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Mode of Action of Organotins to Induce the Development of Imposex in Gastropods, Focusing on Steroid and the Retinoid X Receptor Activation Hypotheses

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Biological Effects by Organotins

Abstract

Basic knowledge of endocrinology or reproductive physiology of prosobranch gastropods is reviewed, focusing on vertebrate-type steroids as possible sex hormones in gastropods. Major points of the view for criticism are steroid-producing cells, enzymes to synthesize and/or metabolize steroids, and functional receptors for steroids. Mechanism of induction and promotion of the development of imposex is also reviewed, regarding six hypotheses proposed as the mechanism by which organotins, such as TBT and TPhT, induce the development of imposex in gastropods: (1) an increase in androgen (e.g., testosterone) levels as a result of TBT-mediated inhibition of aromatase; (2) an increase in testosterone levels owing to the inhibition of acyl CoA-steroid acyltransferase; (3) TBT-mediated inhibition of the excretion of androgen sulfate conjugates, with a consequent increase in androgen levels; (4) TBT interference with the release of penis morphogenetic/retrogressive factor from the pedal/cerebropleural ganglia; (5) an increase in the level of an alanine-proline-glycine-tryptophan amide (APGWamide) neuropeptide in response to TBT; and (6) activation of the retinoid X receptor (RXR). The latest information about nuclear receptors other than RXR in gastropods, namely, retinoic acid receptor (RAR) and peroxisome proliferator-activated receptor (PPAR), is also described.

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Abbreviations

PPAR:

peroxisome proliferator-activated receptor

RAR:

retinoic acid receptor

RXR:

retinoid X receptor

TBT:

tributyltin

TPhT:

triphenyltin

References

  • Albalat R (2009) The retinoic acid machinery in invertebrates: ancestral elements and vertebrate innovations. Mol Cell Endocrinol 313:23–35

    Article  CAS  Google Scholar 

  • Albalat R, Cañestro C (2009) Identification of Aldh1a, Cyp26 and RAR orthologs in protostomes pushes back the retinoic acid genetic machinery in evolutionary time to the bilaterian ancestor. Chem Biol Interact 178:188–196

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Bouton D, Escriva H, de Mendonça R et al (2005) A conserved retinoid X receptor (RXR) from the mollusk Biomphalaria glabrata transactivates transcription in the presence of retinoids. J Mol Endocrinol 34:567–582

    Article  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

    Article  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

    Article  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 

  • Chambon P (1996) A decade of molecular biology of retinoic acid receptors. FASEB J 10:940–954

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • De Luca LM (1991) Retinoids and their receptors in differentiation, embryogenesis, and neoplasia. FASEB J 5:2924–2933

    Google Scholar 

  • de Urquiza AM, Liu S, Sjöberg M et al (2000) Docosahexaenoic acid, a ligand for the retinoid X receptor in mouse brain. Science 290:2140–2144

    Article  Google Scholar 

  • Dmetrichuk JM, Carlone RL, Jones TR et al (2008) Detection of endogenous retinoids in the molluscan CNS and characterization of the trophic and tropic actions of 9-cis retinoic acid on isolated neurons. J Neurosci 28:13014–13024

    Article  CAS  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 U S A 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 U S A 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 Publishing, Amsterdam, pp 173–175

    Google Scholar 

  • Galante-Oliveira S, Oliveira I, Pacheco M et al (2010) Hydrobia ulvae imposex levels at Ria de Aveiro (NW Portugal) between 1998 and 2007: a counter-current bioindicator? J Environ Monit 12:500–507

    Article  CAS  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

    Article  CAS  Google Scholar 

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

    Article  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

    Article  Google Scholar 

  • Gibbs PE, Bryan GW, Pascoe PL et al (1990) Reproductive abnormalities in female Ocenebra erinacea (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

    Article  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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Grün F, Blumberg B (2006) Environmental obesogens: organotins and endocrine disruption via nuclear receptor signaling. Endocrinology 147:S50–S55

    Article  Google Scholar 

  • Grün F, Watanabe H, Zamanian Z et al (2006) Endocrine-disrupting organotin compounds are potent inducers of adipogenesis in vertebrates. Mol Endocrinol 20:2141–2155

    Article  Google Scholar 

  • Heyman RA, Mangelsdorf DJ, Dyck JA et al (1992) 9-cis retinoic acid is a high affinity ligand for the retinoid X receptor. Cell 68:397–406

    Article  CAS  Google Scholar 

  • Hopkins PM, Durica D, Washington T (2008) RXR isoforms and endogenous retinoids in the fiddler crab, Uca pugilator. Comp Biochem Physiol A Mol Integr Physiol 151:602–614

    Article  Google Scholar 

  • Horiguchi T (2000) Molluscs. In: Kawai S, Koyama J (eds) Problems of endocrine disruptors in fisheries environment. Koseisha-Koseikaku, Tokyo, pp 54–72 [in Japanese]

    Google Scholar 

  • Horiguchi T (2006) Masculinization of females caused by organotin compounds in gastropod mollusks, focusing on the mode of action of tributyltin and triphenyltin on the development of imposex. Environ Sci 13(2):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. Koseisha-Koseikaku, Tokyo, pp 99–135. [in Japanese]

    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

    Article  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 (1997) 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, 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, 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 Perspect 114(Supplement 1):13–19

    Google Scholar 

  • Horiguchi T, Nishikawa T, Ohta Y et al (2007) 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 (2008a) Exposure to 9-cis retinoic acid induces penis and vas deferens development in the female rock shell, Thais clavigera. Cell Biol Toxicol 24:553–562

    Google Scholar 

  • Horiguchi T, Nishikawa T, Ohta Y et al (2008b) Monthly changes of RXR gene expression and sexual characteristics in male rock shells (Thais clavigera) in Hiraiso, Japan. SETAC Europe 18th annual meeting, Warsaw SETAC Europe Office, Brussels, p 150

    Google Scholar 

  • Horiguchi T, Nishikawa T, Ohta Y et al (2010a) 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 396:597–607

    Article  CAS  Google Scholar 

  • Horiguchi T, Urushitani H, Ohta Y et al (2010b) Establishment of a polyclonal antibody against the retinoid X receptor of the rock shell Thais clavigera and its application to rock shell tissues for imposex research. Ecotoxicology 19:571–576

    Article  CAS  Google Scholar 

  • Horiguchi T, Lee JH, Park JC et al (2012) Specific accumulation of organotin compounds in tissues of the rock shell, Thais clavigera. Mar Environ Res 76:56–62

    Article  CAS  Google Scholar 

  • Horton C, Maden M (1995) Endogenous distribution of retinoids during normal development and teratogenesis in the mouse embryo. Dev Dyn 202:312–323

    Article  CAS  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 

  • 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 148:315–326

    Article  CAS  Google Scholar 

  • Kanayama T, Kobayashi N, Mamiya S et al (2005) Organotin compounds promote adipocyte differentiation as agonists of the peroxisome proliferators-activated receptor γ/retinoid X receptor pathway. Mol Pharmacol 67:766–774

    Article  CAS  Google Scholar 

  • Kastner P, Chan S (2001) Function of RARalpha during the maturation of neutrophils. Oncogene 20:7178–7185

    Article  CAS  Google Scholar 

  • Kastner P, Mark M, Chambon P (1995) Nonsteroid nuclear receptors: what are genetic studies telling us about their role in real life? Cell 83:859–869

    Article  CAS  Google Scholar 

  • Kaur S, Jobling S, Jones CS et al (2015) The nuclear receptors of Biomphalaria glabrata and Lottia gigantea: implications for developing new model organisms. PLoS One 10(4):e0121259. Published online 2015 Apr 7. doi:10.1371/journal.pone.0121259, doi:10.1371%2Fjournal.pone.0121259#pmc_ext

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

    Article  Google Scholar 

  • le Maire A, Grimaldi M, Roecklin D et al (2009) Activation of RXR-PPAR heterodimers by organotin environmental endocrine disruptors. EMBO Rep 10:367–373

    Article  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, pp 23–106

    Google Scholar 

  • Levin AA, Sturzenbecker LJ, Kazmer S et al (1992) 9-cis retinoic acid stereoisomer binds and activates the nuclear receptor RXR alpha. Nature 355:359–361

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Mangelsdorf DJ, Evans RM (1995) The RXR heterodimers and orphan receptors. Cell 83:841–850

    Article  CAS  Google Scholar 

  • Mangelsdorf DJ, Borgmeyer U, Heyman RA et al (1992) Characterization of three RXR genes that mediate the action of 9-cis retinoic acid. Genes Dev 6:329–344

    Article  CAS  Google Scholar 

  • Mark M, Ghyselinck NB, Chambon P (2009) Function of retinoic acid receptors during embryonic development. Nucl Recept Signal 7:e002

    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 

  • Nordberg H, Cantor M, Dusheyko S et al (2014) The genome portal of the Department of Energy Joint Genome Institute: 2014 updates. Nucleic Acids Res 42(1):D26–31

    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, Ilyanassa obsoleta: TBT as a neurotoxin and aromatase inhibitor. Mar Environ Res 54:715–718

    Article  Google Scholar 

  • Oberdörster E, Romano J, McClellan-Green P (2005) The neuropeptide APGWamide as a penis morphogenic factor (PMF) in gastropod mollusks. Integr Comp Biol 45:28–32

    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 

  • Oehlmann J, Di Benedetto P, Tillmann M et al (2007) Endocrine disruption in prosobranch molluscs: evidence and ecological relevance. Ecotoxicology 16:29–43

    Article  CAS  Google Scholar 

  • Pascoal S, Carvalho G, Vasieva O et al (2013) Transcriptomics and in vivo tests reveal novel mechanisms underlying endocrine disruption in an ecological sentinel, Nucella lapillus. Mol Ecol 22:1589–1608

    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 

  • 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 77:1450–1468

    Article  CAS  Google Scholar 

  • Scott AP (2013) Do mollusks use vertebrate sex steroids as reproductive hormones? II. Critical review of the evidence that steroids have biological effects. Steroids 78:268–281

    Article  CAS  Google Scholar 

  • Simakov O, Marletaz F, Cho SJ et al (2013) Insights into bilaterian evolution from three spiralian genomes. Nature 493:526–531

    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 

  • Sternberg RM, LeBlanc GA (2006) Kinetic characterization of the inhibition of acyl coenzyme A: steroid acyltransferases by tributyltin in the eastern mud snail (Ilyanassa obsoleta). Aquat Toxicol 78:233–242

    Article  CAS  Google Scholar 

  • Sternberg RM, Hotchkiss AK, Leblanc GA (2008) Synchronized expression of retinoid X receptor mRNA with reproductive tract recrudescence in an imposex-susceptible mollusc. Environ Sci Technol 42:1345–1351

    Article  CAS  Google Scholar 

  • Sternberg RM, Gooding MP, Hotchkiss AK et al (2010) Environmental-endocrine control of reproductive maturation in gastropods: implications for the mechanism of tributyltin-induced imposex in prosobranchs. Ecotoxicology 19:4–23

    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 Publishing, Amsterdam, pp 106–111

    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 

  • Ulven SM, Gundersen TE, Sakhi AK et al (2001) Quantitative axial profiles of retinoic acid in the embryonic mouse spinal cord: 9-cis retinoic acid only detected after all-trans-retinoic acid levels are super-elevated experimentally. Dev Dyn 222:341–353

    Article  CAS  Google Scholar 

  • Urquiza AM, Liu S, Sjoberg M et al (2000) Docosahexaenoic acid, a ligand for the retinoid X receptor in mouse brain. Science 290:2140–2144

    Article  Google Scholar 

  • Urushitani H, Katsu Y, Ohta Y et al (2011) Cloning and characterization of retinoid X receptor (RXR) isoforms in the rock shell, Thais clavigera. Aquat Toxicol 103:101–111

    Article  CAS  Google Scholar 

  • Urushitani H, Katsu Y, Ohta Y et al (2013) Cloning and characterization of the retinoic acid receptor-like protein in the rock shell, Thais clavigera. Aquat Toxicol 142–143:403–413

    Article  Google Scholar 

  • Vogeler S, Galloway TS, Lyons BP et al (2014) The nuclear receptor gene family in the Pacific oyster, Crassostrea gigas, contains a novel subfamily group BMC Genomics 15:369. doi:10.1186/1471-2164-15-369. The electronic version of this article is the complete one and can be found online at:http://www.biomedcentral.com/1471-2164/15/369

  • Wang YH, LeBlanc GA (2009) Interactions of methyl farnesoate and related compounds with a crustacean retinoid X receptor. Mol Cell Endocrinol 309:109–116

    Article  CAS  Google Scholar 

  • Werner EA, DeLuca HF (2001) Metabolism of a physiological amount of all-trans-retinol in the vitamin A-deficient rat. Arch Biochem Biophys 393:262–270

    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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  1. Ecosystem Impact Research Section, Center for Health and Environmental Risk Research, National Institute for Environmental Studies, 16-2, Onogawa, Tsukuba, 305-8506, Japan

    Toshihiro Horiguchi Ph.D.

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  1. Center for Health and Environmental Risk Research, National Institute for Environmental Studies, Tsukuba, Japan

    Toshihiro Horiguchi

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Horiguchi, T. (2017). Mode of Action of Organotins to Induce the Development of Imposex in Gastropods, Focusing on Steroid and the Retinoid X Receptor Activation Hypotheses. In: Horiguchi, T. (eds) Biological Effects by Organotins. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56451-5_9

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