Imposex development in Hexaplex trunculus (Gastropoda: Caenogastropoda) involves changes in the transcription levels of the retinoid X receptor (RXR)

Chemosphere

Volumn 93, Issue 6, 2013, Pages 1161-1167

  Abidli, Sami ^a   Castro, Luis Filipe Costa ^b   Lahbib, Youssef ^a   Reis Henriques, Maria Armanda ^b   Trigui El Menif, Najoua ^a   Santos, Miguel Machado ^b,c  

^a UNIVERSITY OF CARTHAGE   (Tunisia)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSITY OF PORTO   (Portugal)

Author keywords

Gene expression; Hexaplex trunculus; Imposex; RXR; TBT

Indexed keywords

GENE EXPRESSION; MOLLUSCS; POLYMERASE CHAIN REACTION; TISSUE;

CENTRAL NERVOUS SYSTEMS; EXPERIMENTAL MODELING; HEXAPLEX TRUNCULUS; IMPOSEX; POSITIVE CORRELATIONS; QUANTITATIVE REAL TIME PCR; RETINOID X RECEPTOR; TRANSCRIPTION LEVEL;

TRANSCRIPTION;

ALITRETINOIN; ANDROSTENEDIONE; AROMATASE; CELL NUCLEUS RECEPTOR; NEUROHORMONE; RETINOID X RECEPTOR; TESTOSTERONE; TRIBUTYLTIN;

FEMALE; GASTROPOD; GENE EXPRESSION; IMPOSEX; MALE; NERVOUS SYSTEM; SIGNALING; TRIBUTYLTIN;

ACCESSORY SEX ORGAN; ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; FEMALE; GASTROPOD; GENE EXPRESSION; GENETIC TRANSCRIPTION; HEXAPLEX TRUNCULUS; IMPOSEX DEVELOPMENT; MALE; NONHUMAN; PENIS; REAL TIME POLYMERASE CHAIN REACTION; SEX DIFFERENTIATION; SEXUAL DEVELOPMENT; TARGET ORGAN;

CAENOGASTROPODA; GASTROPODA; HEXAPLEX TRUNCULUS;

GENE EXPRESSION; HEXAPLEX TRUNCULUS; IMPOSEX; RXR; TBT;

ANIMALS; CENTRAL NERVOUS SYSTEM; DISORDERS OF SEX DEVELOPMENT; FEMALE; GASTROPODA; GENE EXPRESSION; MALE; RETINOID X RECEPTORS; TRIALKYLTIN COMPOUNDS; WATER POLLUTANTS, CHEMICAL;

EID: 84885833737     PISSN: 00456535     EISSN: 18791298     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2013.06.054     Document Type: Article

References (54)

1. Abidli S., Lahbib Y., Trigui-El Menif N. Effects of TBT on the imposex development, reproduction and mortality in Hexaplex trunculus (Gastropoda: Muricidae). J. Mar. Biol. Assoc. UK 2009, 89:139-146.
2. Abidli S., Lahbib Y., Trigui El Menif N. Relative growth and reproductive cycle in two populations of Bolinus brandaris (Gastropoda: Muricidae) from northern Tunisia (Bizerta Lagoon and small Gulf of Tunis). Biologia 2012, 67:751-761.
3. Abidli S., Santos M.M., Lahbib Y., Castro L.F.C., Reis-Henriques M.A., Trigui El Menif N. Tributyltin (TBT) effects on Hexaplex trunculus and Bolinus brandaris (Gastropoda: Muricidae): imposex induction and sex hormone levels insights. Ecol. Indic. 2012, 13:13-21.
4. Axiak V., Vella A.J., Micaleff D., Chircop P. Imposex in Hexaplex trunculus (Gastropoda: Muricidae): first results from biomonitoring of tributyltin contamination in the Mediterranean. Mar. Biol. 1995, 121:685-691.
5. 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.
6. Bouton D., Escriva H., de Mendonca R.L., Glineur C., Bertin B., Noel C., Robinson-Rechavi M., de Groot A., Cornette J., Laudet V., Pierce R.J.A. Conserved retinoid X receptor (RXR) from the mollusc Biomphalaria glabrata transactivates transcription in the presence of retinoids. J. Mol. Endocrinol. 2005, 34:567-582.
7. Bryan G.W., Gibbs P.E., Hummerstone L.G., Burt G.R. The decline of the gastropod Nucella lapillus around southwest England: evidence for the effect of tributyltin from antifouling paints. J. Mar. Biol. Assoc. UK 1986, 66:611-618.
8. Castro L.F., Santos M.M., Reis-Henriques M.A. The genomic environment around the Aromatase gene: evolutionary insights. BMC Evolut. Biol. 2005, 5:43.
9. 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 in mediated through the Retinoid X Receptor signalling pathway in the neogastropod Nucella lapillus. Aquat. Toxicol. 2007, 85:57-66.
10. Cooke G.M. Effect of organotins on human aromatase activity in vitro. Toxicol. Lett. 2002, 126:121-130.
11. Créton R., Zwaan G., Gohmen R. Specific developmental defects in molluscs after treatment with retinoic acid during gastrulation. Dev. Growth Differ. 1993, 35:357-364.
12. Féral C., Le Gall S. The influence of a pollutant factor (tributyltin) on the neuroendocrine mechanism responsible for the occurence of a penis in the females of Ocenebra erinacea. Molluscan Neuroendocrinology 1983, 173-175. North Holland, Amsterdam. J. Lever, H.H. Boer (Eds.).
13. Gesto M., Castro L.F., Reis-Henriques M.A., Santos M.M. Retinol metabolism in the mollusk Osilinus lineatus indicates an ancient origin for retinyl ester storage capacity. PLoS ONE 2012, 7(4):e35138.
14. Gibbs P.E., Bryan G.W. Reproductive failure in populations of the dog-whelk, Nucella lapillus, caused by imposex undiced by tributyltin from antifouling paints. J. Mar. Biol. Assoc. UK 1986, 66:767-777.
15. Gibbs P.E., Bryan G.W., Pascoe P.L., Burt G.R. The use of the dogwhelk, Nucella lapillus, as an indicator of tributyltin (TBT) contamination. J. Mar. Biol. Assoc. UK 1987, 67:507-523.
16. Gooding M.P., LeBlanc G.A. Biotransformation and disposition of testosterone in the eastern mud snail Ilyanassa obsoleta. Gen. Comp. Endocrinol. 2001, 122:172-180.
17. 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.
18. Heidrich D.D., Steckelbroeck S., Klingmuller D. Inhibition of human cytochrome P450 aromatase activity by butyltins. Steroids 2001, 66:763-769.
19. Horiguchi T., Nishikawa T., Ohta Y., Shiraishi H., Morita M. Retinoid X receptor gene expression and protein content in tissues of the rock shell Thais clavigera. Aquat. Toxicol. 2007, 84:379-388.
20. Horiguchi T., Nishikawa T., Ohta Y., Shiraishi H., Morita M. Time course of expression of the retinoid X receptor gene and induction of imposex in the rock shell, Thais clavigera, exposed to triphenyltin chloride. Anal. Bioanal. Chem. 2010, 396:597-607.
21. Janer G., Sternberg R.M., LeBlanc G.A., Porte C. Testosterone conjugating activities in invertebrates: are they targets for endocrine disruption?. Aquat. Toxicol. 2005, 71:273-282.
22. Janer G., Lyssimachou A., Bachmann J., Oehlmann J., Schulte-Oehlmann U., Porte C. Sexual dimorphism in esterified steroid levels in the gastropod Marisa cornuarietis: the effect of xenoandrogenic compounds. Steroids 2006, 71:435-444.
23. Lahbib Y., Abidli S., Le Pennec M., Flawoer R., Trigui El Menif N. Morphological expression and different stages of imposex in Hexaplex trunculus (Neogastropoda: Muricidae) from Tunisian coasts. Cah. Biol. Mar. 2007, 48:315-326.
24. Le Gall S., Feral C., Lengronne C., Porchet M. Partial purification of the neuroendocrine mitogenic factor in the mollusc Crepidula fornicata L. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 1987, 86:393-396.
25. Lima D., Reis-Henriques M.A., Silva R., Santos A.I., Castro L.F., Santos M.M. Tributyltin-induced imposex in marine gastropods involves tissue-specific modulation of the Retinoid X Receptor. Aquat. Toxicol. 2011, 101:221-227.
26. Livak K.J., Schmittgen T.D. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2-[Delta][Delta]CT Method. Methods 2001, 25:402-408.
27. Markov G.V., Tavares R., Dauphin-Villemant C., Demeneix B.A., Baker M.E., Laudet V. Independent elaboration of steroid hormone signaling pathways in metazoans. Proc. Natl. Acad. Sci. USA 2009, 106:11913-11918.
28. Matthiessen P., Gibbs P.E. Critical appraisal of the evidence for tributyltin-mediated endocrine disruption in mollusks. Environ. Toxicol. Chem. 1998, 17:37-43.
29. Morcillo Y., Porte C. Evidence of endocrine disruption in the imposex-affected gastropod Bolinus brandaris. Environ. Res. 1999, 81:349-354.
30. Morcillo Y., Porte C. Evidence of endocrine disruption in clams Ruditapes decussatus transplanted to a tributyltin-polluted environment. Environ. Pollut. 2000, 107:47-52.
31. Morcillo Y., Ronis M.J.J., Porte C. Effects of tributyltin on phase I testosterone metabolism and steroid titres of the clam Ruditapes decussatus. Aquat. Toxicol. 1998, 42:1-13.
32. Nishikawa J.-i., 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.
33. Oberdörster E., McClellan-Green P. The neuropeptide APGWamide induces imposex in the mud snail, Ilyanassa obsoleta. Peptides 2000, 21:1323-1330.
34. Oberdörster E., McClellan-Green P. Mechanisms of imposex induction in the mud snail Ilyanassa obsoleta: TBT as a neurotoxin and aromatase inhibitor. Mar. Environ. Res. 2002, 54:715-718.
35. Pascoal S., Carvalho G., Vasieva O., Hughes R., Cossins A., Fang Y., Ashelford K., Olohan L., Barroso C., Mendo S., Creer S. Transcriptomics and in vivo tests reveal novel mechanisms underlying endocrine disruption in an ecological sentinel, Nucella lapillus. Mol. Ecol. 2012, 22:1589-1608.
36. Romero R., Bueno D. Disto-proximal regional determination and intercalary regeneration in planarians, revealed by retinoic acid induced disruption of regeneration. Int. J. Dev. Biol. 2001, 45:669-673.
37. Ronis M.J.J., Mason A.Z. The metabolism of testosterone by periwinkle (Littorina littorea) in vitro and in vivo: effects of tributyltin. Mar. Environ. Res. 1996, 42:161-166.
38. Santos M.M., Vieira N., Santos A.M. Imposex in the dogwhelk Nucella lapillus(L.) along the Portuguese coast. Mar. Pollut. Bull. 2000, 40:643-646.
39. Santos M.M., ten Hallers-Tjabbes C.C., Vieira N., Boon J.P., Porte C. Cytochrome P450 differences in normal and imposex-affected female whelk Buccinum undatum from the open North Sea. Mar. Environ. Res. 2002, 54:661-665.
40. Santos M.M., Filipe L.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. Phys. C. 2005, 141:101-109.
41. Santos M.M., Reis-Henriques M.A., Vieira M.N., Solé M. Triphenyltin and tributyltin, single and in combination, promote imposex in the gastropod Bolinus brandaris. Ecotox. Environ. Safe. 2006, 64:155-162.
42. 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.
43. Schulte-Oehlmann U., Tillmann M., Markert B., Oehlmann J. Effects of endocrine disruptors on prosobranch snails (Mollusca: Gastropoda) in the laboratory, part II: triphenyltin as a xenoandrogen. Ecotoxicology 2000, 9:399-412.
44. Shi H.H., Huang C.J., Zhu S.X., Yu X.J., Xie W.Y. Generalized system of imposex and reproductive failure in female gastropods of coastal waters of mainland China. Mar. Ecol. Prog. Ser. 2005, 304:179-189.
45. Schulte-Oehlmann U., Oehlmann J., Fioroni P., Bauer B. Imposex and reproductive failure in Hydrobia ulvae (Gastropoda: Prosobranchia). Mar. Biol. 1997, 128:257-266.
46. Simões-costa M.S., Azambuja A.P., Xavier-Neto J. The search for non-chordate retinoic acid signaling: lessons from chordates. J. Exp. Zool. B Mol. Dev. Evol. 2008, 310:54-72.
47. Smith B.S. Sexuality in the American mud snail Nassarius obsoletus Say. Proc. Malacol Soc. London 1971, 39:377-378.
48. 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.
49. Stange D., Sieratowicz A., Oehlmann J. Imposex development in Nucella lapillus - Evidence for the involvement of retinoid X receptor and androgen signalling pathways in vivo. Aquat. Toxicol. 2012, 106-107:20-24.
50. Sternberg R.M., LeBlanc G.A. Kinetic characterization of the inhibition of acyl coenzyme A: steroid acyltransferase by tributyltin in the eastern mud snail (Ilyanassa obsoleta). Aquat. Toxicol. 2006, 78:233-242.
51. Sternberg R.M., Gooding M.P., Hotchkiss A.K., LeBlanc G.A. Environmental-endocrine control of reproductive maturation in gastropods: implications for the mechanism of tributyltin-induced imposex in prosobranchs. Ecotoxicology 2010, 19:4-23.
52. Stroben E., Oehlmann J., Fioroni P. The mor-phological expression of imposex in Hinia reticulata (Gastropoda: Buccinidae): a potential indicator of tributyltin pollution. Mar. Biol. 1992, 113:625-636.
53. Titley-O'Neal C.P., Munkittrick K.R., Macdonald B.A. The effects of organotin on female gastropods. J. Environ. Monit. 2011, 13:2360-2388.
54. Trigui El Menif N., Lahbib Y., Le Pennec M., Flower R., Boumaiza M. Intensity of the imposex phenomenon - impact on growth and fecundity in Hexaplex trunculus (Mollusca: Gastropoda) collected in Bizerta lagoon and channel (Tunisia). Cah. Biol. Mar. 2006, 47:1-11.