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Ecotoxicology of Antifouling Biocides pp 111–123Cite as

Mechanism of Imposex Induced by Organotins in Gastropods

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Certain environmental chemicals cause feminization of males and/or masculinization of females, and such phenomena are generally called endocrine disruption (Colborn et al. 1996). The current status of studies of endocrine disruption both in wildlife and humans is reviewed by the International Programme on Chemical Safety (IPCS) under the joint work of the United Nations Environment Programme (UNEP), the International Labour Organization (ILO) and the World Health Organization (WHO) (International Programme on Chemical Safety 2002). Here, the author will review the masculinization of female gastropod mollusks, called imposex, in terms of the basic biology and induction mechanism of imposex.

The first report of masculinized female gastropods was made by Blaber (1970), describing a penis-like outgrowth behind the right tentacle in spent females of the dog-whelk, Nucella lapillus around Plymouth, UK. The term imposex, however, was coined by Smith (1971) to describe the syndrome of a superimposition of male type genital organs, such as the penis and vas deferens, on female gastropods. Imposex is thought to be irreversible (Bryan et al. 1986). Reproductive failure may occur in females with severe imposex, resulting in population decline or even mass extinction (Gibbs and Bryan 1986, 1996). In some species, imposex is typically induced by tributyltin (TBT) and triphenyltin (TPT), chemicals released from antifouling paints used on ships and fishing nets (Bryan et al. 1987, 1988; Gibbs et al. 1987; Horiguchi et al. 1995, 1997a).

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References

  • Bech M (2002a) A survey of imposex in muricids from 1996 to 2000 and identification of optimal indicators of tributyltin contamination along the east coast of Phuket Island, Thailand. Mar Pollut Bull 44:887–896.

    Article  CAS  Google Scholar 

  • Bech M (2002b) Imposex and tributyltin contamination as consequence of the establishment of a marina and increasing yachting activities at Phuket Island, Thailand. Environ Pollut 117:421–429.

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Blaber SJM (1970) The occurrence of a penis-like outgrowth behind the right tentacle in spent females of Nucella lapillus (L.). Proc Malacol Soc Lond 39:231–233.

    Google Scholar 

  • Bryan GW, Gibbs PE, Hummerstone LG et al. (1986) The decline of the gastropod Nucella lapil-lus around south-west England: evidence for the effect of tributyltin from antifouling paints. J Mar Biol Assoc UK 66:611–640.

    CAS  Google Scholar 

  • Bryan GW, Gibbs PE, Burt GR et al. (1987) The effects of tributyltin (TBT) accumulation on adult dog-whelks, Nucella lapillus: long-term field and laboratory experiments. J Mar Biol Assoc UK 67:525–544.

    CAS  Google Scholar 

  • Bryan GW, Gibbs PE, Burt GR (1988) 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 UK 68:733–744.

    CAS  Google Scholar 

  • Bryan GW, Bright DA, Hummerstone LG et al. (1993) Uptake, tissue distribution and metabolism of 14C-labelled tributyltin (TBT) in the dog-whelk, Nucella lapillus. J Mar Biol Assoc UK 73:889–912.

    CAS  Google Scholar 

  • Castro LFC, Lima D, Machado A et al. (2007) Imposex induction is mediated through the Retinoid X Receptor signalling pathway in the neogastropod Nucella lapillus. Aquat Toxicol 85:57–66.

    Article  CAS  Google Scholar 

  • Chiu AY, Hunkapiller MW, Heller E et al. (1979) Purification and primary structure of neuropep-tide egg-laying hormone of Aplysia californica. Proc Natl Acad Sci USA 76:6656–6660.

    Article  CAS  Google Scholar 

  • Colborn T, Dumanoski D, Myers JP (1996) Our Stolen Future. Dutton, New York: 306p.

    Google Scholar 

  • Ebberink RHM, Loenhout H, van Geraerts WPM et al. (1985) Purification and amino acid sequence of the ovulation neurohormone of Lymnaea stagnalis. Proc Natl Acad Sci USA 82:7767–7771.

    Article  CAS  Google Scholar 

  • Escriva H, Safi R, Hänni C et al. (1997) Ligand binding was acquired during evolution of nuclear receptors. Proc Natl Acad Sci USA 94:6803–6808.

    Article  CAS  Google Scholar 

  • Féral C, Le Gall S (1983) The influence of a pollutant factor (TBT) on the neurosecretory mechanism responsible for the occurrence of a penis in the females of Ocenebra erinacea. In: Lever J, Boer HH (eds) Molluscan Neuro-Endocrinology. North-Holland, Amsterdam: pp.173–175.

    Google Scholar 

  • Fioroni P, Oehlmann J, Stroben E (1991) The pseudohermaphroditism of prosobranchs; morphological aspects. Zool Anz 226:1–26.

    Google Scholar 

  • Gibbs PE, Bryan GW (1986) Reproductive failure in populations of the dog-whelk, Nucella lapillus, caused by imposex induced by tributyltin from antifouling paints. J Mar Biol Assoc UK 66:767–777.

    CAS  Google Scholar 

  • Gibbs PE, Bryan GW (1996) TBT-induced imposex in neogastropod snails: masculinization to mass extinction. In: de Mora SJ (ed) Tributyltin: Case Study of an Environmental Contaminant. Cambridge University Press, Cambridge: pp.212–236.

    Google Scholar 

  • Gibbs PE, Bryan GW, Pascoe PL et al. (1987) The use of the dog-whelk, Nucella lapillus, as anindicator of tributyltin (TBT) contamination. J Mar Biol Assoc UK 67:507–523.

    CAS  Google Scholar 

  • Gibbs PE, Pascoe PL, Burt GR (1988) Sex change in the female dog-whelk, Nucella lapillus, induced by tributyltin from antifouling paints. J Mar Biol Assoc UK 68:715–731.

    Google Scholar 

  • Gibbs PE, Bryan GW, Pascoe PL et al. (1990) Reproductive abnormalities in female Ocenebraerinacea (Gastropoda) resulting from tributyltin-induced imposex. J Mar Biol Assoc UK 70:639–656.

    Article  Google Scholar 

  • Gibbs PE, Spencer BE, Pascoe PL (1991) The American oyster drill, Urosalpinx cinerea (Gastropoda): evidence of decline in an imposex affected population (R. Blackwater, Essex). J Mar Biol Assoc UK 71:827–838.

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Horiguchi T (2000) Molluscs. In: Kawai S, Koyama J (eds) Problems of Endocrine Disruptors in Fisheries Environment. [in Japanese] Koseisha-Koseikaku, Tokyo: pp.54–72.

    Google Scholar 

  • Horiguchi T (2006) Masculinization of female gastropod molluscs induced by organotin compounds, focusing on mechanism of actions of tributyltin and triphenyltin for development of imposex. Environ Sci 13:77–87.

    CAS  Google Scholar 

  • Horiguchi T, Shimizu M (1992) Effects on aquatic organisms, mainly on molluscs. In: Satomi Y, Shimizu M (eds) Organotin Pollution and Its Effects on Aquatic Organisms. [in Japanese] Koseisha-Koseikaku, Tokyo: pp.99–135.

    Google Scholar 

  • Horiguchi T, Shiraishi H, Shimizu M et al. (1994) Imposex and organotin compounds in Thais clavigera and T. bonni in Japan. J Mar Biol Assoc UK 74:651–669.

    CAS  Google Scholar 

  • Horiguchi T, Shiraishi H, Shimizu M et al. (1995) Imposex in Japanese gastropods (Neogastropoda and Mesogastropoda): effects of tributyltin and triphenyltin from antifouling paints. Mar Pollut Bull 31:402–405.

    Article  CAS  Google Scholar 

  • Horiguchi T, Shiraishi H, Shimizu M et al. (1997a) Effects of triphenyltin chloride and five other organotin compounds on the development of imposex in the rock shell, Thais clavigera. Environ Pollut 95:85–91.

    Article  CAS  Google Scholar 

  • Horiguchi T, Shiraishi H, Shimizu M et al. (1997b) Imposex in sea snails, caused by organotin (tributyltin and triphenyltin) pollution in Japan: a survey. Appl Organomet Chem 11:451–455.

    Article  CAS  Google Scholar 

  • Horiguchi T, Takiguchi N, Cho HS et al. (2000) Ovo-testis and disturbed reproductive cycle in the giant abalone, Haliotis madaka: possible linkage with organotin contamination in a site of population decline. Mar Environ Res 50:223–229.

    Article  CAS  Google Scholar 

  • Horiguchi T, Kojima M, Kaya M et al. (2002) Tributyltin and triphenyltin induce spermatogenesis in ovary of female abalone, Haliotis gigantea. Mar Environ Res 54:679–684.

    Article  CAS  Google Scholar 

  • Horiguchi T, Shiraishi H, Morita M (2003) Specific tissue distributions of organotin compounds in prosobranch gastropods. [Abstract] SETAC 24th Annual Meeting Abstract Book p.290.

    Google Scholar 

  • Horiguchi T, Kojima M, Takiguchi N et al. (2005) Continuing observation of disturbed reproductive cycle and ovarian spermatogenesis in the giant abalone, Haliotis madaka, from an organotin-contaminated site of Japan. Mar Pollut Bull 51:817–822.

    Article  CAS  Google Scholar 

  • Horiguchi T, Kojima M, Hamada F et al. (2006) Impact of tributyltin and triphenyltin on ivory shell (Babylonia japonica) populations. Environ Health Persp 114:Supplement 1:13–19.

    Google Scholar 

  • Horiguchi T, Nishikawa T, Ohta Y et al. (2007a) Retinoid X receptor gene expression and protein content in tissues of the rock shell Thais clavigera. Aquat Toxicol 84:379–388.

    Article  CAS  Google Scholar 

  • Horiguchi T, Ohta Y, Nishikawa T et al. (2007b) Exposure to 9-cis retinoic acid induces penis and vas deferens development in the female rock shell, Thais clavigera. Cell Biol Toxicol doi:10.1007/s10565-007-9051-9.

    Google Scholar 

  • Iguchi T, Katsu Y, Horiguchi T et al. (2007) Endocrine disrupting organotin compounds are potent inducers of imposex in gastropods and adipogenesis in vertebrates. Mol Cell Toxicol 3:1–10.

    Google Scholar 

  • International Programme on Chemical Safety (2002) Global Assessment of the State-of-the-Science of Endocrine Disruptors (Damstra T, Barlow S, Bergman A, Kavlock R, Kraak GVD (eds) ). WHO/PCS/EDC/02.2, 180 p.

    Google Scholar 

  • Joosse J, Geraerts WPM (1983) Endocrinology. In: Saleuddin ASM, Wilbur KM (eds) The Mollusca Vol. 4 Physiology Part 1. Academic, New York: pp.317–406.

    Google Scholar 

  • Kajiwara M, Kuraku S, Kurokawa T et al. (2006) Tissue preferential expression of estrogen receptor gene in the marine snail, Thais clavigera. Gen Comp Endocrinol 148:315–26. Epub 2006 Jun 19.

    Article  CAS  Google Scholar 

  • LeBlanc GA, Campbell PM, den Besten P et al. (1999) The endocrinology of invertebrates. In: deFur PL, Crane M, Ingersoll C, Tattersfield L (eds) Endocrine Disruption in Invertebrates: Endocrinology, Testing, and Assessment. SETAC Press, Pensacola, FL: pp.23–106.

    Google Scholar 

  • Le Guellec D, Thiard MC, Remy-Martin JP et al. (1987) In vitro metabolism of androsten-edione and identification of endogenous steroids in Helix aspersa. Gen Comp Endocrinol 66:425–433.

    Article  Google Scholar 

  • Lu M, Horiguchi T, Shiraishi H et al. (2001) Identification and quantitation of steroid hormones in marine gastropods by GC/MS. [in Japanese] Bunseki Kagaku 50:247–255.

    CAS  Google Scholar 

  • Marshall DJ, Rajkumar A (2003) Imposex in the indigenous Nassarius kraussianus (Mollusca: Neogastropoda) from South African harbours. Mar Pollut Bull 46:1150–1155.

    Article  CAS  Google Scholar 

  • Matthiessen P, Gibbs PE (1998) Critical appraisal of the evidence for tributyltin-mediated endocrine disruption in mollusks. Environ Toxicol Chem 17:37–43.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Morishita F, Minakata H, Takeshige K et al. (2006) Novel excitatory neuropeptides isolated from a prosobranch gastropod, Thais clavigera: the molluscan counterpart of the annelidan GGNG peptides. Peptides 27:483–492.

    Article  CAS  Google Scholar 

  • Nishikawa J, Mamiya S, Kanayama T et al. (2004) Involvement of the retinoid X receptor in the development of imposex caused by organotins in gastropods. Environ Sci Technol 38:6271–6276.

    Article  CAS  Google Scholar 

  • Oberdörster E, McClellan-Green P (2000) The neuropeptide APGWamide induces imposex in the mud snail Ilyanassa obsoleta. Peptides 21:1323–1330.

    Article  Google Scholar 

  • Oberdörster E, McClellan-Green P (2002) Mechanism of imposex induction in mud snail, Ilyanassaobsoleta: TBT as a neurotoxin and aromatase inhibitor. Mar Environ Res 54:715–718.

    Article  Google Scholar 

  • Oehlmann J, Fioroni P, Stroben E et al. (1996) Tributyltin (TBT) effects on Ocinebrina aciculata (Gastropoda: Muricidae): imposex development, sterilization, sex change and population decline. Sci Total Environ 188:205–223.

    Article  CAS  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 42:161–166.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Santos MM, Castro LF, Vieira MN et al (2005) New insights into the mechanism of imposex induction in the dogwhelk Nucella lapillus. Comp Biochem Physiol C Toxicol Pharmacol 141:101–109.

    Article  CAS  Google Scholar 

  • Schulte-Oehlmann U, Oehlmann J, Fioroni P et al (1997) Imposex and reproductive failure in Hydrobia ulvae (Gastropoda: Prosobranchia). Mar Biol 128:257–266.

    Article  Google Scholar 

  • Smith BS (1971) Sexuality in the American mud snail, Nassarius obsoletus Say. Proc Malacol Soc Lond 39:377–378.

    Google Scholar 

  • Sole M, Morcillo Y, Porte C (1998) Imposex in the commercial snail Bolinus brandaris in the northwestern Mediterranean. Environ Pollut 99:241–246.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Takeda N (1983) Endocrine regulation of reproduction in the snail, Euhadra peliomphala. In: Lever J, Boer HH (eds) Molluscan Neuro-endocrinology. North-Holland, Amsterdam: pp.106–111.

    Google Scholar 

  • ten Hallers-Tjabbes CC, Wegener JW, Van Hattum BA et al (2003) Imposex and organotin concentrations in Buccinum undatum and Neptunea antiqua from the North Sea: relationship to shipping density and hydrographical conditions. Mar Environ Res 55:203–233.

    Article  CAS  Google Scholar 

  • Terlizzi A, Delos AL, Garaventa F et al (2004) Limited effectiveness of marine protected areas: imposex in Hexaplex trunculus (Gastropoda: Muricidae) populations from Italian marine reserves. Mar Pollut Bull 48:188–192.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Yamabe Y, Hoshino A, Imura N et al (2000) Enhancement of androgen-dependent transcription and cell proliferation by tributyltin and triphenyltin in human prostate cancer cells. Toxicol Appl Pharmacol 169:177–184.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Research Center for Environmental Risk, National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki, 305-8506, Japan

    Toshihiro Horiguchi

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  1. Toshihiro Horiguchi
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Editors and Affiliations

  1. International Coastal Research Center, Ocean Research Institute, The University of Tokyo, 2-106-1 Akahama, Otsuchi, Iwate, 028-1102, Japan

    Takaomi Arai (Associate Professor) (Associate Professor)

  2. Osaka City Institute of Public Health and Environmental Sciences, 8-34 Tojo-cho, Tennoji, Osaka, 543-0026, Japan

    Hiroya Harino (Senior Researcher) (Senior Researcher)

  3. Institute of Symbiotic Science and Technology, Tokyo University of Agriculture and Technology, Fuchu, Tokyo, 183-8509, Japan

    Madoka Ohji (Associate Professor) (Associate Professor)

  4. Marine Biological Association, Citadel Hill, Plymouth, PL1 2PB, UK

    William John Langston (Principal Researcher) (Principal Researcher)

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Horiguchi, T. (2009). Mechanism of Imposex Induced by Organotins in Gastropods. In: Arai, T., Harino, H., Ohji, M., Langston, W.J. (eds) Ecotoxicology of Antifouling Biocides. Springer, Tokyo. https://doi.org/10.1007/978-4-431-85709-9_7

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