Vet Med - Czech, 2016, 61(10):577-589 | DOI: 10.17221/212/2015-VETMED

Adverse effects of bisphenol A on the testicular parenchyma of zebrafish revealed using histomorphological methodsOriginal Paper

A.J. Lora*, A.M. Molina*, C. Bellido, A. Blanco, J.G. Monterde, M.R. Moyano
Veterinary Faculty, University of Cordoba, Cordoba, Spain

The purpose of this study was to evaluate the consequences of bisphenol A (BPA) exposure in zebrafish (Danio rerio). Short-term effects at a testes level were assessed by means of different biomarkers in 60 male zebrafish exposed for 14 days in aquariums to different concentrations of BPA (1, 10, 100 and 1000 µg/l) in addition to a control batch. The LC-MS/MS method was used for the quantification of BPA. The BPA levels in the zebrafish tissues increased together with increasing exposure of fish to BPA. Several alterations were observed in the zebrafish testes. Particularly notable morphological changes included, a pronounced degeneration of all cell components, an increase in the percentage of the sustentacular (Sertoli) cells, and a marked decrease in the percentage of germ cells starting from concentrations of 100 µg/l of BPA. Our results indicate that histopathology and testes morphometry are sensitive biomarkers for the analysis of early effects of an environmental concentration of BPA in zebrafish experimental models. Our observations reveal that the nature and intensity of the morphological changes in the testes are concentration-dependent in the case of BPA, and manifest as adverse effects on the fish's reproductive health.

Keywords: endocrine disruption; BPA; Danio rerio; sustentacular cells; spermatogonia; spermatocytes; spermatids; spermatozoa

Published: October 31, 2016  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Lora AJ, Molina AM, Bellido C, Blanco A, Monterde JG, Moyano MR. Adverse effects of bisphenol A on the testicular parenchyma of zebrafish revealed using histomorphological methods. Vet Med - Czech. 2016;61(10):577-589. doi: 10.17221/212/2015-VETMED.
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Al-Sakran AAM, Virk P, Elobeid M, Hamed SS, Siddiqui MI, Omer S, Mirghani NM (2016): Histopathological effects on testis of adult male carp, Cyprinus carpio carpio, following exposure to graded concentrations of waterborne bisphenol A. Tropical Journal of Pharmaceutical Research 15, 73-80. Go to original source...
    2. Cheng CY, Wong EWP, Lie PPY, Li MWM, Su L, Siu ER, Yan HHN, Mannu J, Mathur PP, Bonanomi M, Silvestrini B, Mruk DD (2011): Environmental toxicants and male reproductive function. Spermatogenesis 1, 2-13. Go to original source... Go to PubMed...
    3. Commission Directive 2011/8/EU of 28 January 2011 amending Directive 2002/72/EC as regards the restriction of use of Bisphenol A in plastic infant feeding bottles. Available: http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2011:026:0011:0014:EN:PDF.
    4. Crain DA, Eriksen M, Iguchi T, Jobling S, Laufer H, LeBlanc GA, Guilette Jr LJ (2007): An ecological asessment of bisphenol-A: evidence from comparative biology. Reproductive Toxicology 24, 225-239. Go to original source... Go to PubMed...
    5. Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes. Available: http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32010L0063&from=EN.
    6. Dorn PB, Chou CS, Gentempo JJ (1987): Degradation of bisphenol A in natural waters. Chemosphere 16, 1501- 1507. Go to original source...
    7. EFSA - European Food Safety Authority (2008): Statement of EFSA on a study associating bisphenol A with medical disorders. The EFSA Journal 838, 1-3. Go to original source...
    8. Flint S, Markle T, Thompson S, Wallace E (2012): Bisphenol A exposure, effects, and policy: A wildlife perspective. Journal of Environmental Management 104, 19-34. Go to original source... Go to PubMed...
    9. Hassanin A, Kuwahara S, Tsukamoto Y, Ogawa K, Hiramatsu K, Sasaki F (2002): Gonadosomatic index and testis morphology of common carp (Cyprinus carpio) in rivers contaminated with estrogenic chemicals. Journal of Veterinary Medical Science 64, 921-926. Go to original source... Go to PubMed...
    10. Hatef A, Alavi SMH, Abdulfatah A, Fontaine P, Rodina M, Linhert O (2012): Adverse effects of bisphenol A on reproductive physiology in male goldfish at environmentally relevant concentrations. Ecotoxicology and Environmental Safety 76, 56-62. Go to original source... Go to PubMed...
    11. Ishibashi H, Watanabe N, Matsumura N, Hirano M, Nagao Y, Shiratsuchi H, Kohra S, Yoshihara S, Arizono K (2005): Toxicity to early life stages and an estrogenic effect of a bisphenol A metabolite, 4-methyl-2,4-bis(4-hydroxyphenyl)pent-1-ene on the medaka (Oryzias latipes). Life Sciences 77, 2643-2655. Go to original source... Go to PubMed...
    12. Kang JH, Aasi D, Katayama Y (2007): Bisphenol A in the aquatic environment and its endocrine-disruptive effects on aquatic organisms. Critical Reviews in Toxicology 37, 670-625. Go to original source... Go to PubMed...
    13. Kinnberg K, Toft G (2003): Effects of estrogenic and antiandrogenic compounds on the testis structure of the adult guppy (Poecilia reticulata). Ecotoxicology and Environmental Safety 54, 16-24. Go to original source... Go to PubMed...
    14. Kinnberg K, Korsgaard B, Bjerregaard P, Jespersen A (2000): Effects of nonhylphenol and 17β-estradiol on vitellogenin synthesis and testis morphology in male platyfish Xiphophorus maculatus. Journal of Experimental Biology 203, 171-181. Go to original source... Go to PubMed...
    15. Li D, Chen Q, Cao J, Chen H, Li L, Cedergreen N, Xie H, Xie L (2016): The chronic effects of ligning-derived bisphenol and bisphenol A in Japanese medaka Oryzias latipes. Aquatic Toxicology 170, 199-207. Go to original source... Go to PubMed...
    16. Lopez-Casas P, Mizrak SC, Lopez-Fernandez LA, Paz M, de Rooij DG, del Mazo J (2012): The effects of different endocrine disruptors defining compound-specific alterations of gene expression profiles in the developing testis. Reproductive Toxicolology 33, 106-115. Go to original source... Go to PubMed...
    17. Mandich A, Bottero S, Benfenati E, Cevasco A, Erratico C, Maggioni S, Massari A, Pedemonte F, Vigano L (2007): In vivo exposure of carps to graded concentrations of bisphenol A. General and Comparative Endocrinology 153, 15-24. Go to original source... Go to PubMed...
    18. McGonnell IM, Fowkes RC (2006): Fishing for gene function-endocrine modelling in the zebrafish. Journal of Endocrinology 189, 425-439. Go to original source... Go to PubMed...
    19. Miles-Richardson SR, Pierens S, Nichols KM, Kramer VJ, Snyder EM, Snyder SA, Render JA, Fitzgerald SD, Giesy JP (1999): Effects of waterborne exposure to 4-nonylphenol and nonylphenol ethoxylate on secondary sex characteristics and gonads of fathead minnows (Pimephales promelas). Environmental Research 80, 122-137. Go to original source... Go to PubMed...
    20. Molina AM, Lora AJ, Blanco A, Monterde JG, Ayala N, Moyano R (2013): Endocrine-active compound evaluation: qualitative and quantitative histomorphological assessment of zebrafish gonads after bisphenol-A exposure. Ecotoxicology and Environmental Safety 88, 155-162. Go to original source... Go to PubMed...
    21. Nakamura D, Yanagiba Y, Duan Z, Ito Y, Okamura A, Asaeda N, Tagawa Y, Li C, Taya K, Zhang S, Naito H, Ramdhan DH, Kamijima M, Nakajima T (2010): Bisphenol A may cause testosterone reduction by adversely affecting both testis and pituitary systems similar to estradiol. Toxicology Letters 194, 16-25. Go to original source... Go to PubMed...
    22. OECD (1992): Guideline 210: Fish, Early Life Stage Toxicity Test. In: OECD Guidelines for Testing of Chemicals, Section 2. Available: http://www.oecd-ilibrary.org/docserver/download/9713191e.pdf?expires=1470224702&id=id&accname=guest✓sum=BA62DB6A22DE49D5BF21971F9549CD9E.
    23. OECD (1993): Guideline 204: Fish, Prolonged Toxicity Test: 14-Day-Study. In: OECD Guidelines for Testing of Chemicals, Section 2. Available: http://www.oecd-ilibrary.org/docserver/download/9720401e.pdf?expires=1470226596&id=id&accname=guest✓sum=FF3EF01FEADF44CC7129552FFBF2CEB3.
    24. OECD (1998): Guideline 212: Fish, Short-term Toxicity Test on Embryo and Sac-fry Stages. In: OECD Guidelines for Testing of Chemicals, Section 2. Available: http://www.oecd-ilibrary.org/docserver/download/9721201e.pdf?expires=1470228946&id=id&accname=guest✓sum=4A44381E3F5388FEA64F3BF10CA72776.
    25. OECD (2006): OECD Report of the validation of the 21-day fish screening asay for the detection of endocrine substances (Phase 1B). In: OECD Series on Testing and Assessment: Testing for Endocrine Disrupters, No. 61. Available: http://www.oecd.org/officialdocuments/publicdisplaydocumentpdf/?cote=env/jm/mono(2006)29&doclanguage=en.
    26. OECD (2010): OECD Guidance document for the diagnosis of endocrine-related histopathology of fish gonads. In: OECD Series on Testing and Assessment: Testing for Endocrine Disrupters, No. 123. Available: http://www.oecd.org/officialdocuments/publicdisplaydocumentpdf/?cote=env/jm/mono(2010)14&doclanguage=en.
    27. Orn S, Holbech H, Madsen TH, Norrgren L, Petersen GI (2003): Gonad development and vitellogenin production in zebrafish (Danio rerio) exposed to ethinylestradiol and methyltestosterone. Aquatic Toxicology 65, 397-411. Go to original source... Go to PubMed...
    28. Schmidt K, Stachel C, Gowik P (2008): Development and in-house validation of an LC-MS/MS method for the determination of stilbenes and resorcylic acid lactones in bovine urine. Analytical and Bioanalytical Chemistry 391, 1199-1210. Go to original source... Go to PubMed...
    29. Segner H, Caroll K, Fenske M, Janssen CR, Maack G, Pascoe D, Schafers C, Vandenbergh GF, Watts M, Wenzel A (2003): Identification of endocrine-disrupting effects in aquatic vertebrates and invertebrates: report from the European IDEA project. Ecotoxicology and Environmental Safety 54, 302-314. Go to original source... Go to PubMed...
    30. Sohoni P, Tyler CR, Hurd K, Caunter J, Hetheridge M, Williams T, Woods C, Evans M, Toy R, Gargas M, Sumpter JP (2001): Reproductive effects of long-term exposure to bisphenol A in the fathead minnow (Pimephales promelas). Environmental Science and Technology 35, 2917- 2925. Go to original source... Go to PubMed...
    31. Toyama Y, Suzuki-Toyota F, Maekawa M, Ito C, Toshimori K (2004): Adverse effects of bisphenol A to spermiogenesis in mice and rats. Archives of Histology and Cytology 67, 373-381. Go to original source... Go to PubMed...
    32. Van den Belt K, Verheyen R, Witters H (2001): Reproductive effects of ethynylestradiol and 4t-octylphenol on the zebrafish (Danio rerio). Archives of Environmental Contamination and Toxicology 41, 458-467. Go to original source... Go to PubMed...
    33. Van der Ven LT, Wester PW, Vos JG (2003): Histopathology as a tool for the evaluation of endocrine disruption in zebrafish (Danio rerio). Environmental Toxicology and Chemistry 22, 908-913. Go to original source...
    34. Villaneuve DL, Garcia-Reyero N, Escalon BL, Jensen KM, Thomas LM, Perkins EJ, Ankley GT (2012): Ecotoxicogenomics to support ecological risk assessment: A case study with bisphenol A in fish. Environmental Science and Technology 46, 51-59. Go to original source... Go to PubMed...
    35. Weber LP, Hill RL, Janz DM (2003): Developmental estrogenic exposure in zebrafish (Danio rerio): II. Histological evaluation of gametogenesis and organ toxicity. Aquatic Toxicology 63, 431-446. Go to original source... Go to PubMed...
    36. Wolf JC, Dietrich DR, Friederich U, Caunter J, Brown A (2004): Qualitative and quantitative histomorphologic assessment of fathead minnow Pimephales promelas gonads as an endpoint for evaluating endocrine-active compounds: a pilot methodology study. Toxicologic Pathology 32, 600-612. Go to original source... Go to PubMed...
    37. Yeung BH, Wan HT, Law AYS, Wong CKC (2011): Endocrine disrupting chemicals. Multiple effects on testicular signalling and spermatogenesis. Spermatogenesis 1, 231-239. Go to original source... Go to PubMed...

    This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content