Differential localization of serotoninergic system elements in human amniotic epithelial cells
Serotonin or 5-hydroxytryptamine (5-HT) is a biogenic amine involved in regulating several functions, including development. However, its impact on human embryo development has been poorly studied. The present work investigated the expression and distribution of the main components of the serotonine...
Gespeichert in:
Veröffentlicht in: | Biology of reproduction 2021-08, Vol.105 (2), p.439-448 |
---|---|
Hauptverfasser: | , , , , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | 448 |
---|---|
container_issue | 2 |
container_start_page | 439 |
container_title | Biology of reproduction |
container_volume | 105 |
creator | Romero-Reyes, Jessica Vázquez-Martínez, Edgar Ricardo Bahena-Alvarez, Daniel López-Jiménez, Jessica Molina-Hernández, Anayansi Camacho-Arroyo, Ignacio Díaz, Néstor Fabián |
description | Serotonin or 5-hydroxytryptamine (5-HT) is a biogenic amine involved in regulating several functions, including development. However, its impact on human embryo development has been poorly studied. The present work investigated the expression and distribution of the main components of the serotoninergic system in human amniotic tissue and human amniotic epithelial cells (hAEC) in vitro, as an alternative model of early human embryo development. Amniotic membranes from full-term healthy pregnancies were used. Human amnion tissue or hAEC isolated from the amnion was processed for reverse transcription-polymerase chain reaction and immunofluorescence analyses of the main components of the serotoninergic system. We found the expression of tryptophan hydroxylase type 1 (TPH1), type 2 (TPH2), serotonin transporter (SERT), monoamine oxidase-A (MAOA), as well as HTR1D and HTR7 receptors at mRNA level in amnion tissue as well in hAEC. Interestingly, we found the presence of 5-HT in the nucleus of the cells in amnion tissue, whereas it was located in the cytoplasm of isolated hAEC. We detected TPH1, TPH2, and HTR1D receptor in both the nucleus and cytoplasm. SERT, MAOA, and HTR7 receptor were only observed in the cytoplasm. The results presented herein show, for the first time, the presence of the serotoninergic system in human amnion in vivo and in vitro. Summary sentence The results presented show the presence of the serotoninergic system in human amnion in vivo and in vitro, which opens the potential role of 5-hydroxytryptamine and the serotoninergic system in the events that occur during early human embryonic development (given the origin of the amniotic cells) in vitro. Graphical Abstract |
doi_str_mv | 10.1093/biolre/ioab106 |
format | Article |
fullrecord | <record><control><sourceid>gale_proqu</sourceid><recordid>TN_cdi_proquest_miscellaneous_2535107866</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A701923153</galeid><oup_id>10.1093/biolre/ioab106</oup_id><sourcerecordid>A701923153</sourcerecordid><originalsourceid>FETCH-LOGICAL-b461t-7007f4236781f65c59313b84f2ccd63adfdb7868193c6444927a8a448c3b03463</originalsourceid><addsrcrecordid>eNqFkc9rFTEUhYMo9lndupQBNwpOm8zNJDPLUn9CwY1uDZnMTZuSSZ5JZlH_ejO8p4IUShaBy3c-DhxCXjJ6xugI55OLPuG5i3piVDwiO9Z3Yys7MTwmO0qpaAEEnJBnOd9Syjh08JScAKe9ZFLsyI_3zlpMGIrTvvHRaO9-6eJiaKJtMqZYYnAB07UzTb7LBZcGPS41kBsXmpt10aHRS3CxVAL3rtyg31wGvc_PyROrfcYXx_-UfP_44dvl5_bq66cvlxdX7cQFK62kVFregZADs6I3_QgMpoHbzphZgJ7tPMlBDGwEIzjnYyf1oDkfDEwUuIBT8ubg3af4c8Vc1OLy1kAHjGtWXQ89o1Wxoa__Q2_jmkJtVylBB9mLkf6jrrVH5YKNJWmzSdWFpGzsgPVQqbN7qPpmXJyJAa2r9_sCJsWcE1q1T27R6U4xqrZB1WFQdRy0Bl4d267TgvNf_M-CFXh7AOK6f1j27sDWey33EP4bbUG50g</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2560875690</pqid></control><display><type>article</type><title>Differential localization of serotoninergic system elements in human amniotic epithelial cells</title><source>MEDLINE</source><source>Oxford University Press Journals All Titles (1996-Current)</source><source>EZB-FREE-00999 freely available EZB journals</source><source>Alma/SFX Local Collection</source><creator>Romero-Reyes, Jessica ; Vázquez-Martínez, Edgar Ricardo ; Bahena-Alvarez, Daniel ; López-Jiménez, Jessica ; Molina-Hernández, Anayansi ; Camacho-Arroyo, Ignacio ; Díaz, Néstor Fabián</creator><creatorcontrib>Romero-Reyes, Jessica ; Vázquez-Martínez, Edgar Ricardo ; Bahena-Alvarez, Daniel ; López-Jiménez, Jessica ; Molina-Hernández, Anayansi ; Camacho-Arroyo, Ignacio ; Díaz, Néstor Fabián</creatorcontrib><description>Serotonin or 5-hydroxytryptamine (5-HT) is a biogenic amine involved in regulating several functions, including development. However, its impact on human embryo development has been poorly studied. The present work investigated the expression and distribution of the main components of the serotoninergic system in human amniotic tissue and human amniotic epithelial cells (hAEC) in vitro, as an alternative model of early human embryo development. Amniotic membranes from full-term healthy pregnancies were used. Human amnion tissue or hAEC isolated from the amnion was processed for reverse transcription-polymerase chain reaction and immunofluorescence analyses of the main components of the serotoninergic system. We found the expression of tryptophan hydroxylase type 1 (TPH1), type 2 (TPH2), serotonin transporter (SERT), monoamine oxidase-A (MAOA), as well as HTR1D and HTR7 receptors at mRNA level in amnion tissue as well in hAEC. Interestingly, we found the presence of 5-HT in the nucleus of the cells in amnion tissue, whereas it was located in the cytoplasm of isolated hAEC. We detected TPH1, TPH2, and HTR1D receptor in both the nucleus and cytoplasm. SERT, MAOA, and HTR7 receptor were only observed in the cytoplasm. The results presented herein show, for the first time, the presence of the serotoninergic system in human amnion in vivo and in vitro. Summary sentence The results presented show the presence of the serotoninergic system in human amnion in vivo and in vitro, which opens the potential role of 5-hydroxytryptamine and the serotoninergic system in the events that occur during early human embryonic development (given the origin of the amniotic cells) in vitro. Graphical Abstract</description><identifier>ISSN: 0006-3363</identifier><identifier>EISSN: 1529-7268</identifier><identifier>DOI: 10.1093/biolre/ioab106</identifier><identifier>PMID: 34057176</identifier><language>eng</language><publisher>United States: Society for the Study of Reproduction</publisher><subject>Amine oxidase (flavin-containing) ; Amnion ; Amnion - chemistry ; Amnion - metabolism ; Analysis ; Catecholamines ; Cytoplasm ; embryo ; Embryonic development ; Epithelial cells ; Epithelial Cells - metabolism ; Humans ; Immunofluorescence ; Localization ; Monoamine oxidase ; neurotransmitter ; Oct4 ; Polymerase chain reaction ; Pregnancy ; RESEARCH ARTICLE ; Reverse transcription ; RNA ; Scientific equipment and supplies industry ; Serotonin ; Serotonin - metabolism ; Serotonin transporter ; Stem cells ; Tryptophan ; Tryptophan hydroxylase</subject><ispartof>Biology of reproduction, 2021-08, Vol.105 (2), p.439-448</ispartof><rights>The Author(s) 2021. Published by Oxford University Press on behalf of Society for the Study of Reproduction. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com journals.permissions@oup.com</rights><rights>The Author(s) 2021. Published by Oxford University Press on behalf of Society for the Study of Reproduction. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2021</rights><rights>The Author(s) 2021. Published by Oxford University Press on behalf of Society for the Study of Reproduction. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.</rights><rights>COPYRIGHT 2021 Oxford University Press</rights><rights>The Author(s) 2021. Published by Oxford University Press on behalf of Society for the Study of Reproduction. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-b461t-7007f4236781f65c59313b84f2ccd63adfdb7868193c6444927a8a448c3b03463</citedby><cites>FETCH-LOGICAL-b461t-7007f4236781f65c59313b84f2ccd63adfdb7868193c6444927a8a448c3b03463</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,1584,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34057176$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Romero-Reyes, Jessica</creatorcontrib><creatorcontrib>Vázquez-Martínez, Edgar Ricardo</creatorcontrib><creatorcontrib>Bahena-Alvarez, Daniel</creatorcontrib><creatorcontrib>López-Jiménez, Jessica</creatorcontrib><creatorcontrib>Molina-Hernández, Anayansi</creatorcontrib><creatorcontrib>Camacho-Arroyo, Ignacio</creatorcontrib><creatorcontrib>Díaz, Néstor Fabián</creatorcontrib><title>Differential localization of serotoninergic system elements in human amniotic epithelial cells</title><title>Biology of reproduction</title><addtitle>Biol Reprod</addtitle><description>Serotonin or 5-hydroxytryptamine (5-HT) is a biogenic amine involved in regulating several functions, including development. However, its impact on human embryo development has been poorly studied. The present work investigated the expression and distribution of the main components of the serotoninergic system in human amniotic tissue and human amniotic epithelial cells (hAEC) in vitro, as an alternative model of early human embryo development. Amniotic membranes from full-term healthy pregnancies were used. Human amnion tissue or hAEC isolated from the amnion was processed for reverse transcription-polymerase chain reaction and immunofluorescence analyses of the main components of the serotoninergic system. We found the expression of tryptophan hydroxylase type 1 (TPH1), type 2 (TPH2), serotonin transporter (SERT), monoamine oxidase-A (MAOA), as well as HTR1D and HTR7 receptors at mRNA level in amnion tissue as well in hAEC. Interestingly, we found the presence of 5-HT in the nucleus of the cells in amnion tissue, whereas it was located in the cytoplasm of isolated hAEC. We detected TPH1, TPH2, and HTR1D receptor in both the nucleus and cytoplasm. SERT, MAOA, and HTR7 receptor were only observed in the cytoplasm. The results presented herein show, for the first time, the presence of the serotoninergic system in human amnion in vivo and in vitro. Summary sentence The results presented show the presence of the serotoninergic system in human amnion in vivo and in vitro, which opens the potential role of 5-hydroxytryptamine and the serotoninergic system in the events that occur during early human embryonic development (given the origin of the amniotic cells) in vitro. Graphical Abstract</description><subject>Amine oxidase (flavin-containing)</subject><subject>Amnion</subject><subject>Amnion - chemistry</subject><subject>Amnion - metabolism</subject><subject>Analysis</subject><subject>Catecholamines</subject><subject>Cytoplasm</subject><subject>embryo</subject><subject>Embryonic development</subject><subject>Epithelial cells</subject><subject>Epithelial Cells - metabolism</subject><subject>Humans</subject><subject>Immunofluorescence</subject><subject>Localization</subject><subject>Monoamine oxidase</subject><subject>neurotransmitter</subject><subject>Oct4</subject><subject>Polymerase chain reaction</subject><subject>Pregnancy</subject><subject>RESEARCH ARTICLE</subject><subject>Reverse transcription</subject><subject>RNA</subject><subject>Scientific equipment and supplies industry</subject><subject>Serotonin</subject><subject>Serotonin - metabolism</subject><subject>Serotonin transporter</subject><subject>Stem cells</subject><subject>Tryptophan</subject><subject>Tryptophan hydroxylase</subject><issn>0006-3363</issn><issn>1529-7268</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</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><recordid>eNqFkc9rFTEUhYMo9lndupQBNwpOm8zNJDPLUn9CwY1uDZnMTZuSSZ5JZlH_ejO8p4IUShaBy3c-DhxCXjJ6xugI55OLPuG5i3piVDwiO9Z3Yys7MTwmO0qpaAEEnJBnOd9Syjh08JScAKe9ZFLsyI_3zlpMGIrTvvHRaO9-6eJiaKJtMqZYYnAB07UzTb7LBZcGPS41kBsXmpt10aHRS3CxVAL3rtyg31wGvc_PyROrfcYXx_-UfP_44dvl5_bq66cvlxdX7cQFK62kVFregZADs6I3_QgMpoHbzphZgJ7tPMlBDGwEIzjnYyf1oDkfDEwUuIBT8ubg3af4c8Vc1OLy1kAHjGtWXQ89o1Wxoa__Q2_jmkJtVylBB9mLkf6jrrVH5YKNJWmzSdWFpGzsgPVQqbN7qPpmXJyJAa2r9_sCJsWcE1q1T27R6U4xqrZB1WFQdRy0Bl4d267TgvNf_M-CFXh7AOK6f1j27sDWey33EP4bbUG50g</recordid><startdate>20210801</startdate><enddate>20210801</enddate><creator>Romero-Reyes, Jessica</creator><creator>Vázquez-Martínez, Edgar Ricardo</creator><creator>Bahena-Alvarez, Daniel</creator><creator>López-Jiménez, Jessica</creator><creator>Molina-Hernández, Anayansi</creator><creator>Camacho-Arroyo, Ignacio</creator><creator>Díaz, Néstor Fabián</creator><general>Society for the Study of Reproduction</general><general>Oxford University Press</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>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>20210801</creationdate><title>Differential localization of serotoninergic system elements in human amniotic epithelial cells</title><author>Romero-Reyes, Jessica ; Vázquez-Martínez, Edgar Ricardo ; Bahena-Alvarez, Daniel ; López-Jiménez, Jessica ; Molina-Hernández, Anayansi ; Camacho-Arroyo, Ignacio ; Díaz, Néstor Fabián</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-b461t-7007f4236781f65c59313b84f2ccd63adfdb7868193c6444927a8a448c3b03463</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Amine oxidase (flavin-containing)</topic><topic>Amnion</topic><topic>Amnion - chemistry</topic><topic>Amnion - metabolism</topic><topic>Analysis</topic><topic>Catecholamines</topic><topic>Cytoplasm</topic><topic>embryo</topic><topic>Embryonic development</topic><topic>Epithelial cells</topic><topic>Epithelial Cells - metabolism</topic><topic>Humans</topic><topic>Immunofluorescence</topic><topic>Localization</topic><topic>Monoamine oxidase</topic><topic>neurotransmitter</topic><topic>Oct4</topic><topic>Polymerase chain reaction</topic><topic>Pregnancy</topic><topic>RESEARCH ARTICLE</topic><topic>Reverse transcription</topic><topic>RNA</topic><topic>Scientific equipment and supplies industry</topic><topic>Serotonin</topic><topic>Serotonin - metabolism</topic><topic>Serotonin transporter</topic><topic>Stem cells</topic><topic>Tryptophan</topic><topic>Tryptophan hydroxylase</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Romero-Reyes, Jessica</creatorcontrib><creatorcontrib>Vázquez-Martínez, Edgar Ricardo</creatorcontrib><creatorcontrib>Bahena-Alvarez, Daniel</creatorcontrib><creatorcontrib>López-Jiménez, Jessica</creatorcontrib><creatorcontrib>Molina-Hernández, Anayansi</creatorcontrib><creatorcontrib>Camacho-Arroyo, Ignacio</creatorcontrib><creatorcontrib>Díaz, Néstor Fabián</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>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech 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>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</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>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Biology of reproduction</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Romero-Reyes, Jessica</au><au>Vázquez-Martínez, Edgar Ricardo</au><au>Bahena-Alvarez, Daniel</au><au>López-Jiménez, Jessica</au><au>Molina-Hernández, Anayansi</au><au>Camacho-Arroyo, Ignacio</au><au>Díaz, Néstor Fabián</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Differential localization of serotoninergic system elements in human amniotic epithelial cells</atitle><jtitle>Biology of reproduction</jtitle><addtitle>Biol Reprod</addtitle><date>2021-08-01</date><risdate>2021</risdate><volume>105</volume><issue>2</issue><spage>439</spage><epage>448</epage><pages>439-448</pages><issn>0006-3363</issn><eissn>1529-7268</eissn><abstract>Serotonin or 5-hydroxytryptamine (5-HT) is a biogenic amine involved in regulating several functions, including development. However, its impact on human embryo development has been poorly studied. The present work investigated the expression and distribution of the main components of the serotoninergic system in human amniotic tissue and human amniotic epithelial cells (hAEC) in vitro, as an alternative model of early human embryo development. Amniotic membranes from full-term healthy pregnancies were used. Human amnion tissue or hAEC isolated from the amnion was processed for reverse transcription-polymerase chain reaction and immunofluorescence analyses of the main components of the serotoninergic system. We found the expression of tryptophan hydroxylase type 1 (TPH1), type 2 (TPH2), serotonin transporter (SERT), monoamine oxidase-A (MAOA), as well as HTR1D and HTR7 receptors at mRNA level in amnion tissue as well in hAEC. Interestingly, we found the presence of 5-HT in the nucleus of the cells in amnion tissue, whereas it was located in the cytoplasm of isolated hAEC. We detected TPH1, TPH2, and HTR1D receptor in both the nucleus and cytoplasm. SERT, MAOA, and HTR7 receptor were only observed in the cytoplasm. The results presented herein show, for the first time, the presence of the serotoninergic system in human amnion in vivo and in vitro. Summary sentence The results presented show the presence of the serotoninergic system in human amnion in vivo and in vitro, which opens the potential role of 5-hydroxytryptamine and the serotoninergic system in the events that occur during early human embryonic development (given the origin of the amniotic cells) in vitro. Graphical Abstract</abstract><cop>United States</cop><pub>Society for the Study of Reproduction</pub><pmid>34057176</pmid><doi>10.1093/biolre/ioab106</doi><tpages>10</tpages></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0006-3363 |
ispartof | Biology of reproduction, 2021-08, Vol.105 (2), p.439-448 |
issn | 0006-3363 1529-7268 |
language | eng |
recordid | cdi_proquest_miscellaneous_2535107866 |
source | MEDLINE; Oxford University Press Journals All Titles (1996-Current); EZB-FREE-00999 freely available EZB journals; Alma/SFX Local Collection |
subjects | Amine oxidase (flavin-containing) Amnion Amnion - chemistry Amnion - metabolism Analysis Catecholamines Cytoplasm embryo Embryonic development Epithelial cells Epithelial Cells - metabolism Humans Immunofluorescence Localization Monoamine oxidase neurotransmitter Oct4 Polymerase chain reaction Pregnancy RESEARCH ARTICLE Reverse transcription RNA Scientific equipment and supplies industry Serotonin Serotonin - metabolism Serotonin transporter Stem cells Tryptophan Tryptophan hydroxylase |
title | Differential localization of serotoninergic system elements in human amniotic epithelial cells |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-02T05%3A40%3A28IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_proqu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Differential%20localization%20of%20serotoninergic%20system%20elements%20in%20human%20amniotic%20epithelial%20cells&rft.jtitle=Biology%20of%20reproduction&rft.au=Romero-Reyes,%20Jessica&rft.date=2021-08-01&rft.volume=105&rft.issue=2&rft.spage=439&rft.epage=448&rft.pages=439-448&rft.issn=0006-3363&rft.eissn=1529-7268&rft_id=info:doi/10.1093/biolre/ioab106&rft_dat=%3Cgale_proqu%3EA701923153%3C/gale_proqu%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2560875690&rft_id=info:pmid/34057176&rft_galeid=A701923153&rft_oup_id=10.1093/biolre/ioab106&rfr_iscdi=true |