Uptake and metabolism of water-borne progesterone by the mussel, Mytilus spp. (Mollusca)

Schwarz, Tamar; Katsiadaki, Ioanna; Maskrey, Benjamin H.; Scott, A. P.

doi:10.1016/j.jsbmb.2017.10.016

Cited by 17 publications

(20 citation statements)

References 46 publications

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“…The estrogen content in tissues decreased in autumn together with a temperature decrease. The highest level of estrogen in mussel tissues found in summer is most likely related not to an increased efficiency of steroidogenesis, but rather to efficient uptake of steroids from the ambient environment as it was already proved by various studies including our own (Schwarz et al, 2017a, 2017b, 2018; Smolarz et al, 2018). Active steroidogenesis occurs only in spring when the level of sex steroids in the ambient environment is low.…”

Section: Discussionsupporting

confidence: 64%

“…Latest studies report that bivalves from genus Mytilidae are able to uptake large amounts of progesterone (Schwarz et al, 2018), testosterone (Schwarz et al, 2017b), and 17β-estradiol (Schwarz et al, 2017a) from the ambient environment. This high steroids uptake potential was also confirmed in our study with A- 13 C 3 and T- 13 C 3 detected in mussel tissues after exposure to labeled substrate.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Aromatisation of steroids in the bivalveMytilus trossulus

Hallmann

Konieczna

Świeżak

et al. 2019

PeerJ

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In this study, we demonstrated the presence of the enzymatic complex able to perform aromatization (estrogen synthesis) in both, the microsomal and mitochondrial fractions of gills and gonads from Mytilus trossulus. Based on in vitro experiments, we highlighted the importance of temperature as the limiting factor of aromatisation efficiency (AE) in mussels. After testing range of temperatures (4–23 °C), the highest AE was found during incubation at 8 °C and pH 7.6 (41.66 pmol/h/mg protein in gills and 58.37 pmol/h/mg protein in gonads). The results were confirmed during field studies where the most efficient aromatisation occurred in bivalves collected in spring while the least effective in those collected in winter. During in vitro studies, AE turned out to be more intensive in female gonads than in male gonads. The process was also more intensive in mitochondrial fraction than in microsomal one (62.97 pmol/h/mg protein in male gills and 73.94 pmol/h/mg protein in female gonads). Enzymatic complex (aromatase-like enzyme) catalysing aromatisation in mussels was found to be insensitive to inhibitory effect of selective inhibitors of mammalian aromatase such as letrozole and anastrazole, suggesting its different structure from vertebrate aromatase. Further in vivo studies using 13C-labeled steroids at 8 °C temperature window confirmed that bivalves are able to uptake testosterone and androstenedione from the ambient environment and metabolise them to estrone and 17β-estradiol thus confirming endogenous estrogen’ synthesis.

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Section: Discussionsupporting

confidence: 64%

Section: Discussionmentioning

confidence: 99%

Aromatisation of steroids in the bivalveMytilus trossulus

Hallmann

Konieczna

Świeżak

et al. 2019

PeerJ

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show abstract

“…Latest studies report that bivalves from genus Mytilidae are able to uptake large amounts of progesterone (Schwarz et al, 2018), testosterone (Schwarz et al, 2017b) and 17β-estradiol (Schwarz et al, 2017a) from the ambient environment. This high steroids uptake potential was also confirmed in our study with A-13 C 3 and T-13 C 3 detected in mussel tissues after exposure to labelled substrate.…”

Section: Discussionmentioning

confidence: 99%

Peer Review #2 of "Aromatisation of steroids in the bivalve Mytilus trossulus (v0.1)"

Minier¹

2019

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In this study, we demonstrated the presence of the enzymatic complex able to perform aromatization (estrogen synthesis) in both, the microsomal and mitochondrial fractions of gills and gonads from Mytilus trossulus. Based on in vitro experiments, we highlighted the importance of temperature as the limiting factor of aromatisation efficiency (AE) in mussels. After testing range of temperatures (4°C-23°C), the highest AE was found during incubation at 8°C and pH 7.6 (41.66 pmol/h/mg protein in gills and 58.37 pmol/h/mg protein in gonads). The results were confirmed during field studies where the most efficient aromatisation occurred in bivalves collected in spring while the least effective in those collected in winter. During in vitro studies, AE turned out to be more intensive in female gonads than in male gonads. The process was also more intensive in mitochondrial fraction than in microsomal one (62.97 pmol/h/mg protein in male gills and 73.94 pmol/h/mg protein in female gonads). Enzymatic complex (aromatase-like enzyme) catalysing aromatisation in mussels was found to be insensitive to inhibitory effect of selective inhibitors of mammalian aromatase such as letrozole and anastrazole, suggesting its different structure from vertebrate aromatase. Further in vivo studies using 13 C-labelled steroids at 8°C temperature window confirmed that bivalves are able to uptake testosterone and androstenedione from the ambient environment and metabolise them to estrone and 17β-estradiol thus confirming endogenous estrogen' synthesis.

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“…Sex steroids may play a functional role in reproduction in some molluscs, as demonstrated by sex reversal and induction of vitellin-like protein in E2-injected bivalves (Mori et al ., 1969; Blaise et al ., 1999; Osada et al ., 2003), correlations between steroid titres and gonad development in clams and mussels (Lafont & Mathieu, 2007), and penis development in testosterone-treated female snails (Bettin et al ., 1996). Indeed, the presence of steroid hormones (and other non-steroidal EDCs) in invertebrate field samples now seems incontrovertible (Janer & Porte, 2007; Scott, 2018), though evidence of an endogenous biosynthetic pathway, involvement in reproduction and their mode of action in terms of ED is equivocal: steroid receptors – present, for example, in molluscs – have still to be shown to be active in mediating steroid action (Matthiessen, 2008). There is, however, growing evidence that marine invertebrates are capable of accumulating hormones and their mimics from their surrounding milieu.…”

Section: Indigenous or Exogenous Hormones And Their Mimics? Bioaccumumentioning

confidence: 99%

“…Reviewing the evidence from various taxa, Scott (2018) concluded that the ability to bioaccumulate steroids (including E2, testosterone and progesterone) was a more likely explanation for their presence and impact in invertebrate tissues than endogenous hormonal involvement in control of reproduction – questioning the possibility of invertebrates acting as surrogates of vertebrate-style endocrine disruption. The significance of steroidal burdens in invertebrates is further confounded by the possibility of transformations within both the organism itself or by other aquatic fauna and flora in the diet, including sediment.…”

Section: Indigenous or Exogenous Hormones And Their Mimics? Bioaccumumentioning

confidence: 99%

Endocrine disruption and altered sexual development in aquatic organisms: an invertebrate perspective

Langston

2020

J. Mar. Biol. Ass.

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Contaminants causing sex-altering, endocrine disrupting-like (ED) effects, or otherwise influencing reproduction, have been of growing concern to humans for more than 50 years. They have also been a perturbing, though less well-studied, phenomenon in marine organisms, following the recognition of tributyltin (TBT)-induced imposex and population extinctions in (neo)gastropods in the 1970s. Whilst ED impacts in mammals and fish are characterized by mimicry or antagonism of endogenous hormones by environmental contaminants (acting through Nuclear Receptors which are present in all metazoans) much less is known regarding pathways to effects in invertebrates. Despite the absence of a defined steroidal/mechanistic component, the extent, severity and widespread nature of ED-like manifestations and altered sexual characteristics observed in marine invertebrates gives rise to comparable concerns, and have been a long-term component of the MBA's research remit. The manifestations seen in sensitive taxa such as molluscs and crustaceans confirm they are valuable indicators of environmental quality, and should be exploited in this capacity whilst we seek to understand the pervasiveness and underlying mechanisms. In so doing, invertebrate indicators address aims of organizations, such as the EEA, OECD, UNEP and WHO, charged with management and monitoring of chemicals and ensuring that adverse effects on humans and the environment are minimized (Bergman et al., 2013). In view of the recent general declines in marine biodiversity, and the potential contribution of ED-like phenomena, safeguarding against deleterious effects through increased research which links pollutant exposure with reproductive dysfunction among invertebrates, is seen as a high priority.

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Uptake and metabolism of water-borne progesterone by the mussel, Mytilus spp. (Mollusca)

Cited by 17 publications

References 46 publications

Aromatisation of steroids in the bivalveMytilus trossulus

Aromatisation of steroids in the bivalveMytilus trossulus

Peer Review #2 of "Aromatisation of steroids in the bivalve Mytilus trossulus (v0.1)"

Endocrine disruption and altered sexual development in aquatic organisms: an invertebrate perspective

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