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Effect of the Organochlorine Pesticide Endosulfan on GnRH and Gonadotrope Cell Populations in Fish Larvae

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Abstract

Endocrine-disrupting chemicals can influence the hypothalamus–pituitary–gonad axis and possibly affect reproduction in vertebrates. We analyzed the effect of 30-day endosulfan (ES) exposure in sexually undifferentiated larvae of the cichlid fish Cichlasoma dimerus. The number, area, mean cytoplasmic and nuclear diameter, and mean cytoplasmic optical density of gonadotropin-releasing hormone (GnRH) I, II, and III immunoreactive (ir-) neurons and β follicle-stimulating hormone (βFSH) ir-cells were measured. Animals exposed to the highest ES concentration (0.1 μg/l) showed a decrease in GnRH I nucleus/cytoplasm area ratio upon exposure. Nuclear area and mean nuclear diameter of βFSH ir-cells was higher in ES treated fish. βFSH nucleus/cytoplasm area ratio was high in exposed animals, and animals exposed to 0.1 μg/l ES showed smaller mean cytoplasmic optical density. These findings suggest that ES affects GnRH I and βFSH protein synthesis/release. However, these responses seem to be insufficient to affect gonadal differentiation at this stage of development.

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References

  • Balasubramani A, Pandian TJ (2008) Endosulfan suppresses growth and reproduction in zebrafish. Curr Sci 94(7):883–890

    CAS  Google Scholar 

  • Baudino OM, Suero EA, Augusto M, Gimenez ME, Flores N (2003) Monitoring organochlorine pesticides in surface and ground water in San Juan Argentina. J Chile Chem Soc 48:7–12

    Google Scholar 

  • Bloomquist JR (2003) Chloride channels as tools for developing selective insecticides. Arch Insect Biochem Physiol 54:145–156

    Article  CAS  Google Scholar 

  • Canadian Council on Animal Care (2005) Guidelines on the care and the use of fish in research, teaching and testing. Ottawa, ON, Canada, pp 87

  • Cerdá-Reverter JM, Zanuy S, Muñoz-Cueto JA (2001a) Cytoarchitectonic study of the brain of a perciform species, the sea bass (Dicentrarchus labrax). I. The telencephalon. J Morphol 247:217–228

    Article  Google Scholar 

  • Cerdá-Reverter JM, Zanuy S, Muñoz-Cueto JA (2001b) Cytoarchitectonic study of the brain of a perciform species, the sea bass (Dicentrarchus labrax). II. The diencephalon. J Morphol 247:229–251

    Article  Google Scholar 

  • Cooper RL, Stoker TE, Tyrey L, Goldman JM, McElroy WK (2000) Atrazine disrupts the hypothalamic control of pituitary-ovarian function. Toxicol Sci 53:297–307

    Article  CAS  Google Scholar 

  • Donohoe RM, Curtis LR (1996) Estrogenic activity of chlordecone, o, p′-DDT and o, p′-DDE in juvenile rainbow trout: Induction of vitellogenesis and interaction with hepatic estrogen binding sites. Aquat Toxicol 36:31–52

    Article  CAS  Google Scholar 

  • Fernald RD, Shelton LC (1985) The organization of the diencephalon and the pretectum in the cichlid fish, Haplochromis burtoni. J Comp Neurol 238:202–217

    Article  CAS  Google Scholar 

  • Giusi G, Facciolo RM, Alò R, Carelli A, Madeo M, Brandmayr P et al (2005) Some environmental contaminants influence motor and feeding behaviors in the ornate wrasse (Thalassoma pavo) via distinct cerebral histamine receptor subtypes. Environ Health Perspect 113:1522–1529

    Article  Google Scholar 

  • Gonzalez-Martinez D, Zmora N, Mañanos E, Saligaut D, Zanuy S, Zohar Y et al (2002) Immunohistochemical localization of three different prepro-GnRHs (gonadotropin-releasing hormones) in the brain and pituitary of the European sea bass (Dicentrarchus labrax) using antibodies to the corresponding GnRH-associated peptides. J Comp Neurol 446:95–113

    Article  CAS  Google Scholar 

  • Gopal K, Khanna RN, Anand M, Gupta GSD (1981) The acute toxicity of endosulfan to freshwater organisms. Toxicol Lett 7:453–456

    Article  CAS  Google Scholar 

  • Gore AC (2000) Organochlorine pesticides directly regulate gonadotropin-releasing hormone gene expression and biosynthesis in the GT1–7 hypothalamic cell line. Mol Cell Endocrinol 192:157–170

    Article  Google Scholar 

  • Gore AC (2008a) Neuroendocrine systems as targets for environmental endocrine-disrupting chemicals. Fertil Steril 89(2):1–2

    Article  Google Scholar 

  • Gore AC (2008b) Developmental programming and endocrine disruptor effects on reproductive neuroendocrine systems. Front Neuroendocrinol 29:358–374

    Article  CAS  Google Scholar 

  • Gormley KL, Teather KL (2003) Developmental, behavioral, and reproductive effects experienced by Japanese medaka (Oryzias latipes) in response to short-term exposure to endosulfan. Ecotoxicol Environ Saf 54(3):30–38

    Article  Google Scholar 

  • Guillette LJ, Crain AD, Rooney AA, Pickford DB (1995) Organization versus activation: the role of endocrine-disrupting contaminants (EDCs) during embryonic development in wildlife. Environ Health Perspect 103(7):157–164

    Article  CAS  Google Scholar 

  • Hallare A, Nagel K, Köhler HR, Triebskorn R (2006) Comparative embryotoxicity and proteotoxicity of three carrier solvents to zebrafish (Danio rerio) embryos. Ecotoxicol Environ Saf 63:387–388

    Article  Google Scholar 

  • Harding WC (1979) Pesticide profiles, part one: Insecticides and miticides. Coop Ext Serv Bull 267. University of Maryland, College Park

    Google Scholar 

  • Harris CA, Santos EM, Janbakhsh A, Pottinger TG, Tyler CR, Sumpter JP (2001) Nonylphenol affects gonadotropin levels in the pituitary gland and plasma of female rainbow trout. Environ Sci Technol 35(14):2909–2916

    Article  CAS  Google Scholar 

  • Hutchinson TH, Shillabeer N, Winter MJ, Pickford DB (2006) Acute and chronic effects of carrier solvents in aquatic organisms: a critical review. Aquat Toxicol 76:69–92

    Article  CAS  Google Scholar 

  • Kah O, Lethimonier C, Somoza G, Guilgur LG, Vaillant C, Lareyre JJ (2007) GnRH and GnRH receptors in metazoan: a historical, comparative, and evolutive perspective. Gen Comp Endocrinol 153:346–364

    Article  CAS  Google Scholar 

  • Kime DE (1999) A strategy for assessing the effects of xenobiotics on fish reproduction. Sci Total Environ 225:3–11

    Article  CAS  Google Scholar 

  • Kullander SO (1983) A revision of the South American cichlid genus Cichlasoma (Teleostei: Cichlidae). Swedish Museum of Natural History, Stockholm

    Google Scholar 

  • López HL, Miquelarena AM, Menni RC (2003) Lista comentada de los peces continentales de la Argentina. Serie técnica y didáctica No 5. Facultad de Ciencias Naturales y Museo-UNLP, Buenos Aires

    Google Scholar 

  • Mac MJ, Seelye JG (1981) Potential influence of acetone in aquatic bioassays testing the dynamics and effects of PCBs. Bull Environ Contam Toxicol 27(3):359–367

    Article  CAS  Google Scholar 

  • Meijide FJ, Lo Nostro FL, Guerrero GA (2005) Gonadal development and sex differentiation in the cichlid fish Cichlasoma dimerus (Teleostei, Perciformes): a light- and electron-microscopic study. J Morphol 264:191–210

    Article  Google Scholar 

  • Mortensen AS, Arukwe A (2006) Dimethyl sulfoxide is a potent modulator of estrogen receptor isoforms and xenoestrogen biomarker responses in primary culture of salmon hepatocytes. Aquat Toxicol 79:99–103

    Article  CAS  Google Scholar 

  • Nakamura M (2000) Gonadal sex differentiation in fish and the effects of environment endocrine disrupters. International Symposium on Environmental Endocrine Disrupters, pp 108–109

  • Palmer BD, Palmer SK (1995) Vitellogenin induction by xenobiotic estrogens in the red-eared turtle and African frog. Environ Health Perspect 103:19–25

    CAS  Google Scholar 

  • Pandolfi M, Parhar IS, Ravaglia MA, Meijide FJ, Maggese MC, Paz DA (2002) Ontogeny and distribution of gonadotropin-releasing hormone (GnRH) neuronal systems in the brain of the cichlid fish Cichlasoma dimerus. Anat Embryol 205:271–281

    Article  CAS  Google Scholar 

  • Pandolfi M, Muñoz Cueto JA, Lo Nostro FL, Downs JL, Paz DA, Maggese MC et al (2005) GnRH systems of Cichlasoma dimerus (Perciformes, Cichlidae) revisited: a localization study with antibodies and riboprobes to GnRH-associated peptides. Cell Tissue Res 321:219–232

    Article  CAS  Google Scholar 

  • Pandolfi M, Lo Nostro FL, Shimizu A, Pozzi AG, Meijide FJ, Rey Vázquez G et al (2006) Identification of immunoreactive FSH and LH cells in the cichlid fish Cichlasoma dimerus during the ontogeny and sexual differentiation. Anat Embryol 211:355–365

    Article  Google Scholar 

  • Pandolfi M, Cánepa MM, Meijide FJ, Alonso F, Rey Vázquez G, Maggese MC et al (2009) Studies on the reproductive and developmental biology of Cichlasoma dimerus (Percifomes, Cichlidae). Biocell 33(1):1–18

    CAS  Google Scholar 

  • Panzica GC, Viglietti-Panzica C, Ottinger MA (2005) Introduction: neurobiological impact of environmental estrogens. Brain Res Bull 65:187–191

    Article  CAS  Google Scholar 

  • Parhar IS, Tosaki H, Sakuma Y, Kobayashi M (2001) Sex differences in the brain of goldfish: gonadotropin-releasing hormone and vasotocinergic neurons. Neurosciences 104:1099–1110

    Article  CAS  Google Scholar 

  • Peter RE, Trudeau VL, Sloley BD (1991) Brain regulation of reproduction in teleosts. Bull Inst Zool Acad Sin 16:89–118

    Google Scholar 

  • Pillai A, Priya L, Gupta S (2003) Effects of combined exposure to lead and cadmium on the hypothalamic-pituitary axis function in proestrous rats. Food Chem Toxicol 41:379–384

    Article  CAS  Google Scholar 

  • Polkowska J, Przekop F (1993) Effect of protein deficiency on luteinizing hormone releasing hormone (LHRH), gonadotropoin releasing hormone associated peptide (GAP) and luteinizing hormone (LH) immunocytochemistry in the hypothalamus and pituitary gland of prepubertal ewes. Exp Clin Endocrinol 101:230–237

    Article  CAS  Google Scholar 

  • RAP-AL (2008) El Endosulfan y sus alternativas en America Latina, pp 148

  • Ronchi E, Aoki C, Krey LC, Pfaff DW (1992) Immunocytochemical study of GnRH and GnRH-associated peptide in male Syriam hamsters as a function of photoperiod and gonadal alterations. Neuroendocrinology 55:134–145

    Article  CAS  Google Scholar 

  • Salvo LM, Sinhorini IL, Malucelli BE, Klemz C, Sanchez DCO, Nicaretta L et al (2008) Effects of endosulfan sublethal concentrations on carp (Cyprinus carpio, Linnaeus, 1758): Morphometric, hystologic, ultrastructural analyses and cholinesterase activity evaluation. Braz J Vet Res Anim Sci 45(2):87–94

    Google Scholar 

  • Scholz NL, Truelove NK, French BL, Berejikian BA, Quinn TP, Casillas E (2000) Diazinon disrupt antipredator and homing behaviors in Chinook salmon (Oncorhynchus tshawytscha). Can J Fish Aquat Sci 57:1911–1918

    Article  CAS  Google Scholar 

  • Senthilkumaran B, Okuzawa K, Gen K, Ookura T, Kagawa H (1999) Distribution and seasonal variation in levels of three native GnRHs in the brain and pituitary of perciform fish. J Neuroendocrinol 11:181–186

    Article  CAS  Google Scholar 

  • Shafiei TM, Costa HH (1990) The Susceptibility and resistance of fry and fingerlings of Oreochromis mossambicus peters to some pesticides commonly used in Sri Lanka. J Appl Ichthyol 6(2):73–80

    Article  CAS  Google Scholar 

  • Shimizu A, Yamashita M (2002) Purification of mummichog (Fundulus heteroclitus) gonadotropins and their subunits using an immunochemical assay with antisera raised against synthetic peptides. Gen Comp Endocrinol 125:79–91

    Article  CAS  Google Scholar 

  • Shimizu A, Tanaka H, Kagawa H (2003) Immunocytochemical applications of specific antisera raised against synthetic fragment peptides of mummichog GtH subunits: Examining seasonal variations of gonadotrophs (FSH cells and LH cells) in the mummichog and applications to other acanthopterygian fishes. Gen Comp Endocrinol 132:35–45

    Google Scholar 

  • Shukla L, Pandey AK (1984) Effect of three insecticides on the histoarchitecture of pituitary gland in Sarotherondon mossambicus. Uttar Pradesh J Zool 4:201–204

    Google Scholar 

  • Shukla L, Pandey AK (1986) Effects of endosulfan on the hypothalamo hypophysial complex and fish reproductive physiology. Bull Environ Contam Toxicol 36:122–131

    Article  CAS  Google Scholar 

  • Singh H, Singh TP (1982) Effect of some pesticides on hypothalamo-hypophyseal-ovarian axis in the freshwater catfish, Heteropneustes fossilis (Bloch). Environ Pollut A 27:283–288

    Article  Google Scholar 

  • Stanley KA, Curtis LR, Massey Simonich SL, Tanguay RL (2009) Endosulfan I and endosulfan sulfate disrupts zebrafish embryonic development. Aquat Toxicol 95:355–361

    Article  CAS  Google Scholar 

  • United Nations (2009) Consolidated list of products whose consumption and/or sale have been banned, withdrawn, severely restricted or not approved by governments: chemicals, issue 13. UNO, New York, p 26

  • White SA, Fernald RD (1993) Gonadotropin-releasing hormone-containing neurons change size with reproductive state in female Haplochromis burtoni. J Neurosci 13:434–441

    CAS  Google Scholar 

  • Willey JF, Krone PH (2001) Effects of endosulfan and nonylphenol on the primordial germ cell population in pre-larval zebrafish embryos. Aquat Toxicol 54:113–123

    Article  CAS  Google Scholar 

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Acknowledgments

We are grateful to R. Da Cuña for helpful suggestions to the manuscript. This work was supported by the National Council of Scientific and Technical Research (CONICET, PIP 5877 and 2302) and the University of Buenos Aires (UBACyT, x457).

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Authors and Affiliations

  1. Laboratory of Animal Embryology, Department of Biodiversity and Experimental Biology, Faculty of Exact and Natural Sciences, University of Buenos Aires, Buenos Aires, C1428EHA, Argentina

    Yanina G. Piazza, Matias Pandolfi & Fabiana L. Lo Nostro

  2. National Council of Scientific and Technical Research (CONICET), Buenos Aires, C1033AAJ, Argentina

    Yanina G. Piazza, Matias Pandolfi & Fabiana L. Lo Nostro

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  1. Yanina G. Piazza
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  2. Matias Pandolfi
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  3. Fabiana L. Lo Nostro
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Correspondence to Fabiana L. Lo Nostro.

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Piazza, Y.G., Pandolfi, M. & Lo Nostro, F.L. Effect of the Organochlorine Pesticide Endosulfan on GnRH and Gonadotrope Cell Populations in Fish Larvae. Arch Environ Contam Toxicol 61, 300–310 (2011). https://doi.org/10.1007/s00244-010-9621-3

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