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Sexual Dimorphism in Esterified Steroid Levels in the Gastropod

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Sexual Dimorphism in Esterified Steroid Levels in the Gastropod steroids 71 (2006) 435–444 available at www.sciencedirect.com journal homepage: www.elsevier.com/locate/steroids Sexual dimorphism in esterified steroid levels in the gastropod Marisa cornuarietis: The effect of xenoandrogenic compounds Gemma Janer a, Angeliki Lyssimachou a, Jean Bachmann b,Jorg¨ Oehlmann b, Ulrike Schulte-Oehlmann b, Cinta Porte a,∗ a Environmental Chemistry Department, IIQAB-CSIC, Jordi Girona 18, 08034 Barcelona, Spain b Johann Wolfgang Goethe-University Frankfurt am Main, Department of Ecology and Evolution-Ecotoxicology, Siesmayerstr. 70, D-60054 Frankfurt, Germany article info abstract Article history: Molluscs can conjugate a variety of steroids to form fatty acid esters. In this work, the Received 16 June 2005 freshwater ramshorn snail Marisa cornuarietis was used to investigate sex differences in Received in revised form 4 January endogenous levels of esterified steroids. Testosterone and estradiol were mainly found in 2006 the esterified form in the digestive gland/gonad complex of M. cornuarietis, and males had Accepted 11 January 2006 higher levels of esterified steroids than females (4–10-fold). Additionally, the ability of sev- Published on line 17 April 2006 eral xenobiotics, namely tributyltin (TBT), methyltestosterone (MT) and fenarimol (FEN) to interfere with the esterification of testosterone and estradiol was investigated. All three Keywords: compounds induced imposex – appearance of male sexual characteristics in females. Expo- Esterification sure to TBT led to a decrease in both esterified testosterone (60–85%) and estradiol (16–53%) Testosterone in females after 100 days exposure, but had no effect on males. Exposure to FEN and MT did Estradiol not alter levels of esterified steroids in males or in females, although exposed females devel- Gastropod oped imposex after 150 days exposure. The decrease in esterified steroids by TBT could not be Imposex directly linked with a decrease in microsomal acyl-CoA:testosterone acyltransferase (ATAT) Acyl-CoA acyltransferase activity, which catalyzes the esterification of steroids. In fact, ATAT activity was marginally induced in organisms exposed to TBT for 50 days (1.3-fold), and significantly induced in males and females exposed to MT for 50 days (1.8- and 1.5-fold, respectively), whereas no effect on ATAT activity was observed after 150 days exposure. © 2006 Elsevier Inc. All rights reserved. 1. Introduction ortholog gene has been sequenced in the mollusc Aplysia cal- ifornica [7], suggesting that steroids might also function via Sex steroids, such as progesterone, testosterone and estra- interaction with steroid receptors in molluscs. In addition, diol, are present in molluscs [1], and several studies have rapid non-genomic effects of estradiol have been demon- demonstrated the ability of these organisms to synthesize sex strated in mussel neural tissue (increase in nitric oxide release steroids from precursors, such as cholesterol or pregnenolone [8]) and in mussel hemocytes (increase in calcium concen- [2–5]. Proteins with a high binding affinity for sex steroids have trations and changes in the phosphorylation of signal trans- been found in Octopus vulgaris [6], and an estrogen receptor ducers and transcription activators [9]). Although there are ∗ Corresponding author. Tel.: +34 93 4006175; fax: +34 93 2045904. E-mail address: [email protected] (C. Porte). 0039-128X/$ – see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.steroids.2006.01.012 436 steroids 71 (2006) 435–444 still important gaps of knowledge concerning both genomic Apart from these studies, there is no data available on and non-genomic actions of steroids in molluscs, the above- endogenous levels of esterified steroids in other mollusc mentioned observations are suggestive of a physiological role species and/or what kind of pollutants can interfere with the of sex steroids in these organisms. Indeed, various studies fatty acid esterification of sex steroids. Thus, this study was have indicated that steroids are involved in the control of mol- designed to further investigate the presence and levels of sex- lusc reproduction and sex differentiation. For example, estra- ual steroids (testosterone and estradiol) in the freshwater gas- diol induces the accumulation of vitellin in the gonads of the tropod Marisa cornuarietis. Free and esterified steroid levels, scallop Patinopecten yessoensis [10]; testosterone administration together with fatty acid conjugating activities, were analyzed to castrated male slugs (Euhadra prelionphala) stimulates the and potential sexual dimorphism in these parameters was production of male secondary sex characteristics [11]; and the assessed. In addition, we investigated whether steroid levels administration of testosterone to female gastropods results were modulated by exposure to xenobiotic compounds and in the development of imposex with extensive penis and vas the association with the phenomenon of imposex and other deferens formation [12,13]. In addition, steroid levels vary in biological effects. Apart from TBT,two other compounds, fena- some species of molluscs in relation to the reproductive status rimol (FEN) and methyltestosterone (MT), were selected for the [3,14,15]. study. Steroid levels within the organism are at least partially reg- FEN is a widely used fungicide that has the potential to ulated by steroidogenesis and/or biotransformation enzymes. interfere with the endocrine system through several mecha- Hydroxylation and polar conjugation (sulfation and glu- nisms. It acts both as an estrogen agonist and an androgen curonidation), which are major metabolic pathways for testos- antagonist, and it is a potent aromatase inhibitor [24]. The terone or estradiol in vertebrates, seem to play a minor role in complexity of FEN action hampers the prediction of its in vivo the metabolism of testosterone in molluscs [16,17]. Instead, effects. Recently, FEN was reported to have an antiandrogenic snails metabolize most of the testosterone into fatty acid con- effect in rats in vivo [25]. In contrast, the effects observed jugates in vivo [16]. Esterification is mediated by a microso- in exposed fathead minnow did not reflect either aromatase mal acyl-coenzyme A acyltransferase enzyme, which, in addi- inhibition or androgen receptor antagonism [26]. In the snail tion to testosterone [16], can conjugate other steroids, such Nassarius reticulatus, FEN has been shown to induce imposex as estradiol and dehydroepiandrostenedione, with fatty acids [27]. The other compound tested, MT, is a synthetic androgen [18]. with high affinity for the mammalian androgen receptor [28] Esterified steroids are not easily excreted from the organ- that has been shown to cause imposex in M. cornuarietis [29]. ism, but stored in fatty tissues. In mammalian species, they are considered potent long acting steroids because, in com- 2. Experimental parison to unconjugated steroids, they are metabolized and excreted at a very low rate [19]. Esterified steroids do not 2.1. Chemicals bind to receptors [20], but can be hydrolyzed by esterases, again liberating the active steroid [19]. Recent studies sug- Tributyltin chloride, fenarimol, methyltestosterone, testos- gest that esterification might be an important factor in reg- terone and estradiol were obtained from Sigma (Stein- ulating the levels of free hormones in molluscs. Thus, Good- heim, Germany). [4-14C]testosterone (specific activity ing and LeBlanc [15] showed that exposure to exogenous 50–60 mCi/mmol) was purchased from NEN Life Science testosterone increased the retention of testosterone as fatty Products Inc. (Boston, MA, USA). Radioimmunoassay (RIA) acid esters in Ilyanassa obsoleta, while unconjugated testos- kits for testosterone and 17␤-estradiol were obtained from terone levels did not appreciably change. Similarly, exoge- Radim (Rome, Italy). All solvents and reagents were of nously administered estradiol was extensively esterified by analytical grade, except tributyltin chloride (96%) and methyl- the mussel Mytilus galloprovincialis, whereas unconjugated testosterone (above 98%). estradiol levels remained almost unaltered [21]. The balance between conjugated and unconjugated steroids also appeared 2.2. Animals to control the variations in unconjugated steroid levels dur- ing the reproductive cycle. Thus, snails at the onset or end of Ramshorn snail, M. cornuarietis (Mollusca: Prosobranchia: the reproductive period had high levels of free testosterone Ampullariidae), is a subtropical species, originally inhabiting coincident with low levels of testosterone fatty acid esters stagnant and slow running freshwater bodies in the northern [15]. part of South America. Because ramshorn snails were used Xenobiotic compounds, such as tributyltin (TBT), have been as a biological control agent in many tropical countries for shown to interfere with the esterification of testosterone [22]. molluscs (Biomphalaria glabrata) hosting trematodes known to TBT is an organotin compound that causes imposex (impo- induce intestinal schistosomiasis, Marisa can also be found sition of male genital characters in females) in several gas- today in the Caribbean, Central and North America, Africa and tropod species at very low concentrations (few ng/L) [23]. Asia. The species is gonochoristic and oviparous, attaining a Recently, Gooding et al. [22] showed that females experimen- maximum shell diameter of up to 5 cm. Juvenile snails hatch tally exposed to 10 ng/L TBT for 3 months showed a lower from the eggs after 8–13 days and reach sexual
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