Transcriptomics and in vivo tests reveal novel mechanisms underlying endocrine disruption in an ecological sentinel, Nucella lapillus

Anthropogenic endocrine disruptors now contaminate all environments globally, with concomitant deleterious effects across diverse taxa. While most studies on endocrine disruption (ED) have focused on vertebrates, the superimposition of male sexual characteristics in the female dogwhelk, Nucella lapi...

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Published in:Molecular Ecology
Main Authors: Pascoal, Sónia, Carvalho, Gary, Vasieva, Olga, Hughes, Roger, Cossins, Andrew, Fang, Yongxiang, Ashelford, Kevin, Olohan, Lisa, Barroso, Carlos, Mendo, Sónia, Creer, Simon
Format: Article in Journal/Newspaper
Language:English
Published: Wiley 2013
Subjects:
Online Access:http://hdl.handle.net/10773/24611
https://doi.org/10.1111/mec.12137
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spelling ftria:oai:ria.ua.pt:10773/24611 2023-05-15T18:49:53+02:00 Transcriptomics and in vivo tests reveal novel mechanisms underlying endocrine disruption in an ecological sentinel, Nucella lapillus Pascoal, Sónia Carvalho, Gary Vasieva, Olga Hughes, Roger Cossins, Andrew Fang, Yongxiang Ashelford, Kevin Olohan, Lisa Barroso, Carlos Mendo, Sónia Creer, Simon 2013 http://hdl.handle.net/10773/24611 https://doi.org/10.1111/mec.12137 eng eng Wiley info:eu-repo/grantAgreement/FCT/SFRH/SFRH%2FBD%2F27711%2F2006/PT 0962-1083 http://hdl.handle.net/10773/24611 doi:10.1111/mec.12137 1365-294X restrictedAccess Nucella lapillus PPAR signalling pathways Roche 454 transcriptome sequencing Endocrine disruption Gene-environment interactions High-density oligoarray Imposex mechanism article 2013 ftria https://doi.org/10.1111/mec.12137 2022-05-25T18:37:04Z Anthropogenic endocrine disruptors now contaminate all environments globally, with concomitant deleterious effects across diverse taxa. While most studies on endocrine disruption (ED) have focused on vertebrates, the superimposition of male sexual characteristics in the female dogwhelk, Nucella lapillus (imposex), caused by organotins, provides one of the most clearcut ecological examples of anthropogenically induced ED in aquatic ecosystems. To identify the underpinning mechanisms of imposex for this 'nonmodel' species, we combined Roche 454 pyrosequencing with custom oligoarray fabrication inexpensively to both generate gene models and identify those responding to chronic tributyltin (TBT) treatment. The results supported the involvement of steroid, neuroendocrine peptide hormone dysfunction and retinoid mechanisms, but suggested additionally the involvement of putative peroxisome proliferator-activated receptor (PPAR) pathways. Application of rosiglitazone, a well-known vertebrate PPARγ ligand, to dogwhelks induced imposex in the absence of TBT. Thus, while TBT-induced imposex is linked to the induction of many genes and has a complex phenotype, it is likely also to be driven by PPAR-responsive pathways, hitherto not described in invertebrates. Our findings provide further evidence for a common signalling pathway between invertebrate and vertebrate species that has previously been overlooked in the study of endocrine disruption. The authors would like to thank Prof. Neil Hall, Dr Margaret Hughes and Dr Delphine Lallias for technical advice. We also acknowledge the long-term support of NERC at both Bangor and Liverpool. This work was supported by Fundação para a Ciência e a Tecnologia (FCT) Ph.D. grant SFRH/BD/27711/ 2006 awarded to Sonia Pascoal and by Natural Environment Research Council Molecular Genetics Facility (NERC MGF) grant 294 awarded to Simon Creer. published Article in Journal/Newspaper Dogwhelk Nucella lapillus Repositório Institucional da Universidade de Aveiro (RIA) Sonia ENVELOPE(-63.485,-63.485,-65.087,-65.087) Molecular Ecology 22 6 1589 1608
institution Open Polar
collection Repositório Institucional da Universidade de Aveiro (RIA)
op_collection_id ftria
language English
topic Nucella lapillus
PPAR signalling pathways
Roche 454 transcriptome sequencing
Endocrine disruption
Gene-environment interactions
High-density oligoarray
Imposex mechanism
spellingShingle Nucella lapillus
PPAR signalling pathways
Roche 454 transcriptome sequencing
Endocrine disruption
Gene-environment interactions
High-density oligoarray
Imposex mechanism
Pascoal, Sónia
Carvalho, Gary
Vasieva, Olga
Hughes, Roger
Cossins, Andrew
Fang, Yongxiang
Ashelford, Kevin
Olohan, Lisa
Barroso, Carlos
Mendo, Sónia
Creer, Simon
Transcriptomics and in vivo tests reveal novel mechanisms underlying endocrine disruption in an ecological sentinel, Nucella lapillus
topic_facet Nucella lapillus
PPAR signalling pathways
Roche 454 transcriptome sequencing
Endocrine disruption
Gene-environment interactions
High-density oligoarray
Imposex mechanism
description Anthropogenic endocrine disruptors now contaminate all environments globally, with concomitant deleterious effects across diverse taxa. While most studies on endocrine disruption (ED) have focused on vertebrates, the superimposition of male sexual characteristics in the female dogwhelk, Nucella lapillus (imposex), caused by organotins, provides one of the most clearcut ecological examples of anthropogenically induced ED in aquatic ecosystems. To identify the underpinning mechanisms of imposex for this 'nonmodel' species, we combined Roche 454 pyrosequencing with custom oligoarray fabrication inexpensively to both generate gene models and identify those responding to chronic tributyltin (TBT) treatment. The results supported the involvement of steroid, neuroendocrine peptide hormone dysfunction and retinoid mechanisms, but suggested additionally the involvement of putative peroxisome proliferator-activated receptor (PPAR) pathways. Application of rosiglitazone, a well-known vertebrate PPARγ ligand, to dogwhelks induced imposex in the absence of TBT. Thus, while TBT-induced imposex is linked to the induction of many genes and has a complex phenotype, it is likely also to be driven by PPAR-responsive pathways, hitherto not described in invertebrates. Our findings provide further evidence for a common signalling pathway between invertebrate and vertebrate species that has previously been overlooked in the study of endocrine disruption. The authors would like to thank Prof. Neil Hall, Dr Margaret Hughes and Dr Delphine Lallias for technical advice. We also acknowledge the long-term support of NERC at both Bangor and Liverpool. This work was supported by Fundação para a Ciência e a Tecnologia (FCT) Ph.D. grant SFRH/BD/27711/ 2006 awarded to Sonia Pascoal and by Natural Environment Research Council Molecular Genetics Facility (NERC MGF) grant 294 awarded to Simon Creer. published
format Article in Journal/Newspaper
author Pascoal, Sónia
Carvalho, Gary
Vasieva, Olga
Hughes, Roger
Cossins, Andrew
Fang, Yongxiang
Ashelford, Kevin
Olohan, Lisa
Barroso, Carlos
Mendo, Sónia
Creer, Simon
author_facet Pascoal, Sónia
Carvalho, Gary
Vasieva, Olga
Hughes, Roger
Cossins, Andrew
Fang, Yongxiang
Ashelford, Kevin
Olohan, Lisa
Barroso, Carlos
Mendo, Sónia
Creer, Simon
author_sort Pascoal, Sónia
title Transcriptomics and in vivo tests reveal novel mechanisms underlying endocrine disruption in an ecological sentinel, Nucella lapillus
title_short Transcriptomics and in vivo tests reveal novel mechanisms underlying endocrine disruption in an ecological sentinel, Nucella lapillus
title_full Transcriptomics and in vivo tests reveal novel mechanisms underlying endocrine disruption in an ecological sentinel, Nucella lapillus
title_fullStr Transcriptomics and in vivo tests reveal novel mechanisms underlying endocrine disruption in an ecological sentinel, Nucella lapillus
title_full_unstemmed Transcriptomics and in vivo tests reveal novel mechanisms underlying endocrine disruption in an ecological sentinel, Nucella lapillus
title_sort transcriptomics and in vivo tests reveal novel mechanisms underlying endocrine disruption in an ecological sentinel, nucella lapillus
publisher Wiley
publishDate 2013
url http://hdl.handle.net/10773/24611
https://doi.org/10.1111/mec.12137
long_lat ENVELOPE(-63.485,-63.485,-65.087,-65.087)
geographic Sonia
geographic_facet Sonia
genre Dogwhelk
Nucella lapillus
genre_facet Dogwhelk
Nucella lapillus
op_relation info:eu-repo/grantAgreement/FCT/SFRH/SFRH%2FBD%2F27711%2F2006/PT
0962-1083
http://hdl.handle.net/10773/24611
doi:10.1111/mec.12137
1365-294X
op_rights restrictedAccess
op_doi https://doi.org/10.1111/mec.12137
container_title Molecular Ecology
container_volume 22
container_issue 6
container_start_page 1589
op_container_end_page 1608
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