The Uptake of Ethinyl-Estradiol and Cortisol From Water by Mussels (Mytilus spp.)
Previous toxicokinetic studies have shown that mussels ( Mytilus spp.) can readily absorb the three main mammalian sex steroids, estradiol (E 2 ), testosterone (T) and progesterone (P) from water. They also have a strong ability to store E 2 and the 5α-reduced metabolites of T and P in the form of f...
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Published in | Frontiers in endocrinology (Lausanne) Vol. 12; p. 794623 |
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Main Authors | , , , |
Format | Journal Article |
Language | English |
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15.12.2021
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Abstract | Previous toxicokinetic studies have shown that mussels (
Mytilus
spp.) can readily absorb the three main mammalian sex steroids, estradiol (E
2
), testosterone (T) and progesterone (P) from water. They also have a strong ability to store E
2
and the 5α-reduced metabolites of T and P in the form of fatty acid esters. These esters were shown to have half-lives that were measured in weeks (i.e. they were not subject to fast depuration). The present study looked at the toxicokinetic profile of two other common steroids that are found in water, the potent synthetic oestrogen, (ethinyl-estradiol) (EE
2;
one of the two components of ‘the pill’), and cortisol, a natural stress steroid in vertebrates. In the first three hours of uptake, tritiated EE
2
was found to be taken up at a similar rate to tritiated E
2
. However, the levels in the water plateaued sooner than E
2
. The ability of the animals to both esterify and sulphate EE
2
was found to be much lower than E
2
, but nevertheless did still take place. After 24 h of exposure, the majority of radiolabelled EE
2
in the animals was present in the form of free steroid, contrary to E
2,
which was esterified. This metabolism was reflected in a much lower half-life (of only 15 h for EE
2
in the mussels as opposed to 8 days for E
2
and >10 days for T and P). Intriguingly, hardly any cortisol (in fact none at all in one of the experiments) was absorbed by the mussels. The implications of this finding in both toxicokinetic profiling and evolutionary significance (why cortisol might have evolved as a stress steroid in bony fishes) are discussed. |
---|---|
AbstractList | Previous toxicokinetic studies have shown that mussels (Mytilus spp.) can readily absorb the three main mammalian sex steroids, estradiol (E2), testosterone (T) and progesterone (P) from water. They also have a strong ability to store E2 and the 5α-reduced metabolites of T and P in the form of fatty acid esters. These esters were shown to have half-lives that were measured in weeks (i.e. they were not subject to fast depuration). The present study looked at the toxicokinetic profile of two other common steroids that are found in water, the potent synthetic oestrogen, (ethinyl-estradiol) (EE2; one of the two components of ‘the pill’), and cortisol, a natural stress steroid in vertebrates. In the first three hours of uptake, tritiated EE2 was found to be taken up at a similar rate to tritiated E2. However, the levels in the water plateaued sooner than E2. The ability of the animals to both esterify and sulphate EE2 was found to be much lower than E2, but nevertheless did still take place. After 24 h of exposure, the majority of radiolabelled EE2 in the animals was present in the form of free steroid, contrary to E2, which was esterified. This metabolism was reflected in a much lower half-life (of only 15 h for EE2 in the mussels as opposed to 8 days for E2 and >10 days for T and P). Intriguingly, hardly any cortisol (in fact none at all in one of the experiments) was absorbed by the mussels. The implications of this finding in both toxicokinetic profiling and evolutionary significance (why cortisol might have evolved as a stress steroid in bony fishes) are discussed. Previous toxicokinetic studies have shown that mussels ( Mytilus spp.) can readily absorb the three main mammalian sex steroids, estradiol (E 2 ), testosterone (T) and progesterone (P) from water. They also have a strong ability to store E 2 and the 5α-reduced metabolites of T and P in the form of fatty acid esters. These esters were shown to have half-lives that were measured in weeks (i.e. they were not subject to fast depuration). The present study looked at the toxicokinetic profile of two other common steroids that are found in water, the potent synthetic oestrogen, (ethinyl-estradiol) (EE 2; one of the two components of ‘the pill’), and cortisol, a natural stress steroid in vertebrates. In the first three hours of uptake, tritiated EE 2 was found to be taken up at a similar rate to tritiated E 2 . However, the levels in the water plateaued sooner than E 2 . The ability of the animals to both esterify and sulphate EE 2 was found to be much lower than E 2 , but nevertheless did still take place. After 24 h of exposure, the majority of radiolabelled EE 2 in the animals was present in the form of free steroid, contrary to E 2, which was esterified. This metabolism was reflected in a much lower half-life (of only 15 h for EE 2 in the mussels as opposed to 8 days for E 2 and >10 days for T and P). Intriguingly, hardly any cortisol (in fact none at all in one of the experiments) was absorbed by the mussels. The implications of this finding in both toxicokinetic profiling and evolutionary significance (why cortisol might have evolved as a stress steroid in bony fishes) are discussed. Previous toxicokinetic studies have shown that mussels (Mytilus spp.) can readily absorb the three main mammalian sex steroids, estradiol (E2), testosterone (T) and progesterone (P) from water. They also have a strong ability to store E2 and the 5α-reduced metabolites of T and P in the form of fatty acid esters. These esters were shown to have half-lives that were measured in weeks (i.e. they were not subject to fast depuration). The present study looked at the toxicokinetic profile of two other common steroids that are found in water, the potent synthetic oestrogen, (ethinyl-estradiol) (EE2; one of the two components of 'the pill'), and cortisol, a natural stress steroid in vertebrates. In the first three hours of uptake, tritiated EE2 was found to be taken up at a similar rate to tritiated E2. However, the levels in the water plateaued sooner than E2. The ability of the animals to both esterify and sulphate EE2 was found to be much lower than E2, but nevertheless did still take place. After 24 h of exposure, the majority of radiolabelled EE2 in the animals was present in the form of free steroid, contrary to E2, which was esterified. This metabolism was reflected in a much lower half-life (of only 15 h for EE2 in the mussels as opposed to 8 days for E2 and >10 days for T and P). Intriguingly, hardly any cortisol (in fact none at all in one of the experiments) was absorbed by the mussels. The implications of this finding in both toxicokinetic profiling and evolutionary significance (why cortisol might have evolved as a stress steroid in bony fishes) are discussed.Previous toxicokinetic studies have shown that mussels (Mytilus spp.) can readily absorb the three main mammalian sex steroids, estradiol (E2), testosterone (T) and progesterone (P) from water. They also have a strong ability to store E2 and the 5α-reduced metabolites of T and P in the form of fatty acid esters. These esters were shown to have half-lives that were measured in weeks (i.e. they were not subject to fast depuration). The present study looked at the toxicokinetic profile of two other common steroids that are found in water, the potent synthetic oestrogen, (ethinyl-estradiol) (EE2; one of the two components of 'the pill'), and cortisol, a natural stress steroid in vertebrates. In the first three hours of uptake, tritiated EE2 was found to be taken up at a similar rate to tritiated E2. However, the levels in the water plateaued sooner than E2. The ability of the animals to both esterify and sulphate EE2 was found to be much lower than E2, but nevertheless did still take place. After 24 h of exposure, the majority of radiolabelled EE2 in the animals was present in the form of free steroid, contrary to E2, which was esterified. This metabolism was reflected in a much lower half-life (of only 15 h for EE2 in the mussels as opposed to 8 days for E2 and >10 days for T and P). Intriguingly, hardly any cortisol (in fact none at all in one of the experiments) was absorbed by the mussels. The implications of this finding in both toxicokinetic profiling and evolutionary significance (why cortisol might have evolved as a stress steroid in bony fishes) are discussed. Previous toxicokinetic studies have shown that mussels ( spp.) can readily absorb the three main mammalian sex steroids, estradiol (E ), testosterone (T) and progesterone (P) from water. They also have a strong ability to store E and the 5α-reduced metabolites of T and P in the form of fatty acid esters. These esters were shown to have half-lives that were measured in weeks (i.e. they were not subject to fast depuration). The present study looked at the toxicokinetic profile of two other common steroids that are found in water, the potent synthetic oestrogen, (ethinyl-estradiol) (EE one of the two components of 'the pill'), and cortisol, a natural stress steroid in vertebrates. In the first three hours of uptake, tritiated EE was found to be taken up at a similar rate to tritiated E . However, the levels in the water plateaued sooner than E . The ability of the animals to both esterify and sulphate EE was found to be much lower than E , but nevertheless did still take place. After 24 h of exposure, the majority of radiolabelled EE in the animals was present in the form of free steroid, contrary to E which was esterified. This metabolism was reflected in a much lower half-life (of only 15 h for EE in the mussels as opposed to 8 days for E and >10 days for T and P). Intriguingly, hardly any cortisol (in fact none at all in one of the experiments) was absorbed by the mussels. The implications of this finding in both toxicokinetic profiling and evolutionary significance (why cortisol might have evolved as a stress steroid in bony fishes) are discussed. |
Author | Cousins, Alex R. O. Scott, Alexander P. Katsiadaki, Ioanna Schwarz, Tamar I. |
AuthorAffiliation | 1 Centre for Environment, Fisheries and Aquaculture Science, Weymouth Laboratory , Weymouth , United Kingdom 2 Centre for Environment, Fisheries and Aquaculture Science, Lowestoft Laboratory , Lowestoft , United Kingdom |
AuthorAffiliation_xml | – name: 2 Centre for Environment, Fisheries and Aquaculture Science, Lowestoft Laboratory , Lowestoft , United Kingdom – name: 1 Centre for Environment, Fisheries and Aquaculture Science, Weymouth Laboratory , Weymouth , United Kingdom |
Author_xml | – sequence: 1 givenname: Ioanna surname: Katsiadaki fullname: Katsiadaki, Ioanna – sequence: 2 givenname: Tamar I. surname: Schwarz fullname: Schwarz, Tamar I. – sequence: 3 givenname: Alex R. O. surname: Cousins fullname: Cousins, Alex R. O. – sequence: 4 givenname: Alexander P. surname: Scott fullname: Scott, Alexander P. |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34975764$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_1016_j_aquatox_2022_106376 crossref_primary_10_1016_j_envpol_2023_121667 crossref_primary_10_3389_fendo_2022_981564 crossref_primary_10_1152_ajpendo_00251_2024 crossref_primary_10_1002_etc_5806 crossref_primary_10_3389_fendo_2024_1458422 crossref_primary_10_3389_fendo_2022_903575 |
Cites_doi | 10.1016/j.ygcen.2018.04.005 10.1016/j.jsbmb.2017.02.016 10.101016/j.envres.102020.109316 10.1016/j.steroids.2017.05.008 10.1124/dmd.112.045583 10.2116/bunsekikagaku.50.247 10.1002/etc.4627 10.1021/es4047507 10.1201/9781003029854-8 10.1016/j.dib.2016.10.030 10.1016/j.aquatox.2014.03.004 10.1897/08-622.1 10.1111/j.0022-1112.2005.00740.x 10.1016/j.ecoenv.2013.12.032 10.1016/j.cbpc.2016.09.002 10.1007/s10646-006-0110-4 10.1111/j.0022-1112.2005.00727.x 10.1016/j.scitotenv.2020.137638 10.1007/s10646-006-0114-0 10.1002/etc.3137 10.1016/j.ygcen.2019.113226 10.1016/j.scitotenv.2021.148306 10.1016/j.steroids.2003.12.002 10.1016/j.jsbmb.2017.10.016 10.1006/gcen.2001.7630 10.1016/j.jpba.2015.09.013 10.1016/j.aquatox.2004.11.024 10.1016/j.jsbmb.2016.08.007 10.1016/j.steroids.2012.11.006 10.1016/j.mce.2020.110949 10.1016/S0147-6513(02)00039-8 10.1016/j.aquatox.2008.03.003 10.1016/j.marenvres.2021.105315 10.1016/j.envint.2007.05.003 10.1007/s10646-010-0529-5 10.1016/j.steroids.2012.08.009 |
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Keywords | cortisol ethinyl-estradiol depuration mollusk endocrine disruption steroid |
Language | English |
License | Copyright © 2021 Katsiadaki, Schwarz, Cousins and Scott. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by: Toshihiro Horiguchi, National Institute for Environmental Studies (NIES), Japan This article was submitted to Experimental Endocrinology, a section of the journal Frontiers in Endocrinology Reviewed by: Taisen Iguchi, Graduate University for Advanced Studies (Sokendai), Japan; Alice Louise Baynes, Brunel University London, United Kingdom |
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References | Brew (B21) 2020; 39 Scott (B4) 2018; 265 Ellis (B27) 2005; 67 Scott (B25) 2005; 67 Janer (B12) 2004; 69 Rohn (B24) 2012; 40 Guercia (B14) 2017; 123 Ojoghoro (B7) 2021; 792 Fernández-González (B31) 2021; 168 Schwarz (B9) 2017; 171 Schwarz (B10) 2018; 178 Hannah (B22) 2009; 28 Benfenati (B26) 2013; 1107 Borysko (B34) 2014; 103 Andrew (B33) 2010; 19 Schwarz (B8) 2017; 165 Fodor (B5) 2020; 516 Lagadic (B29) 2007; 16 Horiguchi (B6) 2020 Schwarz (B15) 2016; 9 Janer (B13) 2005; 71 Leonard (B35) 2014; 150 Fernández-González (B30) 2020; 721 Janer (B1) 2007; 16 Lu (B16) 2001; 50 Ellis (B23) 2020; 285 Segner (B28) 2003; 54 Ricciardi (B20) 2016; 35 Harris (B37) 2014; 48 Scott (B3) 2013; 78 Gooding (B11) 2001; 122 Pojana (B17) 2007; 33 Almeida (B19) 2020; 185 Leonard (B36) 2017; 191 Hallmann (B18) 2016; 117 Scott (B2) 2012; 77 Andrew (B32) 2008; 88 |
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Volume 1, Phyla Other Than Arthropoda year: 2020 ident: B6 article-title: A Critical Review of Sex Steroid Hormones and the Induction Mechanisms of Imposex in Gastropod Mollusks doi: 10.1201/9781003029854-8 – volume: 9 year: 2016 ident: B15 article-title: Data on the Rapid and High Capacity Uptake of the Vertebrate Steroid, Estradiol-17β, From Water by Blue Mussels, Mytilus Spp publication-title: Data Brief doi: 10.1016/j.dib.2016.10.030 – volume: 150 year: 2014 ident: B35 article-title: Metabolomic, Behavioral, and Reproductive Effects of the Synthetic Estrogen 17α-Ethinylestradiol on the Unionid Mussel Lampsilis fasciola publication-title: Aquat toxicol doi: 10.1016/j.aquatox.2014.03.004 – volume: 28 year: 2009 ident: B22 article-title: Exposure Assessment of 17α-Ethinylestradiol in Surface Waters of the United States and Europe publication-title: Environ Toxicol Chem doi: 10.1897/08-622.1 – volume: 67 year: 2005 ident: B27 article-title: Branchial Release of Free Cortisol and Melatonin by Rainbow Trout publication-title: J Fish Biol doi: 10.1111/j.0022-1112.2005.00740.x – volume: 103 start-page: 91 year: 2014 ident: B34 article-title: Adult Exposure to the Synthetic Hormone 17α-Ethynylestradiol Affects Offspring of the Gastropods Nassarius burchardi and Nassarius jonasii publication-title: Ecotoxicol Environ Saf doi: 10.1016/j.ecoenv.2013.12.032 – volume: 191 start-page: 14 year: 2017 ident: B36 article-title: Extending the Toxicity-Testing Paradigm for Freshwater Mussels: Assessing Chronic Reproductive Effects of the Synthetic Estrogen 17α-Ethinylestradiol on the Unionid Mussel Elliptio complanata publication-title: Comp Biochem Physiol C Toxicol Pharmacol doi: 10.1016/j.cbpc.2016.09.002 – volume: 16 year: 2007 ident: B1 article-title: Sex Steroids and Potential Mechanisms of non-Genomic Endocrine Disruption in Invertebrates publication-title: Ecotoxicology doi: 10.1007/s10646-006-0110-4 – volume: 67 start-page: 182 year: 2005 ident: B25 article-title: The Rate of Uptake of Sex Steroids From Water by Tench Tinca tinca L. @ Is Influenced by Their Affinity for Sex Steroid Binding Protein in Plasma publication-title: J Fish Biol doi: 10.1111/j.0022-1112.2005.00727.x – volume: 721 year: 2020 ident: B30 article-title: No Evidence That Vitellogenin Protein Expression is Induced in Marine Mussels After Exposure to an Estrogenic Chemical publication-title: Sci Total Environ doi: 10.1016/j.scitotenv.2020.137638 – volume: 16 start-page: 45 year: 2007 ident: B29 article-title: Endocrine Disruption in Aquatic Pulmonate Molluscs: Few Evidences, Many Challenges publication-title: Ecotoxicology doi: 10.1007/s10646-006-0114-0 – volume: 35 year: 2016 ident: B20 article-title: Bioconcentration and Depuration of 14C-Labeled 17α-Ethinyl Estradiol and 4-Nonylphenol in Individual Organs of the Marine Bivalve, Mytilus edulis L publication-title: Environ Toxicol Chem doi: 10.1002/etc.3137 – volume: 285 year: 2020 ident: B23 article-title: Immunoassays are Not Immune to Errors: Examples From Two Studies of Steroid Output From Freshwater Trout Farms publication-title: Gen Comp Endocrinol doi: 10.1016/j.ygcen.2019.113226 – volume: 792 year: 2021 ident: B7 article-title: Steroid Hormones in the Aquatic Environment publication-title: Sci Total Environ doi: 10.1016/j.scitotenv.2021.148306 – volume: 69 year: 2004 ident: B12 article-title: Esterification of Vertebrate-Type Steroids in the Eastern Oyster (Crassostrea virginica) publication-title: Steroids doi: 10.1016/j.steroids.2003.12.002 – volume: 178 start-page: 13 year: 2018 ident: B10 article-title: Uptake and Metabolism of Water-Borne Progesterone by the Mussel, Mytilus Spp. (Mollusca) publication-title: J Steroid Biochem Mol Biol doi: 10.1016/j.jsbmb.2017.10.016 – volume: 122 year: 2001 ident: B11 article-title: Biotransformation and Disposition of Testosterone in the Eastern Mud Snail Ilyanassa obsoleta publication-title: Gen Comp Endocrinol doi: 10.1006/gcen.2001.7630 – volume: 117 year: 2016 ident: B18 article-title: LC-MS Measurement of Free Steroids in Mussels (Mytilus trossulus) From the Southern Baltic Sea publication-title: J Pharm Biomed doi: 10.1016/j.jpba.2015.09.013 – volume: 71 year: 2005 ident: B13 article-title: Testosterone Conjugating Activities in Invertebrates: Are They Targets for Endocrine Disruptors publication-title: Aquat Toxicol doi: 10.1016/j.aquatox.2004.11.024 – volume: 165 year: 2017 ident: B8 article-title: Mussels (Mytilus Spp.) Display an Ability for Rapid and High Capacity Uptake of the Vertebrate Steroid, Estradiol-17b From Water publication-title: J Steroid Biochem Mol Biol doi: 10.1016/j.jsbmb.2016.08.007 – volume: 78 year: 2013 ident: B3 article-title: Do Mollusks Use Vertebrate Sex Steroids as Reproductive Hormones? II. Critical Review of the Evidence That Steroids Have Biological Effects publication-title: Steroids doi: 10.1016/j.steroids.2012.11.006 – volume: 516 year: 2020 ident: B5 article-title: A Critical Evaluation of Some of the Recent So-Called ‘Evidence’ for the Involvement of Vertebrate-Type Sex Steroids in the Reproduction of Mollusks publication-title: Mol Cell Endocrinol doi: 10.1016/j.mce.2020.110949 – volume: 54 year: 2003 ident: B28 article-title: Identification of Endocrine-Disrupting Effects in Aquatic Vertebrates and Invertebrates: Report From the European IDEA Project publication-title: Ecotoxicol Environ Saf doi: 10.1016/S0147-6513(02)00039-8 – volume: 88 start-page: 39 year: 2008 ident: B32 article-title: Effects of 4-Nonylphenol and 17 α-Ethynylestradiol Exposure in the Sydney Rock Oyster, Saccostrea glomerata: Vitellogenin Induction and Gonadal Development publication-title: Aquat Toxicol doi: 10.1016/j.aquatox.2008.03.003 – volume: 168 year: 2021 ident: B31 article-title: Vitellogenin Gene Expression in Marine Mussels Exposed to Ethinylestradiol: No Induction at the Transcriptional Level publication-title: Mar Environ Res doi: 10.1016/j.marenvres.2021.105315 – volume: 33 year: 2007 ident: B17 article-title: Natural and Synthetic Endocrine Disrupting Compounds (EDCs) in Water, Sediment and Biota of a Coastal Lagoon publication-title: Environ Int doi: 10.1016/j.envint.2007.05.003 – volume: 19 year: 2010 ident: B33 article-title: Exposure to 17α-Ethynylestradiol Causes Dose and Temporally Dependent Changes in Intersex, Females and Vitellogenin Production in the Sydney Rock Oyster publication-title: Ecotoxicology doi: 10.1007/s10646-010-0529-5 – volume: 1107 year: 2013 ident: B26 article-title: VEGA-QSAR: AI Inside a Platform for Predictive Toxicology publication-title: CEUR Workshop Proc – volume: 77 year: 2012 ident: B2 article-title: Do Mollusks Use Vertebrate Sex Steroids as Reproductive Hormones? Part I. Critical Appraisal of the Evidence for the Presence, Biosynthesis and Uptake of Steroids publication-title: Steroids doi: 10.1016/j.steroids.2012.08.009 |
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Snippet | Previous toxicokinetic studies have shown that mussels (
Mytilus
spp.) can readily absorb the three main mammalian sex steroids, estradiol (E
2
), testosterone... Previous toxicokinetic studies have shown that mussels ( spp.) can readily absorb the three main mammalian sex steroids, estradiol (E ), testosterone (T) and... Previous toxicokinetic studies have shown that mussels (Mytilus spp.) can readily absorb the three main mammalian sex steroids, estradiol (E2), testosterone... |
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SubjectTerms | Animals cortisol depuration endocrine disruption Endocrinology Estrogens - analysis Estrogens - metabolism Ethinyl Estradiol - analysis Ethinyl Estradiol - metabolism ethinyl-estradiol Hydrocortisone - analysis Hydrocortisone - metabolism Metabolic Clearance Rate - physiology mollusk Mytilus steroid Water - analysis Water - metabolism Water Pollutants, Chemical - analysis Water Pollutants, Chemical - metabolism |
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Title | The Uptake of Ethinyl-Estradiol and Cortisol From Water by Mussels (Mytilus spp.) |
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