Imposex development in Nucella lapillus - Evidence for the involvement of retinoid X receptor and androgen signalling pathways in vivo

Aquatic Toxicology

Volumn 106-107, Issue , 2012, Pages 20-24

  Stange, Daniela ^a   Sieratowicz, Agnes ^a   Oehlmann, Jörg ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

9 cis retinoic acid; Aromatase; Endocrine disruption; HX531; HX630; Masculinisation

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; ALITRETINOIN; ANDROGEN; CYPROTERONE ACETATE; HX 531; HX 630; RECEPTOR BLOCKING AGENT; RETINOID X RECEPTOR; TRIBUTYLTIN; UNCLASSIFIED DRUG;

BIOCHEMISTRY; ENDOCRINE DISRUPTOR; ENZYME; GASTROPOD; IMPOSEX; INHIBITION; MASCULINIZATION; ORGANIC ACID; ORGANOTIN COMPOUND; POLLUTION EFFECT; SIGNALING; TESTING METHOD;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; FEMALE; IMPOSEX DEVELOPMENT; IN VIVO STUDY; MARINE SNAIL; NONHUMAN; NUCELLA LAPILLUS; PRIORITY JOURNAL; SEXUAL DEVELOPMENT; SIGNAL TRANSDUCTION;

ANDROGENS; ANIMALS; AROMATASE; AROMATASE INHIBITORS; DISORDERS OF SEX DEVELOPMENT; ENDOCRINE DISRUPTORS; ENDOCRINE SYSTEM; FEMALE; GASTROPODA; RETINOID X RECEPTORS; SIGNAL TRANSDUCTION; TRIALKYLTIN COMPOUNDS; WATER POLLUTANTS, CHEMICAL;

GASTROPODA; NUCELLA LAPILLUS;

EID: 80155214503     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2011.10.010     Document Type: Article

References (35)

1. Albanis, T., Allera, A., Bachmann, J., Barbaglio, A., Berntsson, P., Dittmann, N., Carnevali, D.C., Ciceri, F., Dagnac, T., Duft, M., Falandysz, J., Galassi, S., Hala, D., Janer, G., Jeannot, R., Jobling, S., King, I., Klingmüller, D., Kloas, W., Kusk, K.O., Lavado, R., Lo, S., Lutz, I., Oehlmann, J., Oredsson, S., Porte, C., Rand-Weaver, M., Sakkas, V., Schmitt, C., Schulte-Oehlmann, U., Sugni, M., Tyler, X., van Aerle, R., van Ballegoy, C., Wollenberger, L., 2006. Executive summary on the project results of COMPRENDO - comparative research on endocrine disrupters (EU project no. EVK1-CT-2002-00129). Available online under http://www.comprendo-project.org/.
2. Bettin C., Oehlmann J., Stroben E. TBT-induced imposex in marine neogastropods is mediated by an increasing androgen level. Helgol. Meeresunters. 1996, 50:299-317.
3. Bryan G.W., Gibbs P.E., Burt G.R. A comparison of the effectiveness of tri-n-butyltin chloride and five other organotin compounds in promoting the development of imposex in the dog-whelk, Nucella lapillus. J. Mar. Biol. Assoc. U.K. 1988, 68:733-744.
4. Carter C.J., Farrar N., Carlone R.L., Spencer G.E. Developmental expression of a molluscan RXR and evidence for its novel, nongenomic role in growth cone guidance. Dev. Biol. 2010, 343:124-137.
5. Castro L.F.C., Lima D., Machado A., Melo C., Hiromori Y., Nishikawa J., Nakanishi T., Reis-Henriques M.A., Santos M.M. Imposex induction is mediated through the retinoid X receptor signalling pathway in the neogastropod Nucella lapillus. Aquat. Toxicol. 2007, 85:57-66.
6. Chuang K.H., Lee Y.F., Lin W.J., Chu C.Y., Altuwaijri S., Wan Y.J.Y., Chang C.S. 9-cis-retinoic acid inhibits androgen receptor activity through activation of retinoid X receptor. Mol. Endocrinol. 2005, 19:1200-1212.
7. de Urquiza A.M., Liu S.Y., Sjoberg M., Zetterstrom R.H., Griffiths W., Sjovall J., Perlmann T. Docosahexaenoic acid, a ligand for the retinoid X receptor in mouse brain. Science 2000, 290:2140-2144.
8. Fioroni P., Oehlmann J., Stroben E. The pseudohermaphroditism of prosobranchs - morphological aspects. Zool. Anz. 1991, 226:1-26.
9. Gooding M.P., Wilson V.S., Folmar L.C., Marcovich D.T., LeBlanc G.A. The biocide tributyltin reduces the accumulation of testosterone as fatty acid esters in the mud snail (Ilyanassa obsoleta). Environ. Health Perspect. 2003, 111:426-430.
10. Haraguchi G., Suzuki J.I., Kosuge H., Ogawa M., Koga N., Muto S., Itai A., Kagechika H., Shudo K., Isobe M. A new RXR agonist, HX630, suppresses intimal hyperplasia in a mouse blood flow cessation model. J. Mol. Cell. Cardiol. 2006, 41:885-892.
11. Heidrich D.D., Steckelbroeck S., Klingmuller D. Inhibition of human cytochrome p450 aromatase activity by butyltins. Steroids 2001, 66:763-769.
12. Horiguchi T., Shiraishi H., Shimizu M., Morita M. Imposex in sea snails, caused by organotin (tributyltin and triphenyltin) pollution in Japan: a survey. Appl. Organomet. Chem. 1997, 11:451-455.
13. Horiguchi T., Ohta Y., Nishikawa T., Shiraishi F., Shiraishi H., Morita M. Exposure to 9-cis retinoic acid induces penis and vas deferens development in the female rock shell, Thais clavigera. Cell Biol. Toxicol. 2008, 24:553-562.
14. Kanayasu-Toyoda T., Fujino T., Oshizawa T., Suzuki T., Nishimaki-Mogami T., Sato Y., Sawada J., Inoue K., Shudo K., Ohno Y., Yamaguchi T. HX531, a retinoid X receptor antagonist, inhibited the 9-cis retinoic acid-induced binding with steroid receptor coactivator-1 as detected by surface plasmon resonance. J. Steroid Biochem. Mol. Biol. 2005, 94:303-309.
15. Laudet V., Gronemeyer H. The Nuclear Receptor Facts Book 2002, Academic Press, London.
16. Lima D., Reis-Henriques M.A., Silva R., Santos A.I., Castro L.F.C., Santos M.M. Tributyltin-induced imposex in marine gastropods involves tissue-specific modulation of the retinoid X receptor. Aquat. Toxicol. 2011, 101:221-227.
17. Matthiessen P., Gibbs P.E. Critical appraisal of the evidence for tributyltin-mediated endocrine disruption in mollusks. Environ. Toxicol. Chem. 1998, 17:37-43.
18. Nishikawa J., Mamiya S., Kanayama T., Nishikawa T., Shiraishi F., Horiguchi T. Involvement of the retinoid X receptor in the development of imposex caused by organotins in gastropods. Environ. Sci. Technol. 2004, 38:6271-6276.
19. Oehlmann J., Stroben E., Fioroni P. The morphological expression of imposex in Nucella lapillus (Linnaeus) (Gastropoda: Muricidae). J. Moll. Stud. 1991, 57:375-390.
20. Oehlmann J., Bauer B., Minchin D., Schulte-Oehlmann U., Fioroni P., Markert B. Imposex in Nucella lapillus and intersex in Littorina littorea: interspecific comparison of two TBT-induced effects and their geographical uniformity. Hydrobiologia 1998, 378:199-213.
21. Oehlmann J., Di Benedetto P., Tillmann M., Duft M., Oetken M., Schulte-Oehlmann U. Endocrine disruption in prosobranch molluscs: evidence and ecological relevance. Ecotoxicology 2007, 16:29-43.
22. Ronis M.J.J., Mason A.Z. The metabolism of testosterone by the periwinkle (Littorina littorea) in vitro and in vivo: effects of tributyl tin. Mar. Environ. Res. 1996, 42:161-166.
23. Saitoh M., Yanase T., Morinaga H., Tanabe M., Mu Y.M., Nishi Y., Nomura M., Okabe T., Goto K., Takayanagi R., Nawata H. Tributyltin or triphenyltin inhibits aromatase activity in the human granulosa-like tumor cell line KGN. Biochem. Biophys. Res. Commun. 2001, 289:198-204.
24. Santos M.M., Castro L.F.C., Vieira M.N., Micael J., Morabito R., Massanisso P., Reis-Henriques M.A. New insights into the mechanism of imposex induction in the dogwhelk Nucella lapillus. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2005, 141:101-109.
25. Schulte-Oehlmann U., Bettin C., Fioroni P., Oehlmann J., Stroben E. Marisa cornuarietis (Gastropoda, Prosobranchia): a potential TBT bioindicator for freshwater environments. Ecotoxicology 1995, 4:372-384.
26. Schulte-Oehlmann U., Watermann B., Tillmann M., Scherf S., Markert B., Oehlmann J. Effects of endocrine disruptors on prosobranch snails (Mollusca: Gastropoda) in the laboratory. Part II: Triphenyltin as a xeno-androgen. Ecotoxicology 2000, 9:399-412.
27. Smith B.S. Male characteristics on female mud snails caused by antifouling bottom paints. J. Appl. Toxicol. 1981, 1:22-25.
28. Spooner N., Gibbs P.E., Bryan G.W., Goad L.J. The effect of tributyltin upon steroid titres in the female dogwhelk, Nucella lapillus, and the development of imposex. Mar. Environ. Res. 1991, 32:37-49.
29. Sternberg R.M., Hotchkiss A.K., Leblanc G.A. Synchronized expression of retinoid X receptor mRNA with reproductive tract recrudescence in an imposex-susceptible mollusc. Environ. Sci. Technol. 2008, 42:1345-1351.
30. Stroben E., Oehlmann J., Bettin C. TBT-induced imposex and the role of steroids in marine snails. Proceedings of the Tenth World Meeting of ORTEP (Organotin Environmental Programme) Association 1991, 68-73. J.A. Jonker (Ed.).
31. Stroben E., Oehlmann J., Fioroni P. Hinia reticulata and Nucella lapillus, comparison of two gastropod tributyltin bioindicators. Mar. Biol. 1992, 114:289-296.
32. Tillmann, M., 2004. Sediment toxicological investigations using gastropods and insects, with special emphasis on endocrine active substances. Göttingen, Cuvillier. (in German).
33. Umemiya H., Fukasawa H., Ebisawa M., Eyrolles L., Kawachi E., Eisenmann G., Gronemeyer H., Hashimoto Y., Shudo K., Kagechika H. Retinobenzoic acids. VIII. Regulation of retinoidal actions by diazepinylbenzoic acids. Retinoid synergists which activate the RXR-RAR heterodimers. J. Med. Chem. 1997, 40:4222-4234.
34. Urushitani H., Katsu Y., Ohta Y., Shiraishi H., Iguchi T., Horiguchi T. Cloning and characterization of retinoid X receptor (RXR) isoforms in the rock shell, Thais clavigera. Aquat. Toxicol. 2011, 103:101-111.
35. Zheng R.H., Wang C.G., Zhao Y., Zu Z.H., Chen Y.X. Effect of tributyltin, benzo(a)pyrene and their mixture exposure on the sex hormone levels in gonads of cuvier (Sebastiscus marmoratus). Environ. Toxicol. Pharmacol. 2005, 20:361-367.