Academic journal article Environmental Health Perspectives

The Biocide Tributyltin Reduces the Accumulation of Testosterone as Fatty Acid Esters in the Mud Snail (Ilyanassa Obsoleta). (Research)

Academic journal article Environmental Health Perspectives

The Biocide Tributyltin Reduces the Accumulation of Testosterone as Fatty Acid Esters in the Mud Snail (Ilyanassa Obsoleta). (Research)

Article excerpt

Imposex, the development of male sex characteristics by female gonochoristic snails, has been documented globally and is causally associated with exposure in the ubiquitous environmental contaminant tributyltin (TBT). Elevated testosterone levels in snails also are associated with TBT, and direct exposure to testosterone has been shown to cause imposex. We discovered previously that the mud snail (Ilyanassa obsoleta) biotransforms and retains excess testosterone primarily as fatty acid esters. The purpose of this study was to determine whether TBT interferes with the esterification of testosterone, resulting in the elevated free (unesterified) testosterone levels associated with imposex. Exposure of snails to environmentally relevant concentrations of TBT ([greater than or equal to] 1.0 ng/L as tin) significantly increased the incidence of imposex. Total (free + esterified) testosterone levels in snails were not altered by TBT; however, free testosterone levels increased with increasing exposure concentration of TBT. TBT-exposed snails were given [[sup.14]C]testosterone to measure the production of [[sup.14]C]testosterone-fatty acid esters. The production of testosterone-fatty acid esters decreased with increasing exposure concentration of TBT. These results indicate that TBT elevates free testosterone levels in snails by decreasing the production or retention of testosterone-fatty acid esters. These findings were confirmed among field-sampled snails where individuals collected from a high-tin-affected site exhibited a greater incidence of imposex, higher free testosterone levels, and lower testosterone-fatty acid ester levels when compared with individuals sampled from a low-tin-affected site. Decreased testosterone-fatty acid esterification among TBT-treated snails was not caused by direct inhibition of the acyl coenzyme A:testosterone acyltransferase (ATAT) enzyme responsible for testosterone esterification, nor by suppressed ATAT protein expression. The target of TBT may be a co-contributor to the testosterone fatty esterification process or a factor in the enhanced hydrolysis of the testosterone-fatty acid pool. Key words: acyltransferase, fatty acid esters, Ilyanassa obsoleta, imposex, invertebrate endocrinology, mud snail, testosterone, tributyltin.

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Tributyltin (TBT) is a ubiquitous contaminant in the marine environment that causes a pseudohermaphroditic condition known as imposex in female prosobranch gastropods. Imposex is characterized by the presence of a penis and/or vas deferens in females and has been identified in over 140 species of snails worldwide (Matthiessen et al. 1999). Testosterone is reportedly elevated in imposex individuals and has been causally implicated in the occurrence of this disorder (Bettin et al. 1996; Spooner et al. 1991). Marine prosobranch gastropods are extremely sensitive to TBT contamination, and imposex can be elicited in some species at concentrations of < 1 ng tin/L (Bryan et al. 1987; Gibbs et al. 1988). The increase in testosterone titers with TBT exposure has been attributed both to the inhibition of the aromatase enzyme (CYP19A) (Oehlmann and Bettin 1996; Spooner et al. 1991) and a decrease in the metabolic elimination of testosterone as sulfate conjugates (Ronis and Mason 1996).

The aromatase inhibition hypothesis was developed in response to the observation that testosterone levels were significantly elevated in TBT-exposed dog whelks (Nucella lapillus) when compared with controls (Spooner et al. 1991). Increases in testosterone levels following TBT exposure were proposed to be caused by a change in the estradiol:testosterone ratio resulting from the direct inhibition of aromatase by TBT. However, TBT exposure had no effect on estradiol levels in these experiments (Spooner et al. 1991). Although the inhibition of aromatase by TBT remains a possible mechanism of imposex, we are not aware of any direct evidence that TBT inhibits aromatase at environmentally relevant concentrations. …

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