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Sex steroids and potential mechanisms of non-genomic endocrine disruption in invertebrates

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Abstract

The review reports on the presence and metabolism of sex steroids in several invertebrate species and provides detailed information on possible mechanisms of endocrine disruption other than the interaction with nuclear receptors. The presence of most vertebrate sex steroids in invertebrate tissues has been demonstrated by liquid or gas chromatography coupled to mass spectrometry. In addition, enzymatic pathways involved in the steroidogenic pathway have been described in at least some invertebrate phyla. Some endocrine disruptors induce alterations in these metabolic pathways and might lead to changes in steroid levels. Growing evidence suggests that estradiol can act through non-genomic pathways in molluscs, and that xenobiotics can as well interfere in these signalling casacades. In spite of these recent advances, most question marks on the action and function of sex steroids in invertebrates remain to be answered.

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References

  • Baker ME (1997) Steroid receptor phylogeny and vertebrate origins. Mol Cell Endocrinol 135:101–107

    CAS  Google Scholar 

  • Baker ME (2001a) Adrenal and sex steroid receptor evolution: environmental implications. J Mol Endocrinol 26(2):119–125

    CAS  Google Scholar 

  • Baker ME (2001b) Evolution of 17β-hydroxysteroid dehydrogenases and their role in androgen, estrogen and retinoid action. Mol Cell Endocrinol 171:211–215

    CAS  Google Scholar 

  • Baker ME (2003) Evolution of adrenal and sex steroid action in vertebrates: a ligand-based mechanism for complexity. Bioessays 25:396–400

    CAS  Google Scholar 

  • Baldwin WS, Graham SE, Shea D, LeBlanc GA (1998) Altered metabolic elimination of testosterone and associated toxicity following exposure of Daphnia magna to nonylphenol polyethoxylate. Ecotoxicol Environ Saf 39:104–111

    CAS  Google Scholar 

  • Baldwin WS, LeBlanc GA (1994a) In vivo biotransformation of testosterone by phase I and II detoxication enzymes and their modulation by 20-hydroxyecdysone in Daphnia magna. Aquat Toxicol 29:103–117

    CAS  Google Scholar 

  • Baldwin WS, LeBlanc GA (1994b) Identification of multiple steroid hydroxylases in daphnia magna and their modulation by xenobiotics. Environ Toxicol Chem 13:1013–1021

    CAS  Google Scholar 

  • Bettin C, Oehlmann J, Stroben E (1996) TBT-induced imposex in marine neogastropods is mediated by an increasing androgen level. Helgoländer Meeresun 50:299–317

    Google Scholar 

  • Blanchet M-F, Ozon R, Meusy JJ (1972) Metabolism of steroids, in vitro, in the male crab Carcinus maenas Linné. Comp Biochem Physiol 41B:251–261

    Google Scholar 

  • Borg W, Shackleton C, Pahuja SL, Hochburg RB (1995) Long-lived testosterone esters in the rat. Proc Natl Acad Sci USA 92:1545–1549

    CAS  Google Scholar 

  • Bose R, Majumdar C, Bhattacharya S (1997) Steroids in Achatina fulica (Bowdich): steroid profile in haemolymph and in vitro release of steroids from endogenous precursors by ovotestis and albumen gland. Comp Biochem Physiol 116C:179–182

    CAS  Google Scholar 

  • Bulayeva NN, Watson CS (2004) Xenoestrogen-induced ERK-1 and ERK-2 activation via multiple membrane-initiated signaling pathways. Environ Health Perspect 112(15):1481–1487

    Article  CAS  Google Scholar 

  • Canesi L, Ciacci C, Betti M, Lorusso LC, Marchi B, Burattini S, Falcieri E, Gallo G (2004a) Rapid effects of 17β-estradiol on cell signaling and function of Mytilus hemocytes. Gen Comp Endocrinol 136(1):58–71

    CAS  Google Scholar 

  • Canesi L, Lorusso LC, Ciacci C, Betti M, Zampini M, Gallo G (2004b) Environmental estrogens can affect the function of mussel hemocytes through rapid modulation of kinase pathways. Gen Comp Endocrinol 138(1):58–69

    CAS  Google Scholar 

  • Connat J-L, Diehl PA, Morici M (1984) Metabolism of ecdysteroid during vitellogenesis of the tick Orinthodoros moubata (Ixodoidea, Argasidae): accumulation of apolar metabolites in the eggs. Gen Comp Endocrinol 56:100–110

    CAS  Google Scholar 

  • D’Aniello A, Di Cosmo A, Di Cristo C, Assisi L, Botte V, Di Fiore MM (1996) Occurrence of sex steroid hormones and their binding proteins in Octopus vulgaris lam. Biochem Biophys Res Commun 227:782–788

    CAS  Google Scholar 

  • De Fur P, Crane M, Ingersoll C, Tattersfield L (eds) (1999) Endocrine disruption in invertebrates: endocrinology, testing and assessment. SETAC Press, Pensacola, FL, pp 23–106

  • De Knecht JA, Stroomberg GJ, Tump C, Helms M, Verweij RA, Commandeur J, van Gestel CA, van Straalen NM (2001) Characterization of enzymes involved in biotransformation of polycyclic aromatic hydrocarbons in terrestrial isopods. Environ Toxicol Chem 20:1457–1464

    Google Scholar 

  • De Longcamp D, Lubet P, Drosdowsky M (1974) The in vitro biosynthesis of steroids by the gonad of the mussel (Mytilus edulis). Gen Comp Endocrinol 22:116–127

    Google Scholar 

  • Den Besten PJ, Elenbaas JML, Maas JR, Dieleman SJ, Herwig HJ, Voogt PA (1991) Effects of cadmium and polychlorinated biphenyls (Clophen A50) on steroid metabolism and cytochrome P-450 monooxygenase system in sea star Asterias rubens L. Aquat Toxicol 20:95–110

    Google Scholar 

  • De Waal M, Portman J, Voogt PA (1982) Steroid receptors in invertebrates. A specific 17β-estradiol binding protein in a seastar. Mar Biol Lett 3:317–323

    Google Scholar 

  • Di Cosmo A, Di Cristo C, Paolucci M (2002) A estradiol-17β receptor in the reproductive system of the female of Octopus vulgaris: characterization and immunolocalization. Mol Reprod Dev 61(3):367–375

    CAS  Google Scholar 

  • Di Cosmo A, Paolucci M, Di Cristo C, Botte V, Ciarcia G (1998) Progesterone receptor in the reproductive system of the female of Octopus vulgaris: characterization and immunolocalization. Mol Reprod Dev 50(4):451–460

    CAS  Google Scholar 

  • Dutton GJ (1996) Uridine diphosphate glucose and the synthesis of phenolic glucosides by mollusks. Arch Biochem Biophys 116(1):399–405

    Google Scholar 

  • Elmamlouk TH, Gessner T (1978) Carbohydrate and sulfate conjugations of p-Nitrophenol by hepatopancreas of Homarus americanus. Comp Biochem Physiol 61C:363–367

    CAS  Google Scholar 

  • Escriva H, Delaunay R, Laudet V (2000) Ligand binding and nuclear receptor evolution. Bioessays 22:717–727

    CAS  Google Scholar 

  • Escriva H, Safi R, Hanni C, Langlois M-C, Saumitou-Laprade P, Stehelin D, Capron A, Pierce R, Laudet V (1997) Ligand binding was acquired during evolution of nuclear receptors. Proc Natl Acad Sci USA 94:6803–6808

    CAS  Google Scholar 

  • Fairs NJ, Evershed RP, Quinlan PT, Goad LJ (1989) Detection of unconjugated and conjugated steroids in the ovary, eggs, and haemolymph of the decapod crustacean Nephrops norvegicus. Gen Comp Endocrinol 74(2):199–208

    CAS  Google Scholar 

  • Falkenstein E, Tillmann HC, Christ M, Feuring M, Wehling M (2000) Multiple actions of steroid hormones-a focus on rapid, nongenomic effects. Pharmacol Rev 52(4):513–56

    CAS  Google Scholar 

  • Florin C, Kohler T, Grandguillot M, Plesiat P (1996) Comamonas testosteroni 3-ketosteroid-Δ4(5α)-dehydrogenase: gene and protein characterization. J Bacteriol 178(11):3322–3330

    CAS  Google Scholar 

  • Foster GD, Crosby DG (1986) Xenobiotic metabolism of p-nitrophenol derivatives by the rice field crayfish (Procambarus clarkii). Environ Toxicol Chem 15:1059–1070

    Google Scholar 

  • Gauthier-Clerc S, Pellerin J, Amiard JC (2006) Estradiol-17β and testosterone concentrations in male and female Mya arenaria (Mollusca bivalvia) during the reproductive cycle. Gen Comp Endocrinol 145:133–139

    CAS  Google Scholar 

  • Giessing AMB, Lund T (2002) Identification of 1-hydroxypyrene glucuronide in tissue of marine polychaete Nereis diversicolor by liquid chromatography/ion trap multiple mass spectrometry. Rapid Commun Mass Spectrom 16:1521–1525

    CAS  Google Scholar 

  • Gooding MP, LeBlanc GA (2001) Biotransformation and disposition of testosterone in the eastern mud snail Ilyanassa obsoleta. Gen Comp Endocrinol 122:172–180

    CAS  Google Scholar 

  • Gooding MP, LeBlanc GA (2004) Seasonal variation in the regulation of testosterone levels in the eastern mud snail (Ilyanassa obsoleta). Invert Biol 123:237–243

    Article  Google Scholar 

  • Gooding MP, Wilson VS, Folmar LC, Marcovich DT, LeBlanc GA (2003) The biocide tributyltin reduces the accumulation of testosterone as fatty acid esters in the mud snail (Ilyanassa obsoleta). Environ Health Perspect 111(4):426–430

    Article  CAS  Google Scholar 

  • Gottfried H, Lusis O (1966) Steroids of invertebrates: the in vitro production of 11-ketotestosterone and other steroids by the eggs of the slug, Arion ater rufus (Linn.). Nature 212:1488–1489

    CAS  Google Scholar 

  • Gottfried H, Dorfman RI, Wall PE (1967) Steroids of invertebrates: production of oestrogens by an accessory reproductive tissue of the slug Arion ater rufus (Linn.). Nature 215:409–410

    CAS  Google Scholar 

  • Gottfried H, Dorfman RI (1970) Steroids of invertebrates. V. The in vitro biosynthesis of steroids by the male-phase ovotestis of the slug (Ariolimax californicus). Gen Comp Endocrinol 15(1):120–138

    CAS  Google Scholar 

  • Hines GA, Bryan PJ, Wasson KM, McClintock JB, Watts SA (1996) Sex steroid metabolism in the antarctic pteropod Clione antarctica (Mollusca: Gastropoda). Invert Biol 115:113–119

    Google Scholar 

  • Hines GA, Watts SA, Walker CW, Voogt PA (1992) Androgen metabolism in somatic and germinal tissues of the sea star Asterias vulgaris. Comp Biochem Physiol 102B(3):521–526

    CAS  Google Scholar 

  • Hochberg RB (1998) Biological esterification of steroids. Endocr Rev 19:331–348

    CAS  Google Scholar 

  • Horiguchi T, Katsu Y, Ohta Y, Watanabe H, Iguchi T, Morishita F, Matsushima O, Shiraishi H, Morita M (2004) Is inhibition of aromatase activity due to TBT exposure the primary factor for gastropod imposex? Mar Environ Res 58:459–460

    Google Scholar 

  • Hum DW, Bélanger A, Lévesque E, Barbier O, Beaulieu M, Albert C, Vallée M, Guillemette C, Tchernof A, Turgeon D, Dubois S (1999) Characterization of UDP-glucuronosyltransferases active on steroid hormones. J Steroid Biochem Mol Biol 69(1–6):413–423

    CAS  Google Scholar 

  • James MO, Boyle SM (1998) Cytochromes P450 in crustacea. Comp Biochem Physiol 121C:157–172

    CAS  Google Scholar 

  • James MO, Little PJ (1984) 3-Methylcholanthrene does not induce in vitro xenobiotic metabolism in spiny lobster hepatopancreas, or affect in vivo disposition of benzo(a)pyrene. Comp Biochem Physiol 78C:241–245

    CAS  Google Scholar 

  • James MO (1987) Conjugation of organic pollutants in aquatic species. Environ Health Perspect 71:97–103

    CAS  Google Scholar 

  • James MO (1989) Cytochrome P450 monooxygenases in crustaceans. Xenobiotica 19:1063–1076

    CAS  Google Scholar 

  • Janer G, Mesia-Vela S, Porte C, Kauffman FC (2004) Esterification of vertebrate-type steroids in the Eastern oyster (Crassostrea virginica). Steroids 69(2):129–136

    CAS  Google Scholar 

  • Janer G (2005) Steroid levels, steroid metabolic pathways and their modulation by endocrine disruptors in invertebrates. PhD Thesis

  • Janer G, LeBlanc GA, Porte C (2005a) Identification of vertebrate-type steroid metabolism in three invertebrate species: a comparative study on androgen metabolism. Gen Comp Endocrinol 143:211–221

    CAS  Google Scholar 

  • Janer G, Lavado R, Thibaut R, Porte C (2005b) Effects of 17β-estradiol exposure in the mussel Mytilus galloprovincialis: a possible regulating role for acyltransferases. Aquat Toxicol 75:32–42

    CAS  Google Scholar 

  • Janer G, Stenberg RM, LeBlanc GA, Porte C (2005c) Testosterone conjugating activities in invertebrates: are they targets for endocrine disruptors? Aquat Toxicol 71(3):273–282

    CAS  Google Scholar 

  • Janer G, Lyssimachou A, Bachman J, Oehlmann J, Schulte-Oehlmann U, Porte C (2006a) Sexual dimorphism in esterified steroid levels in the gastropod Marisa cornuarietis: the effect of xenoandrogenic compounds. Steroids 71(6):435–444

    CAS  Google Scholar 

  • Janer G, Bachmann J, Oehlmann J, Schulte-Oehlmann U, Porte C (2006b) The effect of organotin compounds on gender specific androstenedione metabolism in Marisa cornuarietis. Steroid Biochem Mol Biol 99(2–3):147–156

    CAS  Google Scholar 

  • Keshan B, Ray AK (2001) The presence of estradiol-17β and its specific binding sites in posterior silk gland of Bombyx mori. Gen Comp Endocrinol 123:23–30

    CAS  Google Scholar 

  • Kiser CS, Parish EJ, Bone LW (1986) Binding of steroidal sex hormones by supernatant from Trichostrongylus colubriformis (nematoda). Comp Biochem Physiol 83B:787–790

    CAS  Google Scholar 

  • Köhler H-R, Kloas W, Schirling M, Lutz I, Reye AL, Langen JS, Triebskorn R, Nagel R, Schönfelder G (2006) Sex steroid receptor evolution and signalling in aquatic invertebrates. Ecotoxicology, DOI: 10.1007/s10646-006-0111-3

  • Kondo K, Kai M, Setoguchi Y, Eggertsen G, Sjoborn P, Setoguchi T, Okuda K, Bjorkhem I (1994) Cloning and expression of cDNA of human D4-3-oxosteroid-5β-reductase and substrate specificity of the expressed enzyme. Eur J Biochem 219:357–363

    CAS  Google Scholar 

  • Krusch B, Schoenmakers HJN, Voogt PA, Nolte A (1979) Steroid synthesizing capacity of the dorsal body of Helix pomatia L. (Gastropoda)- and in vitro study. Comp Biochem Physiol 64B:101–104

    CAS  Google Scholar 

  • Labrie F, Luu-The V, Lin S-X, Labrie C, Simard J, Breton R, Bélanger A (1997) The key role of 17β-hydroxysteroid dehydrogenases in sex steroid biology. Steroids 62:148–158

    CAS  Google Scholar 

  • LaFont R (2000) The endocrinology of invertebrates. Ecotoxicology 9:41–57

    CAS  Google Scholar 

  • Lafont R, Mathieu M (2006) Steroids in aquatic invertebrates. Ecotoxicology, DOI: 10.1007/s10646-006-0113-1

  • Lanisnik-Rizner T, Zaeklj-Mavric M (2000) Characterization of fungal 17β-hydroxysteroid dehydrogenases. Comp Biochem Physiol 127B:53–63

    CAS  Google Scholar 

  • Lavado R, Janer G, Porte C (2006a) Steroid levels and steroid metabolism in the mussel Mytilus edulis: the modulation effect of dispersed crude oil and alkylphenols. Aquat Toxicol 78(Suppl 1):S65–S72

    CAS  Google Scholar 

  • Lavado R, Barbaglio A, Carnevali CP, Porte C (2006b) Steroid levels in crinoid echinoderms are altered by exposure to model endocrine disruptors. Steroids 71(6):489–497

    CAS  Google Scholar 

  • Lavado R, Sugni M, Carnevali MDC, Porte C (2006c) Triphenyltin alters androgen metabolism in the sea urchin Paracentrotus lividus. Aquat Toxicol 79(3):247–256

    CAS  Google Scholar 

  • Le Curieux-Belfond O, Moslemi S, Mathieu M, Séralini GE (2001) Androgen metabolism in oyster Crassostera gigas: evidence for 17β-HSD activities and characterization of an aromatase-like activity inhibited by pharmacological compounds and a marine pollutant. J Steroid Bioch Mol Biol 78:359–366

    CAS  Google Scholar 

  • Le Guellec D, Thiard MC, Remy-Martin JP, Deray A, Gomot L, Adessi GL (1987) In vitro metabolism of androstenedione and identification of endogenous steroids in Helix aspersa. Gen Comp Endocrinol 66:425–433

    CAS  Google Scholar 

  • Li C-LJ, James MO (2000) Oral bioavailability and pharmacokinetics of elimination of 8-hydroxybenzo[a]pyrene and its glucoside and sulfate conjugates after administration to male and female american lobster, Homarus americanus. Toxicol Sci 57:75–86

    CAS  Google Scholar 

  • Livingstone DR, Kirchin MA, Wiseman A (1989) Cytochrome P-450 and oxidative metabolism in molluscs. Xenobiotica 19(10):1041–1062

    Article  CAS  Google Scholar 

  • Livingstone DR (1991) Organic xenobiotic metabolism in marine invertebrates. In: Advances in comparative and environmental physiology, vol 7. Springer-Verlag, Berlin, pp 46–185

  • Lo S, Allera A, Albers P, Heimbrecht J, Jantzen E, Klingmuller D, Steckelbroeck S (2003) Dithioerythritol (DTE) prevents inhibitory effects of triphenyltin (TPT) on the key enzymes of the human sex steroid hormone metabolism. J Steroid Biochem Mol Biol 84(5):569–576

    CAS  Google Scholar 

  • Lupo di Prisco C, Dessi’ Fulgheri F (1975) Alternative pathways of steroid biosynthesis in gonads and hepatopancreas of Aplysia depilans. Comp Biochem Physiol 50B:191–195

    Google Scholar 

  • Matsumoto T, Osada M, Osawa Y, Mori K (1997) Gonadal estrogen profile and immunohistochemical localization of steroidogenic enzymes in the oyster and scallop during sexual maturation. Comp Biochem Physiol 118B:811–817

    CAS  Google Scholar 

  • Milanesi L, Monje P, Boland R (2001) Presence of estrogens and estrogen receptor-like proteins in Solanum glaucophyllum. Biochem Biophys Res Commun 289:1175–1179

    CAS  Google Scholar 

  • Miller WL (2002) Androgen biosynthesis from cholesterol to DHEA. Mol Cell Endocrinol 198(1–2):7–14

    CAS  Google Scholar 

  • Morcillo Y, Albalat A, Porte C (1999) Mussels as sentinels of organotin pollution: bioaccumulation and effects on P450-mediated aromatase activity. Environ Toxicol Chem 18:1203–1208

    CAS  Google Scholar 

  • Morcillo Y, Porte C (1999) Evidence of endocrine disruption in the imposex-affected Gastropod Bolinus brandaris. Environ Res Sect A 81:349–354

    CAS  Google Scholar 

  • Morcillo Y, Ronis MJJ, Porte C (1998) Effects of tributyltin on the Phase I testosterone metabolism and steroid titres of the clam Ruditapes decussata. Aquat Toxicol 42(1):1–13

    CAS  Google Scholar 

  • Mori K, Muramatsu T, Nakamura Y (1969) Effect of steroid on oyster IV: acceleration of sexual maturation in female Crassostrea gigas by estradiol-17β. Bull Jpn Soc Sci Fish 35:1077–1079

    CAS  Google Scholar 

  • Nagabhushanam R, Kulkarni GK (1981) Effect of exogenous testosterone on the androgenic gland and testis of a marine penaeid prawn, Parapenaeopsis hardwickii (Miers) (Crustacea, Decapoda, Penaeidae). Aquaculture 23(1–4):19–27

    CAS  Google Scholar 

  • Norman AW, Litwack G (1998) Hormones, 2nd edn. Academic Press. San Diego

  • Oberdörster E, Rittschof D, McClellan-Green P (1998) Testosterone metabolism in imposex and normal Ilyanassa obsoleta: comparison of field and TBT Cl-induced imposex. Mar Poll Bull 36:144–151

    Google Scholar 

  • Okuda A, Okuda K (1984) Purification and characterization of Δ4-3-ketosteroid 5β-reductase. J Biol Chem 259:7519–7524

    CAS  Google Scholar 

  • Ollevier F, De Clerck D, Diederik H, De Loof A (1986) Identification of nonecdysteroid steroids in hemolymph of both male and female Astacus leptodactylus (Crustacea) by gas chromatography-mass spectrometry. Gen Comp Endocrinol 61:214–228

    CAS  Google Scholar 

  • Osada M, Tawarayama H, Mori K (2004) Estrogens in relation to goandal development of Japanese scallop, Patinopecten yessosensis: gonadal profile and immunolocalisation of P450 aromatase and estrogen. Comp Biochem Physiol 139:123–128

    Google Scholar 

  • Paesen G, De Loof A (1989) The presence of progesterone binding protein in spermathecae of the migratory Locust, Locusta migratoria migratorioides. Invert Reprod Dev 14:267–277

    Google Scholar 

  • Parks LG, LeBlanc GA (1998) Involvement of multiple biotransformation processes in the metabolic elimination of testosterone by juvenile and adult fathead minnows (Pimephales promelas). Gen Comp Endocrinol 112:69–79

    CAS  Google Scholar 

  • Peng L, Arensburg J, Orly J, Payne AH (2002) The murine 3β-hydroxysteroid dehydrogenase (3β-HSD) gene family: a postulated role for 3β-HSD VI during early pregnancy. Mol Cell Endocrinol 187(1–2):213–221

    CAS  Google Scholar 

  • Penning TM, Jin Y, Heredia VV, Lewis M (2003) Structure-function relationships in 3α-hydroxysteroid dehydrogenases: a comparison of the rat and human isoforms. J Steroid Biochem Mol Biol 85:247–255

    CAS  Google Scholar 

  • Pernet V, Anctil M (2002) Annual variations and sex-related differences of estradiol-17β levels in the anthozoan Renilla koellikeri. Gen Comp Endocrinol 129(1):63–68

    CAS  Google Scholar 

  • Reis-Henriques MA, Coimbra J (1990) Variations in the levels of progesterone in Mytilus edulis during the annual reproductive cycle. Comp Biochem Physiol 95A:343–348

    CAS  Google Scholar 

  • Reis-Henriques MA, LeGuellec D, Remy-Martin JP, Adessi GL (1990) Studies on endogenous steroid from the marine mollusc Mytilus edulis L. by gas chromatography and mass spectrometry. Comp Biochem Physiol 95:303–309

    Google Scholar 

  • Ronis MJJ, Mason AZ (1996) The metabolism of testosterone by the periwinkle (Littorina littorea) in vitro and in vivo: effects of tribultyl Tin. Mar Environ Res 42:161–166

    CAS  Google Scholar 

  • Sakr AA, Osman GY, Abo-Shafey AE (1992) Effect of testosterone on the ovotestis of the land snail Theba pisana. Funct Dev Morphol 2:99–101

    CAS  Google Scholar 

  • Santos MM, Hallers-Tjabbes CC X, Vieira N, Boon JP, Porte C (2002) Cytochrome P450 differences in normal and imposex-affected female whelk Buccinum undatum from the open North Sea. Mar Environ Res 54:661–665

    CAS  Google Scholar 

  • Schell JD, James MO (1989) Glucose and sulfate conjugation of phenolic compounds by the spiny lobster (Panulirus argus). J Biochem Toxicol 4:133–138

    CAS  Google Scholar 

  • Schoenmakers HJN (1979) In vitro biosynthesis of steroids from cholesterol by the ovaries and pyloric caeca of the starfish Asterias rubens. Comp Biochem Physiol 63:179–184

    Google Scholar 

  • Schoenmakers HJN, Voogt PA (1980) In vitro biosynthesis of steroids from progesterone by the ovaries and pyloric caeca of the starfish Asterias rubens. Gen Comp Endocrinol 41:408–416

    CAS  Google Scholar 

  • Siah A, Pellerin J, Benosman A, Gagné J-P, Amiard J-C (2002) Seasonal gonad progesterone pattern in the soft-shell clam Mya arenaria. Comp Biochem Physiol 132:499–511

    CAS  Google Scholar 

  • Simpson ER, Davis SR (2001) Minireview: aromatase and the regulation of estrogen biosynthesis-some new perspectives. Endocrinology 142(11):4589–4594

    CAS  Google Scholar 

  • Singer SC, Marsh PE, Gonsoulin F, Lee RF (1980) Mixed function oxidase activity in the blue crab, Callinectes sapidus: characterization of enzyme activity from stomach tissue. Comp Biochem Biophys 65:129–134

    Google Scholar 

  • Slinger AJ, Dinan LN, Isaac RE (1986) Isolation of apolar ecdysteroid conjugates from newly-laid oothecae of Periplaneta americana. Insect Biochem 16:115–119

    CAS  Google Scholar 

  • Slinger AJ, Isaac RE (1988) Synthesis of apolar ecdysone esters by ovaries of the cockroach Periplaneta americana. Gen Comp Endocrinol 70:74–82

    CAS  Google Scholar 

  • Snyder MJ (2000) Cytochrome P450 enzymes in aquatic invertebrates: recent advances and future directions. Aquat Toxicol 48:529–547

    CAS  Google Scholar 

  • Spooner N, Gibbs PE, Bryan GW, Goad LJ (1991) The effect of tributyltin upon steroid titers in the female dogwhelk, Nucella lapillus, and the development of imposex. Mar Environ Res 32:37–49

    CAS  Google Scholar 

  • Stefano GB, Cadet P, Mantiene K, Cho JJ, Jones D, Zhu W (2003) Estrogen signaling at the cell surface coupled to nitric oxide release in Mytilus edulis nervous system. Endocrinology 144:1234–1240

    CAS  Google Scholar 

  • Stroomberg GJ, Zappey H, Steen RJ, van Gestel CA, Ariese F, Velthorst NH, van Straalen NM (2004) PAH biotransformation in terrestrial invertebrates-a new phase II metabolite in isopods and springtails. Comp Biochem Physiol 138:129–137

    Google Scholar 

  • Strott CA (1996) Steroid sulfotransferases. Endocrin Rev 17:670–697

    CAS  Google Scholar 

  • Sugimoto Y, Yoshida M, Tamaoki B (1990) Purification of 5β-reductase from hepatic cytosol fraction of chicken. J Steroid Biochem Mol Biol 37:717–724

    CAS  Google Scholar 

  • Swevers L, Lambert JG, De Loof A (1991) Metabolism of vertebrate-type steroids by tissues of three crustacean species. Comp Biochem Physiol 99:35–41

    Google Scholar 

  • Takahashi N, Kanatani H (1981) Effect of 17β-estradiol on growth of oocytes in cultured ovarian fragments of the starfish, Asterina pectinifera. Dev Growth Diff 23:565–569

    Google Scholar 

  • Takeda N (1979) Induction of egg-laying by steroid hormones in slugs. Comp Biochem Physiol 62:273–278

    Google Scholar 

  • Thibaut R, Porte C (2004) Effects of endocrine disrupters on sex steroid synthesis and metabolism pathways in fish. J Steroid Biochem Mol Biol 92:485–494

    CAS  Google Scholar 

  • Thornton JW, Need E, Crews D (2003) Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. Science 301:1714–1717

    CAS  Google Scholar 

  • Verslycke T, De Wasch K, De Brabander HF, Janssen CR (2002) Testosterone metabolism in the estuarine mysid Neomysis integer (Crustacea; Mysidacea): identification of testosterone metabolites and endogenous vertebrate-type steroids. Gen Comp Endocrinol 126:190–199

    CAS  Google Scholar 

  • Verslycke T, Poelmans S, De Wasch K, De Brabander HF, Janssen CR (2004) Testosterone and energy metabolism in the estuarine mysid Neomysis integer (Crustacea: Mysidacea) following exposure to endocrine disruptors. Environ Toxicol Chem 23:1289–1296

    CAS  Google Scholar 

  • Verslycke T, Poelmans S, De Wasch K, Vercauteren J, Devos C, Moens L, Sandra P, De Brabander HF, Janssen CR (2003) Testosterone metabolism in the estuarine mysid Neomysis integer (Crustacea; Mysidacea) following tributyltin exposure. Environ Toxicol Chem 22:2030–2036

    CAS  Google Scholar 

  • Voogt PA, van Rheenen JWA (1986) Androstenedione metabolism in the sea star Asterias rubens L. studied in homogenates and intact tissue: biosynthesis of the novel steroid fatty-acyl testosterone. Comp Biochem Physiol 85:497–501

    Google Scholar 

  • Voogt PA, van Rheenen JWA, Lambert JGD, de Groot BF, Mollema C (1986) Effects of different experimental conditions on progesterone metabolism in the sea star Asterias rubens L. Comp Biochem Physiol 84:397–402

    Google Scholar 

  • Voogt PA, den Besten PJ, Kusters GC, Messing MW (1987) Effects of cadmium and zinc on steroid metabolism and steroid level in the sea star Asterias rubens L. Comp Biochem Physiol 86:83–89

    CAS  Google Scholar 

  • Voogt PA, den Besten PJ, Jansen M (1990) The Δ5-pathway in steroid metabolism in the sea star Asterias rubens L. Comp Biochem Physiol 97:555–562

    Google Scholar 

  • Voogt PA, den Besten PJ, Jansen M (1991) Steroid metabolism in relation to the reproductive cycle in Asterias rubens L. Comp Biochem Physiol 99:77–82

    Google Scholar 

  • Voogt PA, Lambert JGD, Granneman JCM, Jansen M (1992) Confirmation of the presence of oestradiol-17β in sea star asterias rubens by GC-MS. Comp Biochem Physiol 101:13–16

    Google Scholar 

  • Warrier SR, Tirumalai R, Subramoniam T (2001) Occurrence of vertebrate steroids, estradiol 17beta and progesterone in the reproducing females of the mud crab Scylla serrata. Comp Biochem Physiol 130:283–294

    Google Scholar 

  • Wasson KM, Hines GA, Watts SA (1998) Synthesis of testosterone and 5α-androstanediols during nutritionally stimulated gonadal growth in Lytechinus variegatus Lamarck (Echinodermata: Echinoidea). Gen Comp Endocrinol 111:197–206

    CAS  Google Scholar 

  • Wasson KM, Watts SA (2000) Progesterone metabolism in the ovaries and testes of the echinoid Lytechinus variegatus Lamarck (Echinodermata). Comp Biochem Physiol 127:263–272

    CAS  Google Scholar 

  • Waxman DJ, Ko A, Walsh C (1983) Regioselectivity and stereoselectivity of androgen hydroxylation catalyzed by cytochrome P-450 isozymes purified from phenobarbital-induced rat liver. J Biol Chem 10:11937–11947

    Google Scholar 

  • Weinshilboum RM, Otterness DM, Aksoy IA, Wood TC, Her C, Raftogianis RB (1997) Sulfation and sulfotransferases 1: sulfotransferase molecular biology: cDNAs and genes. FASEB 11(1):3–14

    CAS  Google Scholar 

  • Whiting P, Dinan L (1989) Identification of the endogenous apolar ecdysteroid conjugates present in newly-laid eggs of the house cricket (Acheta domesticus) as 22-long-chain fatty acyl esters of ecdysone. Insect Biochem 19:759–765

    CAS  Google Scholar 

  • Wilson JD (2001) The role of 5α-reduction in steroid hormone physiology. Reprod Fertil Dev 13:673–678

    CAS  Google Scholar 

  • Wilson VS, LeBlanc GA (1998) Endosulfan elevates testosterone biotransformation and clearance in CD-1 mice. Toxicol Appl Pharmacol 148(1):158–168

    CAS  Google Scholar 

  • Xu RA, Barker MF (1990) Annual changes in the steroid levels in the ovaries and the pyloric caeca of Sclerasterias mollis (Echinodermata asteroidea) during the reproductive cycle. Comp Biochem Physiol 95:127–133

    Google Scholar 

  • Zhang M, Kubo I (1992) Characterization of ecdysteroid-22-O-acyltransferase from tobacco budworm, Heliothis virescens. Insect Biochem Mol Biol 22:599–603

    CAS  Google Scholar 

  • Zhu W, Mantione K, Jones D, Salamon E, Cho JJ, Cadet P, Stefano GB (2003) The presence of 17β-estradiol in Mytilus edulis gonadal tissues: evidence for estradiol isoforms. Neuro Endocrinol Lett 24:137–140

    CAS  Google Scholar 

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Aknowledgments

This study was supported by the European Union (COMPRENDO-Project, EVK1-CT-2002-00129).

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  1. Environmental Chemistry Department, IIQAB-CSIC, C/ Jordi Girona, 18, 08034, Barcelona, Spain

    Gemma Janer & Cinta Porte

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  1. Gemma Janer
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  2. Cinta Porte
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Correspondence to Gemma Janer.

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Janer, G., Porte, C. Sex steroids and potential mechanisms of non-genomic endocrine disruption in invertebrates. Ecotoxicology 16, 145–160 (2007). https://doi.org/10.1007/s10646-006-0110-4

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