Estrogen therapy offsets thermal impairment of vitellogenesis, but not zonagenesis, in maiden spawning female Atlantic salmon (Salmo salar)

In female Atlantic salmon (Salmo salar), exposure to warm summer temperatures causes a reduction in plasma 17β-estradiol (E2), which impairs downstream vitellogenesis and zonagenesis, and reduces egg fertility and embryo survival. The aim of the present study was to determine whether E2-treatment co...

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Published in:PeerJ
Main Authors: Kelli Anderson, Ned Pankhurst, Harry King, Abigail Elizur
Format: Article in Journal/Newspaper
Language:English
Published: PeerJ Inc. 2017
Subjects:
R
Online Access:https://doi.org/10.7717/peerj.3897
https://doaj.org/article/fc73e9f7a93844d0939bf464ab70fb5f
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spelling ftdoajarticles:oai:doaj.org/article:fc73e9f7a93844d0939bf464ab70fb5f 2024-01-07T09:42:14+01:00 Estrogen therapy offsets thermal impairment of vitellogenesis, but not zonagenesis, in maiden spawning female Atlantic salmon (Salmo salar) Kelli Anderson Ned Pankhurst Harry King Abigail Elizur 2017-11-01T00:00:00Z https://doi.org/10.7717/peerj.3897 https://doaj.org/article/fc73e9f7a93844d0939bf464ab70fb5f EN eng PeerJ Inc. https://peerj.com/articles/3897.pdf https://peerj.com/articles/3897/ https://doaj.org/toc/2167-8359 doi:10.7717/peerj.3897 2167-8359 https://doaj.org/article/fc73e9f7a93844d0939bf464ab70fb5f PeerJ, Vol 5, p e3897 (2017) Gene expression Temperature Salmon Ovarian steroidogenesis Climate change Aquaculture Medicine R Biology (General) QH301-705.5 article 2017 ftdoajarticles https://doi.org/10.7717/peerj.3897 2023-12-10T01:49:45Z In female Atlantic salmon (Salmo salar), exposure to warm summer temperatures causes a reduction in plasma 17β-estradiol (E2), which impairs downstream vitellogenesis and zonagenesis, and reduces egg fertility and embryo survival. The aim of the present study was to determine whether E2-treatment could offset thermal impairment of endocrine function and maintain egg quality in maiden (first-time-spawning) S. salar reared at 22 °C. Treatment with E2 at 22 °C stimulated vitellogenin (vtg) gene expression and subsequent protein synthesis which promoted oocyte growth and increased egg size relative to untreated fish at 14 and 22 °C. However, E2-treatment at 22 °C was not associated with an increase in egg fertility and embryo survival relative to untreated fish at 22 °C, despite the positive effects of E2-treatment on vitellogenesis and oocyte growth. As there was no evidence to suggest that the estrogen receptor alpha expression was suppressed by high temperature, this could be due to the lack of stimulation on zonagenesis by E2-treatment observed at high temperature during oocyte development. Our results demonstrate that treatment with E2 is not able to maintain zonagenesis or egg quality in maiden S. salar at high temperature, even when vtg gene expression, protein synthesis and subsequent oocyte growth is promoted. This implies that the mechanisms regulating zonagenesis, but not vitellogenesis are impaired at elevated temperature in female S. salar broodstock, and highlights the remarkable complexity of thermally induced endocrine disruption in fish. Article in Journal/Newspaper Atlantic salmon Salmo salar Directory of Open Access Journals: DOAJ Articles PeerJ 5 e3897
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Gene expression
Temperature
Salmon
Ovarian steroidogenesis
Climate change
Aquaculture
Medicine
R
Biology (General)
QH301-705.5
spellingShingle Gene expression
Temperature
Salmon
Ovarian steroidogenesis
Climate change
Aquaculture
Medicine
R
Biology (General)
QH301-705.5
Kelli Anderson
Ned Pankhurst
Harry King
Abigail Elizur
Estrogen therapy offsets thermal impairment of vitellogenesis, but not zonagenesis, in maiden spawning female Atlantic salmon (Salmo salar)
topic_facet Gene expression
Temperature
Salmon
Ovarian steroidogenesis
Climate change
Aquaculture
Medicine
R
Biology (General)
QH301-705.5
description In female Atlantic salmon (Salmo salar), exposure to warm summer temperatures causes a reduction in plasma 17β-estradiol (E2), which impairs downstream vitellogenesis and zonagenesis, and reduces egg fertility and embryo survival. The aim of the present study was to determine whether E2-treatment could offset thermal impairment of endocrine function and maintain egg quality in maiden (first-time-spawning) S. salar reared at 22 °C. Treatment with E2 at 22 °C stimulated vitellogenin (vtg) gene expression and subsequent protein synthesis which promoted oocyte growth and increased egg size relative to untreated fish at 14 and 22 °C. However, E2-treatment at 22 °C was not associated with an increase in egg fertility and embryo survival relative to untreated fish at 22 °C, despite the positive effects of E2-treatment on vitellogenesis and oocyte growth. As there was no evidence to suggest that the estrogen receptor alpha expression was suppressed by high temperature, this could be due to the lack of stimulation on zonagenesis by E2-treatment observed at high temperature during oocyte development. Our results demonstrate that treatment with E2 is not able to maintain zonagenesis or egg quality in maiden S. salar at high temperature, even when vtg gene expression, protein synthesis and subsequent oocyte growth is promoted. This implies that the mechanisms regulating zonagenesis, but not vitellogenesis are impaired at elevated temperature in female S. salar broodstock, and highlights the remarkable complexity of thermally induced endocrine disruption in fish.
format Article in Journal/Newspaper
author Kelli Anderson
Ned Pankhurst
Harry King
Abigail Elizur
author_facet Kelli Anderson
Ned Pankhurst
Harry King
Abigail Elizur
author_sort Kelli Anderson
title Estrogen therapy offsets thermal impairment of vitellogenesis, but not zonagenesis, in maiden spawning female Atlantic salmon (Salmo salar)
title_short Estrogen therapy offsets thermal impairment of vitellogenesis, but not zonagenesis, in maiden spawning female Atlantic salmon (Salmo salar)
title_full Estrogen therapy offsets thermal impairment of vitellogenesis, but not zonagenesis, in maiden spawning female Atlantic salmon (Salmo salar)
title_fullStr Estrogen therapy offsets thermal impairment of vitellogenesis, but not zonagenesis, in maiden spawning female Atlantic salmon (Salmo salar)
title_full_unstemmed Estrogen therapy offsets thermal impairment of vitellogenesis, but not zonagenesis, in maiden spawning female Atlantic salmon (Salmo salar)
title_sort estrogen therapy offsets thermal impairment of vitellogenesis, but not zonagenesis, in maiden spawning female atlantic salmon (salmo salar)
publisher PeerJ Inc.
publishDate 2017
url https://doi.org/10.7717/peerj.3897
https://doaj.org/article/fc73e9f7a93844d0939bf464ab70fb5f
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source PeerJ, Vol 5, p e3897 (2017)
op_relation https://peerj.com/articles/3897.pdf
https://peerj.com/articles/3897/
https://doaj.org/toc/2167-8359
doi:10.7717/peerj.3897
2167-8359
https://doaj.org/article/fc73e9f7a93844d0939bf464ab70fb5f
op_doi https://doi.org/10.7717/peerj.3897
container_title PeerJ
container_volume 5
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