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Marine Biology

, Volume 149, Issue 1, pp 65–77 | Cite as

Effects of exposure to ED contaminants (TPT-Cl and Fenarimol) on crinoid echinoderms: comparative analysis of regenerative development and correlated steroid levels

  • Alice Barbaglio
  • Daniela Mozzi
  • Michela Sugni
  • Paolo Tremolada
  • Francesco Bonasoro
  • Ramon Lavado
  • Cinta Porte
  • M. Daniela Candia Carnevali
Research Article

Abstract

Regenerative phenomena reproduce developmental processes in adult organisms and are regulated by neuro-endocrine mechanisms. They can therefore provide sensitive tests for monitoring the effects of exposure to endocrine disrupter contaminants (EDs) which can be bioaccumulated by the organisms causing dysfunctions in steroid hormone metabolism and activities and affecting reproduction and development. Echinoderms are prime candidates for this new ecotoxicological approach, since (1) they offer unique models to study physiological regenerative processes and (2) in echinoderms vertebrate-type steroids can be synthesized and used as terminal hormones along the neuro-endocrine cascades regulating reproductive, growth and developmental processes. We are currently exploring the effects on the regenerative potential of echinoderms of different classes of compounds that are well known to have ED activity. The present paper focuses on the possible effects of well-known compounds with suspected androgenic activity such as TPT-Cl (Triphenyltin-chloride) and Fenarimol [(±)-2,4-dichloro-α-(pyrimidin-5-yl) benzhydryl alcohol]. The selected test-species is the crinoid Antedon mediterranea, a tractable and sensitive benthic filter-feeding species which represents a valuable experimental model for investigation on the regenerative process from the macroscopic to the molecular level. The present investigation employs an integrated approach which combines exposure experiments and biological analysis utilizing microscopy, immunocytochemistry and biochemistry. The experiments were carried out on experimentally induced arm regenerations in semistatic controlled conditions with exposure concentrations comparable to those of moderately polluted coastal zones. The bulk of results obtained so far provide indications of significant sublethal effects from exposure to TPT-Cl and Fenarimol and mechanisms of toxicity related to developmental physiology, which are associated with variations in steroid levels in the animal tissues. The results indicate that these two substances (1) affect growth and development by interfering with the same basic cellular mechanisms of regeneration, such as cell proliferation, migration and differentiation/dedifferentiation, which are possibly controlled by steroid hormones; and (2) can induce a number of significant modifications in the timing, modalities and pattern of arm regeneration, which may involve the activation of cell mechanisms related to steroid synthesis/metabolism.

Keywords

PCBs Regenerative Stage Organotin Compound Exposed Sample Coelomic Epithelium 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The present work has received financial support from the EU (COMPRENDO Project n° EVK1-CT-2002-00129). The authors are particularly grateful to Dr Ulrike Shulte-Oehlmann for her valuable coordinating activity and to all the partners of the COMPRENDO project for their direct or indirect support and advice. Special thanks are addressed to Drs Simona Ceriani and Angelita Doria for their valuable help and technical assistance. All the experiments carried out for the research work are in accord with the current laws of our country. The authors are grateful to the anonymous reviewers for their invaluable suggestions and careful revision of the manuscript.

References

  1. Aminin DL, Agafonova IG, Federov SN (1995) Biological activity of disulfated polyhydroxysterids from the Pacific brittle star Ophiopholis aculeata. Comp Biochem Physiol 112(C):201–204Google Scholar
  2. Anderson S, Hose JE, Knezovic JP (1994) Genotoxic and developmental effects in sea urchin are sensitive indicators of effects genotoxic chemicals. Environ Toxicol Chem 13:1033–1041CrossRefGoogle Scholar
  3. Andersen HR, Vinggard AM, Rasmussen TH, Gjermandsen IM, Bonefeld-Jørgensen EC (2002) Effects of currently used pesticides in assays for estrogenicity, androgenicity and aromatase activity in vitro. Toxicol Appl Pharmacol 179:1–12CrossRefGoogle Scholar
  4. Barbaglio A, Sugni M, Mozzi D, Invernizzi A, Doria A, Pacchetti G, Tremolada P, Bonasoro F, Candia Carnevali MD (2004) Exposure effects of organotin compounds (TPT-Cl) on regenerative potential of crinoids. In: Heinzeller, Nebelsick (eds) Echinoderms. Munchen Taylor & Francis Group, London, pp 91–95Google Scholar
  5. Békri K, Pelletier E (2004) Trophic transfer and in vivo immunitoxicological effects of tributyltin (TBT) in polar seastar Leptasterias polaris. Aquat Toxicol 66:39–53CrossRefGoogle Scholar
  6. Bell G (1994) Rubigan 12 EC (EAF 457) acute toxicity to Daphnia magna. DowElanco Company reportGoogle Scholar
  7. Bryan GW, Gibbs PE, Hummerstone LG, Burt GR (1986) The decline of the gastropod Nucella lapillus around south-west England: evidence for the effect of tributyltin from antifouling paints. J Mar Biol Ass UK 66:611–640CrossRefGoogle Scholar
  8. Cadbury D (1998) The feminisation of nature. Our future at risk. Penguin Books, LondonGoogle Scholar
  9. Candia Carnevali MD (2005) Regenerative response and Endocrine Disrupters in Crinoid Echinoderms: an old experimental model, a new ecotoxicological test. In: Matranga V (ed) Echinodermata. Progress in molecular and subcellular biology. vol 39. Subseries marine molecular biotechnology. Springer, Berlin Heidelberg New York, pp 187–198Google Scholar
  10. Candia Carnevali MD, Bonasoro F (2001) Microscopic overview of crinoid regeneration. Microsc Res Tech 55:403–426CrossRefGoogle Scholar
  11. Candia Carnevali MD, Lucca E, Bonasoro F (1993) Mechanism of arm regeneration in the feather star Antedon mediterranea: healing of wound and early stages of development. J Exp Zool 267:299–317CrossRefGoogle Scholar
  12. Candia Carnevali MD, Bonasoro F, Lucca E, Thorndyke MC (1995) Pattern of cell proliferation in the feather star Antedon mediterranea. J Exp Zool 272:464–474CrossRefGoogle Scholar
  13. Candia Carnevali MD, Bonasoro F, Biale A (1997) Pattern of bromodeoxyuridine incorporation in the advanced stages of arm regeneration in the feather star Antedon mediterranea. Cell Tissue Res 289:363–374CrossRefGoogle Scholar
  14. Candia Carnevali MD, Bonasoro F, Patruno M, Thorndyke MC, Galassi S (2001a) PCB exposure and regeneration in crinoids (Echinodermata). Mar Ecol Prog Ser 215:155–167CrossRefGoogle Scholar
  15. Candia Carnevali MD, Bonasoro F, Patruno M, Thorndyke MC (2001b). Role of the nervous system in echinoderm regeneration. In: Barker M (ed), Echinoderm 2000: Proceedings of 10th international echinoderm conference, Dunedin 2000, Balkema, Rotterdam, pp 5–20Google Scholar
  16. Candia Carnevali MD, Galassi S, Bonasoro F, Patruno M, Thorndyke MC (2001c) Regenerative response and endocrine disrupters in crinoid echinoderms: arm regeneration in Antedon mediterranea after experimental exposure to polychlorinated biphenyls. J Exp Biol 204:835–842Google Scholar
  17. Candia Carnevali MD, Bonasoro F, Ferreri P, Galassi S (2003) Regenerative potential and effects of exposure to pseudo-estrogenic contaminants (4-nonylphenol) in the crinoid Antedon mediterranea. In: Feral JP (ed) Echinoderm research 2001. Balkema, Rotterdam, pp 201–207Google Scholar
  18. Caricchia AM, Chiavarini S, Cremisini C, Fantini M, Morabito R (1992) Monitoring of organotins in the La Spezia Gulf – II. Results of the 1990 sampling campaigns and concluding remarks. Sci Total Environ 121:133–144CrossRefGoogle Scholar
  19. Cima F, Ballarin L, Bressa G, Martinucci G, Burighel P (1996) Toxicity of organotin compounds on embryos of a marine invertebrate (Styela plicata; Tunicata). Ecotoxicol Environ Saf 35:174–182CrossRefGoogle Scholar
  20. Colborn T, von Saal FS, Soto AM (1993) Developmental effects of endocrine disrupting chemicals in wildlife and humans. Environ Health Perspect 101:378–384CrossRefGoogle Scholar
  21. Cooper RL, Kavlock RJ (1997) Endocrine disruptors and reproductive development: a weight-of-evidence overview. J Endocrinol 152:159–166CrossRefGoogle Scholar
  22. Coteur G, Danis B, Fowler SW, Teyssié J-L, Dubois Ph, Warnau M (2001) Effects of PCBs on reactive oxygen species (ROS) production by the immune cells of Paracentrotus lividus (Echinodermata). Mar Pollut Bull 42:667–672CrossRefGoogle Scholar
  23. D’Andrea AF, Stancyk S, Chandler GT (1996) Sublethal effects of cadmium on arm regeneration in the burrowing brittlerstars, Microphiopholis gracillima (Stimpson) (Echinodermata: Ophiuroidea). Ecotoxicology 5:115–133CrossRefGoogle Scholar
  24. Degen GH, Botl HM (2000) Endocrine disruptors: update on xenoestrogens. Int Arch Occup Environ Health 73:433–441CrossRefGoogle Scholar
  25. den Besten PJ (1998) Cytochrome P450 monooxygenase system in echinoderms. Comp Biochem Physiol 121(C):139–146Google Scholar
  26. den Besten PJ, Herwig HJ, Zandee DI, Voogt PA (1989) Effects of cadmium and PCBs on reproduction of the sea star Asterias rubens: aberrations in the early development. Ecotoxicol Environ Saf 18:173–180CrossRefGoogle Scholar
  27. den Besten PJ, Herwig HJ, Smaal AC, Zandee DI, Voogt PA (1990) Interference of polychlorinated biphenyls (Clophen A50) with gametogenesis in the sea star Asterias rubens L. Aquat Toxicol 18:231–246CrossRefGoogle Scholar
  28. den Besten PJ, Elenbaas JM, Maas EJR, Dielman SJ, Herwig HJ, Voogt PA (1991a) Effects of cadmium and polychlorinated biphenyls (Clophen A50) on steroid metabolism and cytochrome P-450 monooxygenase system in the sea star Asterias rubens L. Aquat Toxicol 20:95–110CrossRefGoogle Scholar
  29. den Besten PJ, Mass JR, Livingstone DR, Zandee DI, Voogt PA (1991b) Interference of benzo[α]pyrene with cytochrome P450 mediated steroid metabolism in pyloric caeca microsomes of the sea star Asterias rubens L. Comp Biochem Physiol 100(C):165–168Google Scholar
  30. Depledge MH, Billinghurst Z (1999) Ecological significance of endocrine disruption in marine invertebrates. Mar Pollut Bull 39:32–38CrossRefGoogle Scholar
  31. Dieleman SJ, Schoenmakers HNJ (1979) Radioimmunoassay to determine the presence of progesterone and estrone in starfish Asterias rubens. Gen Comp Endocrinol 39:534–542CrossRefGoogle Scholar
  32. EEC (1967) Council Directive 67/548/EEC on the approximation of laws, regulations and administrative provisions relating to the classification, packaging and labelling of dangerous substances. Official Journal of the European Communities, Luxemborg, 196, p.1Google Scholar
  33. Fairley P, Roberts M, Stringer J (1996). Endocrine disruptor. Chem Week May 8:29–36Google Scholar
  34. Fait A, Ferioli A, Barbieri F (1994) Organotin compounds. Toxicology 91:77–82CrossRefGoogle Scholar
  35. Federoff NE, Young D, Cowles J, Spatz D, Shamin M (1999) TPTH. Environmental fate and ecological risk assessment. United States Environmental Protection Agency, Washington DCGoogle Scholar
  36. Fitox (1999) Database on physical, chemical and ecotoxicological properties of pesticides. In: Finizio A (ed) Environmental impact of pesticides: risk evaluation for non-target organism. Ampa n 1 RomaGoogle Scholar
  37. Gibbs PE, Pascoe PL, Burt GR (1988) Sex changes in the female dog-whelk, Nucella lapillus, induced by tributyltin from antifouling paints. J Mar Biol Ass UK 68:715–731CrossRefGoogle Scholar
  38. Gray LE Jr, Monosson E, Kelce WR (1996) Emerging issues: the effects of endocrine disrupters on reproductive development. In: Di Giulio RT, Monosson E (eds) Interconnection between human and ecosystem health. Chapman & Hall, London, pp 47–81Google Scholar
  39. Heinzeller T, Welsch U (1994) Crinoidea. In: Harrison F (ed) Microscopic anatomy of invertebrates: Echinodermata, vol 14. Wiley-Liss, New York, pp 9–148Google Scholar
  40. Hines GA, Watts SA, McClintock JB (1994) Biosynthesis of estrogen derivatives in the echinoid Lytechinus variegates Lamark. In: David, Guille, Féral, Roux (eds) Echinoderms through time. Balkema, Rotterdam, pp 711–716Google Scholar
  41. Hoffman DG, Grothe DW, Francis PC (1987) Chronic toxicity of fenarimol to Daphnia magna in a static renewal life cycle test. DowElanco Company reportGoogle Scholar
  42. Horiguchi T, Shiraishi H, Shimizu M, Morita M (1995) Imposex in Japanese gastropods (Neogastropoda and Mesogastropoda): effects of tributyltin and triphenyltin from antifouling paints. Mar Pollut Bull 31:402–405CrossRefGoogle Scholar
  43. IPCS (2004) (International programme on chemical safety), by World Health Organization, United Nations Environmental Programme, International Labour Organization, http://www.inchem.org
  44. Jackson R, Lewis C (1994) The degradation and retention of 14C Fenarimol in water-sediment systems. DowElanco Company reportGoogle Scholar
  45. Janer G, LeBlanc GA, Porte C (2004) A comparative study on the metabolism of androgens in invertebrates and its modulation by xenoandrogens. In: Proceedings of CREDO cluster workshop on ecological relevance of chemically induced endocrine disruption in wildlife, p 23Google Scholar
  46. Kline RM, Knox JW (1981) Fenarimol: Interactions with sewage microorganism. DowElanco Company reportGoogle Scholar
  47. Kabayashi N (1984) Marine ecotoxicological testing with Echinoderms. In: Persoone G, Jaspers F, Claus C (eds) Ecotoxicological testing for the marine environment. Vol.I, State University of Ghent and Institute of Marine Scientific Research, Bredene, Belgium, pp 341–405Google Scholar
  48. LeBlanc GA, Campbell PM, den Besten P, Brown RP, Chang ES, Coats JR, De Fur PL, Dhadialla T, Edwards J, Riddiford Lm, Simpson MG, Snell TW, Thorndyke MC, Matsumura F (1999) The endocrinology of invertebrates. In: deFur P, Crane M, Ingersoll C, Tattersfield L (eds) Endocrine dirsruption in invertebrates: endocrinology, testing and assessment. Workshop on endocrine disruption in invertebrates: endocrinology, testing and assessment: 1998 Dec 12–15. SETAC Noordwijkerhout, The Netherlands, pp 23–106Google Scholar
  49. Lorenzo J (2003) A new hypothesis for how sex steroid hormones regulate bone mass. J Clin Invest 111:1641–1643CrossRefGoogle Scholar
  50. Lutz I, Sugni M, Candia Carnevali MD, Lavado R, Porte C, Schulte-Oehlmann U, Kloas W (2004) First evidence for specific [3H]-testosterone and [3H]-estradiol binding sites in echinoderms. In: Proceedings of CREDO cluster workshop on ecological relevance of chemically induced endocrine disruption in wildlife, p 43Google Scholar
  51. Mackay D, Shiu WY, Ma KC (1997) Illustrated handbook of physical-chemical properties and environmental fate for organic chemicals. vol 5, Lewis Publishers, New York, p 812Google Scholar
  52. Marsh A, Walker C (1995) Effect of estradiol and progesterone on c-myc expression in the sea star testis and the seasonal regulation of spermatogenesis. Mol Reprod Dev 40:62–68CrossRefGoogle Scholar
  53. Matthiessen P, Gibbs PE (1998) Critical appraisal of the evidence for tributyltin-mediated endocrine disruption in mollusks. Environ Toxicol Chem 17(1):37–43CrossRefGoogle Scholar
  54. Moschino V, Marin M (2002) Spermiotoxicity and embriotoxicity of triphenyltin in the sea urchin Paracentrotus lividus Lmk. Appl Organomet Chem 16:175–181CrossRefGoogle Scholar
  55. Mu XY, LeBlanc GA (2002) Environmental antiecdysteroids alter embryo development in the crustacean Daphnia magna. J Exp Zool 292(3):287–292CrossRefGoogle Scholar
  56. Novelli AA, Argese E, Tagliapietra D, Bettiol C, Volpi Ghirardini A (2002) Toxicity of tributyltin and triphenyltin to early life-stages of Paracentrotus lividus (Echinodermata: Echinoidea). Environ Toxicol Chem 21:859–864CrossRefGoogle Scholar
  57. Powers MF, Beavis AD (1991) Triorganotins inhibit the mitochondrial inner membrane anion channel. J Biol Chem 266(26):17250–17256PubMedGoogle Scholar
  58. Rippen G (ed) (1990) Handbuch Umweltechemikalien. Stoffdaten, Pfüfverfahren, Vorschirften. 3. Auflage, 5. Ergänzungslieferung 2/90. Ecomed, Landsberg am LechGoogle Scholar
  59. Schoenmakers HJN (1979) In vitro biosynthesis of steroids from cholesterol by the ovaries and pyloric caeca of the starfish Asterias rubens. Comp Biochem Physiol (B) 63:179–184Google Scholar
  60. Schoenmakers HJN (1980) The variation of 3ß-hydroxysteroid dehydrogenase activity of the ovaries and pyloric caeca of the starfish Asterias rubens during the annual reproductive cycle. J Comp Physiol 138:27–30CrossRefGoogle Scholar
  61. Schoenmakers HJN, Voogt PA (1980) In vitro biosynthesis of steroids from progesterone by the ovaries and pyloric caeca of the starfish Asterias rubens. Gen Comp Endocrinol 41:408–416CrossRefGoogle Scholar
  62. Shirai H, Walker CW (1988) Chemical control of asexual and sexual reproduction in echinoderms. Alan R Liss Inc, New YorkGoogle Scholar
  63. Shubina LK, Fedorov SN, Levina EV, Andriyaschenko PV, Kalinovsky AI, Stonik VA, Smirnov IS (1998) Comparative study on polyhydroxylated steroids from echinoderms. Comp Biochem Physiol 119(B):505–511CrossRefGoogle Scholar
  64. Smith AB (1990) Biomineralization in Echinoderms. In: Carler JG (ed) Skeletal biomineralization: patterns, processes and evolutionary trends. vol I, pp 413–435CrossRefGoogle Scholar
  65. Smith DF, Meyer DL, Horner SMJ (1981) Amino acid uptake by the comatulid crinoid Cenometra bella (Echinodermata) following evisceration. Mar Biol 61:207–213CrossRefGoogle Scholar
  66. Soto AM, Sonnenschein C, Chung KL (1995) The E-Screen as a tool to identify estrogens: an update on estrogenic environmental pollutants. Environ Health Perspect 103(Suppl):113–122PubMedPubMedCentralGoogle Scholar
  67. Thorndyke MC, Candia Carnevali MD (2001) Regeneration and neurohormones and growth factors in echinoderms. Can J Zool 79:1171–1208CrossRefGoogle Scholar
  68. Tolosa I, Readman JW, Blaevoet A, Ghilini S, Bartocci J, Horvat M (1996) Contamination of Mediterranean (Côte d’Azur) coastal waters by organotins and Irgarol 1051 used in antifouling paints. Mar Pollut Bull 32:335–341CrossRefGoogle Scholar
  69. Tremolada P, Bristeau S, Mozzi D, Sugni M, Barbaglio A, Dagnac T, Candia Carnevali MD (2005) A simple model to predict compound loss processes in aquatic ecotoxicological tests: calculated and measured TPT-Cl levels in water and biota. Int J Env Anal Chem 86:171–184CrossRefGoogle Scholar
  70. Voogt PA, Oudejans RCHM, Broertjes JJS (1984) Steroids and reproduction in starfish. In: Engels W, Clark WH, Fischer A, Olive PJM, Went DF (eds) Advances in invertebrate reproduction. Elsevier North-Holland Inc, New York, pp 151–161Google Scholar
  71. Voogt PA, den Besten PJ, Jansen M (1990) The Δ5 –pathway in steroid metabolism in the sea star Asterias rubens L. Comp Biochem Physiol 97(B):555–562Google Scholar
  72. Voogt PA, den Besten PJ, Jansen M (1991) Steroid metabolism in relation to the reproductive cycle in Asterias rubens L. Comp Biochem Physiol 99(B):77–82Google Scholar
  73. Walsh GE, McLaughlin LL, Louie MK, Deans CH, Lores EM (1986) Inhibition of arm regeneration by Ophioderma brevispina (Echinodermata, Ophiuroidea) by tributyltin oxide and triphenyltin oxide. Ecotoxicol Environ Saf 12:95–100CrossRefGoogle Scholar
  74. Yallapragada PR, Vig PJS, Desaiah D (1990) Differential effects of triorganotins on calmodulin activity. J Toxicol Environ Health 29:317–327CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Alice Barbaglio
    • 1
  • Daniela Mozzi
    • 1
  • Michela Sugni
    • 1
  • Paolo Tremolada
    • 1
  • Francesco Bonasoro
    • 1
  • Ramon Lavado
    • 2
  • Cinta Porte
    • 2
  • M. Daniela Candia Carnevali
    • 1
  1. 1.Dipartimento di BiologiaUniversità degli Studi di MilanoMilanoItaly
  2. 2.Environmental Chemistry DepartmentIIQAB-CSICBarcelonaSpain

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