Testosterone concentration and aromatisation efficiency at different stages of gonad development: a case study with Mytilus edulis trossulus

References

• Avila -Poveda OH, Montes-Pérez RC, Benitez-Villalobos F, Rosas C. 2013. Development and validation of a solid-phase radioimmunoassay for measuring progesterone and testosterone in Octopus gonad extracts. Malacologia. 56(1 & 2):121–134. doi: 10.4002/040.056.0209.
   Web of Science ®Google Scholar
• Basaria S. 2013. Reproductive aging in men. Endocrinol Metab Clin North Am. 42(2):255–270. doi: 10.1016/j.ecl.2013.02.012.
   PubMed Web of Science ®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. Compar Biochem Physio Part C: Toxico Pharma. 116(3):179–182. doi: 10.1016/S0742-8413(96)00163-6.
   Web of Science ®Google Scholar
• Bulun SE, Sebastian S, Takayama K, Suzuki T, Sasano H, Shozu M. 2003. The human CYP19 (aromatase P450) gene: Update on physiologic roles and genomic organization of promoters. J Steroid Biochem Mol Biol. 86(3–5):219–224. doi: 10.1016/S0960-0760(03)00359-5.
   PubMed Web of Science ®Google Scholar
• Callard GV, Tarrant AM, Novillo A, Yacci P, Ciaccia LVS, Vajda S, Chuang G-Y, Kozakov D, Greytak SR, Sawyer S. 2011. Evolutionary origins of the estrogen signaling system: Insights from amphioxus. J Steroid Biochem Mol Biol. 127(3–5):176–188. doi: 10.1016/j.jsbmb.2011.03.022.
   PubMed Web of Science ®Google Scholar
• Chong Sánchez F, Enriquez Díaz M, Murillo Rodríguez E, Aldana Aranda D. 2019. First use of a non-invasive technique for determination of sex hormones in the queen conch Lobatus gigas, Mollusca Gastropoda. Aquacult Int. 27(2):437–448. doi: 10.1007/s10499-018-0336-1.
   Web of Science ®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 Bioph Res Co. 227(3):782–788. doi: 10.1006/BBRC.1996.1585.
   PubMed Web of Science ®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 Endocr. 22(1):116–127. doi: 10.1016/0016-6480(74)90093-8.
   PubMed Web of Science ®Google Scholar
• di Cosmo A, di Cristo C, Paolucci M. 2001. Sex steroid hormone fluctuations and morphological changes of the reproductive system of the female of Octopus vulgaris throughout the annual cycle. J Experimen Zoo Part A. 289:33–47. doi: 10.1002/1097-010X(20010101/31)289:1<33:AID-JEZ4>3.0.CO;2-A.
   PubMedGoogle 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. doi: 10.1002/mrd.10014.
   PubMed Web of Science ®Google Scholar
• Fernandes D, Loi B, Porte C. 2011. Biosynthesis and metabolism of steroids in molluscs. J Steroid Biochem Mol Biol. 127(3–5):189–195. doi: 10.1016/j.jsbmb.2010.12.009.
   PubMed Web of Science ®Google Scholar
• Fodor I, Urbán P, Scott AP, Pirger Z. 2020. A critical evaluation of some of the recent so-called ‘evidence’ for the involvement of vertebrate-type sex steroids in the reproduction of mollusks. Mol Cell Endocrinol. 516:110949. doi: 10.1016/j.mce.2020.110949.
   PubMed Web of Science ®Google Scholar
• Fukushima M, Funabiki I, Hashizume T, Osada K, Yoshida W, Ishida S. 2008. Detection and changes in levels of testosterone during spermatogenesis in the freshwater planarian bdellocephala brunnea. Zoolog Sci. 25(7):760–765. doi: 10.2108/ZSJ.25.760.
   PubMed Web of Science ®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 Endocr. 145(2):133–139. doi: 10.1016/j.ygcen.2005.08.004.
   PubMed Web of Science ®Google Scholar
• Gooding MP, LeBlanc GA. 2001. Biotransformation and disposition of testosterone in the eastern mud snail Ilyanassa obsoleta. Gen Comp Endocr. 122(2):172–180. doi: 10.1006/gcen.2001.7630.
   PubMed Web of Science ®Google Scholar
• Gooding MP, LeBlanc GA. 2004. Seasonal variation in the regulation of testosterone levels in the eastern mud snail (Ilyanassa obsoleta). Invert Bio. 123(3):237–243. doi: 10.1111/j.1744-7410.2004.tb00158.x.
   Web of Science ®Google Scholar
• Guercia C, Cianciullo P, Porte C. 2017. Analysis of testosterone fatty acid esters in the digestive gland of mussels by liquid chromatography-high resolution mass spectrometry. Steroids. 123:67–72. doi: 10.1016/J.STEROIDS.2017.05.008.
   PubMed Web of Science ®Google Scholar
• Hallmann A, Konieczna L, Swiezak J, Milczarek R, Smolarz K. 2019. Aromatisation of steroids in the bivalve Mytilus trossulus. Peer J 2019. 7:e6953. doi:10.7717/peerj.6953.
   Google Scholar
• Hallmann A, Smolarz K, Konieczna L, Zabrzańska S, Belka M, Baczek T. 2016. LC-MS measurment of free steroids in mussels (Mytilus trossulus) from the southern Baltic Sea. J Pharmaceut Biomed. 117:311–315. doi:10.1016/j.jpba.2015.09.013.
   PubMed Web of Science ®Google Scholar
• Janer G, Porte C. 2007. Sex steroids and potential mechanisms of non-genomic endocrine disruption in invertebrates. Ecotoxicol. 16(1):145–160. doi: 10.1007/S10646-006-0110-4.
   PubMed Web of Science ®Google Scholar
• Janer G, Sternber RM, Leblanc GA, Porte C. 2005. Testosterone conjugating activities in invertebrates: Are they targets for endocrine disruptors? Aquat Toxicol. 71(3):273–282. doi: 10.1016/j.aquatox.2004.11.024.
   PubMed Web of Science ®Google Scholar
• Kellis JT, Vickery LE. 1987. The active site of aromatase cytochrome P-450. Differential effects of cyanide provide evidence for proximity of heme-iron and carbon-19 in the enzyme-substrate complex. J Biol Chem. 262(18):8840–8844. doi: 10.1016/S0021-9258(18)47491-1.
   PubMed Web of Science ®Google Scholar
• Lavado R, Janer G, Porte C. 2006. Steroid levels and steroid metabolism in the Mussel Mytilus edulis: The modulating effect of dispersed crude oil and alkylphenols. Aquat Toxicol. 78:S65–S72. doi: 10.1016/j.aquatox.2006.02.018.
   PubMed Web of Science ®Google Scholar
• LeBlanc GA, Gooding MP, Sternberg RM. 2005. Testosterone-fatty acid esterification: A unique target for the endocrine toxicity of tributyltin to gastropods. Integr Comp Biol. 45(1):81–87. doi: 10.1093/icb/45.1.81.
   PubMed Web of Science ®Google Scholar
• Li Q, Osada M, Suzuki T, Mori K, Li Q, Suzuki T, Mori K. 1998. Changes in vitellin during oogenesis and effect of estradiol on vitellogenesis in the Pacific oyster Crassostrea gigas. Invert Reproduc Develop. 33:87–93. doi:10.1080/07924259.1998.9652345.
   Web of Science ®Google Scholar
• Liu J, Zhang Z, Zhang L, Liu X, Yang D, Ma X. 2014. Variations of estradiol-17β and testosterone levels correlated with gametogenesis in the gonad of Zhikong scallop (Chlamys farreri) during annual reproductive cycle. Can J Zool. 92(3):195–204. doi: 10.1139/CJZ-2013-0202.
   Google Scholar
• Liu W, Li Q, Kong L. 2008. Estradiol‐17β and testosterone levels in the cockle Fulvia mutica during the annual reproductive cycle. J Mar Freshwat Res. 42(4):417–424. doi: 10.1080/00288330809509970.
   Web of Science ®Google Scholar
• Lu M, Horiguchi T, Shiraishi H, Shibata Y, Abo M, Okubo A, Yamazaki S. 2001. Identification and quantitation of steroid hormones in marine gastropods by GC/MS. Bunseki Kagaku. 50:247–255. doi: 10.2116/BUNSEKIKAGAKU.50.247.
   Web of Science ®Google Scholar
• Minakata H, Tsutsui K. 2016. Oct-GnRH, the first protostomian gonadotropin-releasing hormone-like peptide and a critical mini-review of the presence of vertebrate sex steroids in molluscs. Gen Comp Endocr. 227:109–114. doi: 10.1016/J.YGCEN.2015.07.011.
   PubMed Web of Science ®Google Scholar
• Mindnich R, Möller G, Adamski J. 2004. The role of 17 beta-hydroxysteroid dehydrogenases. Mol Cell Endocrinol. 218(1–2):7–20. doi: 10.1016/j.mce.2003.12.006.
   PubMed Web of Science ®Google Scholar
• Morcillo Y, Porte C. 2000. Evidence of endocrine disruption in clams — Ruditapes decussata — transplanted to a tributyltin-polluted environment. Environ Pollut. 107(1):47–52. doi: 10.1016/s0269-7491(99)00133-5.
   PubMed Web of Science ®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. doi: 10.1016/S0166-445X(97)00102-1.
   Web of Science ®Google Scholar
• Motavkin PA, Varaksin AA, Maslennikova LA, Varaksina GS. 1989. Spermatogenesis in Mizuhopecten yessoensis as a model for valuation gonadotropin activity of the chemical substances. Preprinted. Vladivostok: Institute of Marine Biology Far East Branch Academy of Sciences U.S.S.R. 1989. p. 147.
   Google Scholar
• Motavkin PA, YuS K, Dereidovich I. 1990. Regulation of reproduction and biotechnology of obtaining sex cells at bivalve molluscs. Moscow: Nauka. pp. l–216.
   Google Scholar
• Osada M, Treen N. 2013. Molluscan GnRH associated with reproduction. Gen Comp Endocr. 181:254–258. doi: 10.1016/j.ygcen.2012.09.002.
   PubMed Web of Science ®Google Scholar
• Pak TR, Chung WCJ, Lund TD, Hinds LR, Clay CM, Handa RJ. 2005. The androgen metabolite, 5α-androstane-3β, 17β-diol, is a potent modulator of estrogen receptor-β1-mediated gene transcription in neuronal cells. Endocrinol. 146(1):147–155. doi: 10.1210/en.2004-0871.
   PubMed Web of Science ®Google Scholar
• Pazos AJ, Mathieu M. 1999. Effects of five natural gonadotropin-releasing hormones on cell suspensions of marine bivalve gonad: Stimulation of gonial DNA synthesis. Gen Comp Endocr. 113(1):112–120. doi: 10.1006/gcen.1998.7186.
   PubMed Web of Science ®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 Part A. 95(3):343–348. doi: 10.1016/0300-9629(90)90230-P.
   Google Scholar
• Ronis MJJ, Mason AZ. 1996. The metabolism of testosterone by the periwinkle (Littorina littorea) in vitro and in vivo: Effects of tributyltin. Mar Environ Res. 42(1–4):161–166. doi: 10.1016/0141-1136(95)00069-0.
   Web of Science ®Google Scholar
• Schnaitman C, Greenawalt JW. 1968. Enzymatic properties of the inner and outer membranes of rat liver mitochondria. J Cell Biol. 38(1):158–175. doi: 10.1083/jcb.38.1.158.
   PubMed Web of Science ®Google Scholar
• Schwarz TI, Katsiadaki I, Maskrey BH, Scott AP. 2017a. Mussels (Mytilus spp.) display an ability for rapid and high capacity uptake of the vertebrate steroid, estradiol-17β from water. J Steroid Biochem Mol Biol. 165:407–420. doi: 10.1016/j.jsbmb.2016.08.007.
   PubMed Web of Science ®Google Scholar
• Schwarz TI, Katsiadaki I, Maskrey BH, Scott AP. 2017b. Rapid uptake, biotransformation, esterification and lack of depuration of testosterone and its metabolites by the common mussel, Mytilus spp. J Steroid Biochem Mol Biol. 171:54–65. doi: 10.1016/j.jsbmb.2017.02.016.
   PubMed Web of Science ®Google Scholar
• Schwarz TI, Katsiadaki I, Maskrey BH, Scott AP. 2018. Uptake and metabolism of water-borne progesterone by the mussel, Mytilus spp. J Ster Biochem Mol Bio. 178:13–21. doi:10.1016/j.jsbmb.2017.10.016.
   PubMed Web of Science ®Google Scholar
• Scott AP. 2012. Do mollusks use vertebrate sex steroids as reproductive hormones? Part I: Critical appraisal of the evidence for the presence, biosynthesis and uptake of steroids. Steroids. 77(13):1450–1468. doi: 10.1016/j.steroids.2012.08.009.
   PubMed Web of Science ®Google Scholar
• Shimizu Y, Yarborough CP, Elger W, Chwalisz K, Osawa Y. 1995. Inhibition of aromatase activity in human placental microsomes by 13-retro-antiprogestins. Steroids. 60(2):234–238. doi: 10.1016/0039-128X(94)00043-C.
   PubMed Web of Science ®Google Scholar
• Siah A, Pellerin J, Benosman A, Gagné JP, Amiard JC. 2002. Seasonal gonad progesterone pattern in the soft-shell clam Mya arenaria. Comp Biochem Physiol Part A. 132(2):499–511. doi: 10.1016/S1095-6433(02)00095-8.
   PubMed Web of Science ®Google Scholar
• Smolarz K, Zabrzańska S, Konieczna L, Hallmann A. 2018. Changes in steroid profiles of the blue mussel Mytilus trossulus as a function of season, stage of gametogenesis, sex, tissue and mussel bed depth. Gen Comp Endocr. 259:231–239. doi: 10.1016/j.ygcen.2017.12.006.
   PubMed Web of Science ®Google Scholar
• Sokołowski A, Lasota R, Alias IS, Piłczyńska J, Wołowicz M. 2022. Prospects and opportunities for mussel Mytilus trossulus farming in the southern Baltic Sea (the Gulf of Gdańsk). Oceanol Hydrobio Stud. 51(1):53–73. doi: 10.26881/oahs.2022.1.06.
   Web of Science ®Google Scholar
• Steidle H. 1930. Über die Verbreitung des weiblichen Sexualhormons. Naunyn-Schmiedebergs Archiv für Experimentelle Pathol und Pharmakol. 157(1):89–89. doi: 10.1007/BF01972095.
   Google Scholar
• Thompson EA, Siiteri PK. 1974. Utilization of oxygen and reduced nicotinamide adenine dinucleotide phosphate by human placental microsomes during aromatisation of androstenedione. J Biol Chem. 249(17):5364–5372. doi: 10.1016/S0021-9258(20)79735-8.
   PubMed Web of Science ®Google Scholar
• Wang C, Croll RP. 2006. Effects of sex steroids on spawning in the sea scallop, Placopecten magellanicus. Aquacult. 256(1–4):423–432. doi: 10.1016/j.aquaculture.2006.01.017.
   Google Scholar
• Wenne R. 2015. Microgeographic differentiation in condition and biochemical composition of Macoma balthica (L.) from the Gdansk Bay (South Baltic). Polish Arch Hydrobio. 32:175–194.
   Google Scholar
• Yan H, Li Q, Liu W, Ke Q, Yu R, Kong L. 2011. Seasonal changes of oestradiol-17β and testosterone concentrations in the gonad of the razor clam Sinonovacula constricta (Lamarck, 1818). J Molluscan Stud. 77(2):116–122. doi: 10.1093/mollus/eyq045.
   Google Scholar
• Yang Y, Bao C, Liu A, Ye H, Huang H, Li S. 2014. Immune responses of prophenoloxidase in the mud crab Scylla paramamosain against Vibrio alginolyticus infection: In vivo and in vitro gene silencing evidence. Fish Shellfish Immunol. 39(2):237–244. doi: 10.1016/J.FSI.2014.05.014.
   PubMed Web of Science ®Google Scholar