics</subject><subject>Conserved Sequence - genetics</subject><subject>CpG islands</subject><subject>CpG Islands - genetics</subject><subject>Cytochrome P-450</subject><subject>Demethylation</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA methylation</subject><subject>DNA Methylation - genetics</subject><subject>Embryos</subject><subject>Endocrinology</subject><subject>Epigenesis, Genetic</subject><subject>Epigenetic inheritance</subject><subject>Epigenetics</subject><subject>Female</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genetic engineering</subject><subject>Genomes</subject><subject>Gonads</subject><subject>Gonads - embryology</subject><subject>Gonads - enzymology</subject><subject>Hormones</subject><subject>Male</subject><subject>Mammals</subject><subject>Methylation</subject><subject>Molecular Sequence Data</subject><subject>Organ Specificity - genetics</subject><subject>Promoter Regions, Genetic - genetics</subject><subject>Protein Biosynthesis - genetics</subject><subject>Reptiles & amphibians</subject><subject>Sequence Homology, Nucleic Acid</subject><subject>Sex</subject><subject>Sex determination</subject><subject>Sex Determination Processes - genetics</subject><subject>Steroidogenic factor 1</subject><subject>Tata box</subject><subject>Temperature</subject><subject>Temperature effects</subject><subject>Trachemys scripta</subject><subject>Transcription (Genetics)</subject><subject>Transcription Factors - metabolism</subject><subject>Transcription Initiation Site</subject><subject>Turtles</subject><subject>Turtles - embryology</subject><subject>Turtles - genetics</subject><subject>Vertebrates</subject><subject>Zebra finch</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNptUl1rFDEUHUSxtfoPRAd8qQ-75juZF6GUqoWCL_oc7kzurFlmkjGZLe2_N9udllZKIAnJOefeczlV9Z6SNeWaftnGXQowrKcYcE2I4rJpXlTHtOFspRjhLx_dj6o3OW8Jkdwo9bo6Ylwrxjg9rm4uJr_BgLPv6i6GOcWhjn29iQEcDDWkOMIMGevT7naiDdDPtQ_1jOOECeZdwpXDCYPDMNcZb2qHM6bRB5h9DHulhG6FUPY6D95hqgtpHjC_rV71MGR8t5wn1e9vF7_Of6yufn6_PD-7WnWy4fOK9Q1pgbSMNlqidL0RXGvdcimUcJJ1xQlRmhjDG2iUcoYJ3nZtKzoFUrX8pPp40J2GmO0ytGwpV9IQrY0qiMsDwkXY2in5EdKtjeDt3UNMGwupzGdAi0RKJikQzpxomWg6ARwMtKqlWoApWl-Xart2RNeVsSQYnog-_Qn-j93Ea8uVVoLumzldBFL8u8M829HnDocBAsbdXd_aGEI4KdBP_0Gfd7egNlAM-NDHUrfbi9ozoY0glDBdUOtnUGU5HH3JBfa-vD8hiAOhSzHnhP2DR0rsPp_3zdh9Pu2Sz0L78Hg-D6T7QPJ_cCniTQ</recordid><startdate>20130607</startdate><enddate>20130607</enddate><creator>Matsumoto, Yuiko</creator><creator>Buemio, Alvin</creator><creator>Chu, Randy</creator><creator>Vafaee, Mozhgon</creator><creator>Crews, David</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><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>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20130607</creationdate><title>Epigenetic control of gonadal aromatase (cyp19a1) in temperature-dependent sex determination of red-eared slider turtles</title><author>Matsumoto, Yuiko ; Buemio, Alvin ; Chu, Randy ; Vafaee, Mozhgon ; Crews, David</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c593t-2f90ba0b21975e5df843777b35464d52c37606708839a966d8243bcbb4c6a56b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>5' Flanking Region - genetics</topic><topic>Alligators</topic><topic>Animals</topic><topic>Aquatic reptiles</topic><topic>Aromatase</topic><topic>Aromatase - genetics</topic><topic>Aromatase - metabolism</topic><topic>Base Pairing - genetics</topic><topic>Base Sequence</topic><topic>Binding Sites</topic><topic>Biology</topic><topic>Codon, Initiator - genetics</topic><topic>Conserved Sequence - genetics</topic><topic>CpG islands</topic><topic>CpG Islands - genetics</topic><topic>Cytochrome P-450</topic><topic>Demethylation</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA methylation</topic><topic>DNA Methylation - genetics</topic><topic>Embryos</topic><topic>Endocrinology</topic><topic>Epigenesis, Genetic</topic><topic>Epigenetic inheritance</topic><topic>Epigenetics</topic><topic>Female</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Genetic engineering</topic><topic>Genomes</topic><topic>Gonads</topic><topic>Gonads - embryology</topic><topic>Gonads - enzymology</topic><topic>Hormones</topic><topic>Male</topic><topic>Mammals</topic><topic>Methylation</topic><topic>Molecular Sequence Data</topic><topic>Organ Specificity - genetics</topic><topic>Promoter Regions, Genetic - genetics</topic><topic>Protein Biosynthesis - genetics</topic><topic>Reptiles & amphibians</topic><topic>Sequence Homology, Nucleic Acid</topic><topic>Sex</topic><topic>Sex determination</topic><topic>Sex Determination Processes - genetics</topic><topic>Steroidogenic factor 1</topic><topic>Tata box</topic><topic>Temperature</topic><topic>Temperature effects</topic><topic>Trachemys scripta</topic><topic>Transcription (Genetics)</topic><topic>Transcription Factors - metabolism</topic><topic>Transcription Initiation Site</topic><topic>Turtles</topic><topic>Turtles - embryology</topic><topic>Turtles - genetics</topic><topic>Vertebrates</topic><topic>Zebra finch</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Matsumoto, Yuiko</creatorcontrib><creatorcontrib>Buemio, Alvin</creatorcontrib><creatorcontrib>Chu, Randy</creatorcontrib><creatorcontrib>Vafaee, Mozhgon</creatorcontrib><creatorcontrib>Crews, David</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Matsumoto, Yuiko</au><au>Buemio, Alvin</au><au>Chu, Randy</au><au>Vafaee, Mozhgon</au><au>Crews, David</au><au>Shioda, Toshi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Epigenetic control of gonadal aromatase (cyp19a1) in temperature-dependent sex determination of red-eared slider turtles</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-06-07</date><risdate>2013</risdate><volume>8</volume><issue>6</issue><spage>e63599</spage><epage>e63599</epage><pages>e63599-e63599</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>In the red-eared slider turtle (Trachemys scripta), a species with temperature-dependent sex determination (TSD), the expression of the aromatase gene during gonad development is strictly limited to the female-producing temperature. The underlying mechanism remains unknown. In this study, we identified the upstream 5'-flanking region of the aromatase gene, gonad-specific promoter, and the temperature-dependent DNA methylation signatures during gonad development in the red-eared slider turtle. The 5'-flanking region of the slider aromatase exhibited sequence similarities to the aromatase genes of the American alligator, chicken, quail, and zebra finch. A putative TATA box was located 31 bp upstream of the gonad-specific transcription start site. DNA methylation at the CpG sites between the putative binding sites of the fork head domain factor (FOX) and vertebrate steroidogenic factor 1 (SF1) and adjacent TATA box in the promoter region were significantly lower in embryonic gonads at the female-producing temperature compared the male-producing temperature. A shift from male- to female-, but not from female- to male-, producing temperature changed the level of DNA methylation in gonads. Taken together these results indicate that the temperature, particularly female-producing temperature, allows demethylation at the specific CpG sites of the promoter region which leads the temperature-specific expression of aromatase during gonad development.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23762231</pmid><doi>10.1371/journal.pone.0063599</doi><oa>free_for_read</oa></addata></record> |
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| subjects | 5' Flanking Region - genetics Alligators Animals Aquatic reptiles Aromatase Aromatase - genetics Aromatase - metabolism Base Pairing - genetics Base Sequence Binding Sites Biology Codon, Initiator - genetics Conserved Sequence - genetics CpG islands CpG Islands - genetics Cytochrome P-450 Demethylation Deoxyribonucleic acid DNA DNA methylation DNA Methylation - genetics Embryos Endocrinology Epigenesis, Genetic Epigenetic inheritance Epigenetics Female Gene expression Genes Genetic engineering Genomes Gonads Gonads - embryology Gonads - enzymology Hormones Male Mammals Methylation Molecular Sequence Data Organ Specificity - genetics Promoter Regions, Genetic - genetics Protein Biosynthesis - genetics Reptiles & amphibians Sequence Homology, Nucleic Acid Sex Sex determination Sex Determination Processes - genetics Steroidogenic factor 1 Tata box Temperature Temperature effects Trachemys scripta Transcription (Genetics) Transcription Factors - metabolism Transcription Initiation Site Turtles Turtles - embryology Turtles - genetics Vertebrates Zebra finch |
| title | Epigenetic control of gonadal aromatase (cyp19a1) in temperature-dependent sex determination of red-eared slider turtles |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-21T01%3A56%3A13IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Epigenetic%20control%20of%20gonadal%20aromatase%20(cyp19a1)%20in%20temperature-dependent%20sex%20determination%20of%20red-eared%20slider%20turtles&rft.jtitle=PloS%20one&rft.au=Matsumoto,%20Yuiko&rft.date=2013-06-07&rft.volume=8&rft.issue=6&rft.spage=e63599&rft.epage=e63599&rft.pages=e63599-e63599&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0063599&rft_dat=%3Cgale_plos_%3EA478401027%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1365807786&rft_id=info:pmid/23762231&rft_galeid=A478401027&rft_doaj_id=oai_doaj_org_article_e055251a032d4b249c4a3a8ab6b174a8&rfr_iscdi=true |