Advertisement

Effects of Bisphenol A on redox balance in red blood and sperm cells and spermatic quality in zebrafish Danio rerio

  • C. R. Silveira
  • A. S. Varela Junior
  • C. D. Corcini
  • S. L. Soares
  • A. N. Anciuti
  • M. T. Kütter
  • P. E. MartínezEmail author
Article

Abstract

Bisphenol-A (BPA) is a potential endocrine disruptor besides being associated with oxidative damage in several vertebrate classes. In the present study we investigated oxidative effects in erythrocytes and sperm cells as well as spermatic quality in Danio rerio exposed to 14 days at BPA concentrations of 2, 10 and 100 μg/L. Organelles structure, reactive species of oxygen (ROS) and lipoperoxidation (LPO) on erythrocytes and sperm cells were measured by flow cytometry and spermatic parameters were analyzed by the computer-assisted sperm analysis (CASA) system. For both cell types, when compared with control BPA treatment induced a significant increase in ROS and LPO production causing the membrane fluidity disorder, loss of membrane integrity and mitochondrial functionality. Furthermore, it was found a significant increase in DNA fragmentation in erythrocytes of zebrafish BPA exposed. Regarding the spermatic quality, results showed lower sperm motility in animals exposed to BPA, and alterations on velocity parameters of spermatozoa. Thus, the present study concludes that BPA affects the oxidative balance of both cell types, and that can directly affects the reproductive success of the adult Danio rerio. The sensitivity of erythrocytes to oxidative damage induced by BPA was similar to sperm cells, indicating a potential use of blood cells as indicators of oxidative damage present in fish sperm.

Keywords

Bisphenol-A Blood cells Danio rerio Oxidative stress Reproduction Sperm quality 

Notes

Acknowledgements

We would like to acknowledge the Fundação de Amparo à pesquisa Rio Grande do Sul (FAPERGS). ASV Jr (Process number 307195/2015-7) and CDC (Process number 306356/2014-7) are a research fellow from the Brazilian Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted (Experimental Animal Ethic Committee CEUA – FURG Process number 23116.000355/2016-72).

References

  1. Akhter A, Rahaman M, Suzuki R-T et al. (2018) Next-generation and further transgenerational effects of bisphenol A on zebrafish reproductive tissues. Heliyon 4:e00788.  https://doi.org/10.1016/j.heliyon.2018.e00788 CrossRefGoogle Scholar
  2. Baker TR, Peterson RE, Heideman W (2014) Using zebrafish as a model system for studying the transgenerational effects of dioxin. Toxicol Sci 138:403–411.  https://doi.org/10.1093/toxsci/kfu006 CrossRefGoogle Scholar
  3. Bambino K, Chu J (2017) Zebrafish in toxicology and environmental health. In: Current topics in developmental biology. pp 331–367.  https://doi.org/10.1016/bs.ctdb.2016.10.007
  4. Bermudez DS, Gray LE, Wilson VS (2010) Modeling the interaction of binary and ternary mixtures of estradiol with Bisphenol A and Bisphenol AF in an in vitro estrogen-mediated transcriptional activation assay (T47D-KBluc). Toxicol Sci 116:477–487.  https://doi.org/10.1093/toxsci/kfq156 CrossRefGoogle Scholar
  5. Bhandari RK, Deem SL, Holliday DK et al. (2015) Effects of the environmental estrogenic contaminants bisphenol A and 17α-ethinyl estradiol on sexual development and adult behaviors in aquatic wildlife species. Gen Comp Endocrinol 214:195–219.  https://doi.org/10.1016/j.ygcen.2014.09.014 CrossRefGoogle Scholar
  6. Bindhumol V, Chitra KC, Mathur PP (2003) Bisphenol A induces reactive oxygen species generation in the liver of male rats. Toxicology 188:117–124.  https://doi.org/10.1016/S0300-483X(03)00056-8 CrossRefGoogle Scholar
  7. Calafat AM, Ye X, Wong L-Y et al. (2008) Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003–2004. Environ Health Perspect 116:39–44.  https://doi.org/10.1289/ehp.10753 CrossRefGoogle Scholar
  8. Careghini A, Mastorgio AF, Saponaro S, Sezenna E (2015) Bisphenol A, nonylphenols, benzophenones, and benzotriazoles in soils, groundwater, surface water, sediments, and food: a review. Environ Sci Pollut Res 22:5711–5741.  https://doi.org/10.1007/s11356-014-3974-5 CrossRefGoogle Scholar
  9. Chen J, Xiao Y, Gai Z et al. (2015) Reproductive toxicity of low level bisphenol A exposures in a two-generation zebrafish assay: evidence of male-specific effects. Aquat Toxicol 169:204–214.  https://doi.org/10.1016/j.aquatox.2015.10.020 CrossRefGoogle Scholar
  10. Chitra KC, Latchoumycandane C, Mathur PP (2003) Induction of oxidative stress by bisphenol A in the epididymal sperm of rats. Toxicology 185:119–127CrossRefGoogle Scholar
  11. Chyb J, Kime DE, Szczerbik P et al. (2001) Computer-assisted analysis (CASA) of common Carp Cyprinus Carpio l. spermatozoa motility in the presence of cadmium. Arch Pol Fish 9:173–181Google Scholar
  12. Çimen MYB (2008) Free radical metabolism in human erythrocytes. Clin Chim Acta 390:1–11.  https://doi.org/10.1016/j.cca.2007.12.025 CrossRefGoogle Scholar
  13. Cocci P, Capriotti M, Mosconi G, Palermo FA (2017) Effects of endocrine disrupting chemicals on estrogen receptor alpha and heat shock protein 60 gene expression in primary cultures of loggerhead sea turtle (Caretta caretta) erythrocytes. Environ Res 158:616–624.  https://doi.org/10.1016/J.ENVRES.2017.07.024 CrossRefGoogle Scholar
  14. Coe TS, Hamilton PB, Griffiths AM et al. (2009) Genetic variation in strains of zebrafish (Danio rerio) and the implications for ecotoxicology studies. Ecotoxicology 18:144–150.  https://doi.org/10.1007/s10646-008-0267-0 CrossRefGoogle Scholar
  15. Corrales J, Kristofco LA, Steele WB et al. (2015) Global assessment of Bisphenol A in the environment. Dose-Response 13:155932581559830.  https://doi.org/10.1177/1559325815598308 CrossRefGoogle Scholar
  16. Cosson J (2010) Frenetic activation of fish spermatozoa flagella entails short-term motility, portending their precocious decadence. J Fish Biol 76:240–279.  https://doi.org/10.1111/j.1095-8649.2009.02504.x CrossRefGoogle Scholar
  17. Cosson J (2004) The ionic and osmotic factors controlling motility of fish Spermatozoa. Aquac Int 12:69–85.  https://doi.org/10.1023/B:AQUI.0000017189.44263.bc CrossRefGoogle Scholar
  18. Crain DA, Eriksen M, Iguchi T et al. (2007) An ecological assessment of Bisphenol-A: evidence from comparative biology Reprod Toxicol 24:225–239.  https://doi.org/10.1016/j.reprotox.2007.05.008 CrossRefGoogle Scholar
  19. de Kermoysan G, Joachim S, Baudoin P et al. (2013) Effects of bisphenol A on different trophic levels in a lotic experimental ecosystem. Aquat Toxicol 144–145:186–198.  https://doi.org/10.1016/j.aquatox.2013.09.034 CrossRefGoogle Scholar
  20. Devasagayam TPA, Tilak JC, Boloor KK et al. (2004) Free radicals and antioxidants in human health: current status and future prospects. J Assoc Physicians India 52:794–804Google Scholar
  21. Dietrich MA, Arnold GJ, Nynca J et al. (2014) Characterization of carp seminal plasma proteome in relation to blood plasma. J Proteom 98:218–232.  https://doi.org/10.1016/J.JPROT.2014.01.005 CrossRefGoogle Scholar
  22. Domínguez-Rebolledo A, Martínez-Pastor F, Bisbal A et al. (2011) Response of thawed epidi dymal red deer spermatozoa to increasing concentrations of hydrogen peroxide, and importance of individual male variability. Reprod Domest Anim 46:393–403.  https://doi.org/10.1111/j.1439-0531.2010.01677.x CrossRefGoogle Scholar
  23. Duan P, Hu C, Butler HJ et al. (2016) Effects of 4-nonylphenol on spermatogenesis and induction of testicular apoptosis through oxidative stress-related pathways. Reprod Toxicol 62:27–38.  https://doi.org/10.1016/j.reprotox.2016.04.016 CrossRefGoogle Scholar
  24. Dziewirska E, Hanke W, Jurewicz J (2018) Environmental non-persistent endocrine-disrupting chemicals exposure and reproductive hormones levels in adult men. Int J Occup Med Environ Health  https://doi.org/10.13075/ijomeh.1896.01183
  25. Dzyuba V, Cosson J (2014) Motility of fish spermatozoa: from external signaling to flagella response. Reprod Biol 14:165–175.  https://doi.org/10.1016/J.REPBIO.2013.12.005 CrossRefGoogle Scholar
  26. Farag MR, Alagawany M (2018) Erythrocytes as a biological model for screening of xenobiotics toxicity. Chem Biol Inter 279:73–83.  https://doi.org/10.1016/j.cbi.2017.11.007 CrossRefGoogle Scholar
  27. Flint S, Markle T, Thompson S, Wallace E (2012) Bisphenol A exposure, effects, and policy: a wildlife perspective. J Environ Manag 104:19–34.  https://doi.org/10.1016/j.jenvman.2012.03.021 CrossRefGoogle Scholar
  28. Gao M, Yang Y, Lv M et al. (2018) Oxidative stress and DNA damage in zebrafish liver due to hydroxyapatite nanoparticles-loaded cadmium. Chemosphere 202:498–505.  https://doi.org/10.1016/j.chemosphere.2018.03.146 CrossRefGoogle Scholar
  29. Gillan L, Evans G, Maxwell WMC (2005) Flow cytometric evaluation of sperm parameters in relation to fertility potential. Theriogenology 63:445–457.  https://doi.org/10.1016/j.theriogenology.2004.09.024 CrossRefGoogle Scholar
  30. Gran View Research (2015) Global Bisphenol A (BPA) market by application (appliances, automotive, consumer, construction, electrical & electronics) expected to reach USD 20.03 billion by 2020: Grand View Research, Inc. https://www.grandviewresearch.com/press-release/global-bisphenol-a-bpa-market. Accessed 28 Jun 2018
  31. Hagedorn M, McCarthy M, Carter VL, Meyers SA (2012) Oxidative stress in zebrafish (Danio rerio) sperm. PLoS ONE 7:e39397.  https://doi.org/10.1371/journal.pone.0039397 CrossRefGoogle Scholar
  32. Hamed HS, Abdel-Tawwab M (2017) Ameliorative effect of propolis supplementation on alleviating bisphenol-A toxicity: growth performance, biochemical variables, and oxidative stress biomarkers of Nile tilapia, Oreochromis niloticus (L.) fingerlings. Comp Biochem Physiol Part—C Toxicol Pharm 202:63–69.  https://doi.org/10.1016/j.cbpc.2017.08.001 CrossRefGoogle Scholar
  33. Harayashiki CAY, Junior ASV, Machado AA, de S et al. (2013) Toxic effects of the herbicide Roundup in the guppy Poecilia vivipara acclimated to fresh water. Aquat Toxicol 142–143:176–184.  https://doi.org/10.1016/j.aquatox.2013.08.006 CrossRefGoogle Scholar
  34. Hassan ZK, Elobeid MA, Virk P, et al. (2012) Bisphenol a induces hepatotoxicity through oxidative stress in rat model. Oxid Med Cell Longev 2012.  https://doi.org/10.1155/2012/194829
  35. Hatef A, Alavi SMH, Abdulfatah A et al. (2012) Adverse effects of bisphenol A on reproductive physiology in male goldfish at environmentally relevant concentrations. Ecotoxicol Environ Saf 76:56–62.  https://doi.org/10.1016/j.ecoenv.2011.09.021 CrossRefGoogle Scholar
  36. Sohoni PCRT, Tyler CR, Hurd K et al. (2001) Reproductive effects of long-term exposure to Bisphenol A in the fathead minnow (Pimephales promelas) Environ Sci Technol 35:2917–2925CrossRefGoogle Scholar
  37. Huang YQ, Wong CKC, Zheng JS et al. (2012) Bisphenol A (BPA) in China: a review of sources, environmental levels, and potential human health impacts. Environ Int 42:91–99.  https://doi.org/10.1016/j.envint.2011.04.010 CrossRefGoogle Scholar
  38. Hulak M, Gazo I, Shaliutina A, Linhartova P (2013) In vitro effects of bisphenol A on the quality parameters, oxidative stress, DNA integrity and adenosine triphosphate content in sterlet (Acipenser ruthenus) spermatozoa. Comp Biochem Physiol—C Toxicol Pharm 158:64–71.  https://doi.org/10.1016/j.cbpc.2013.05.002 CrossRefGoogle Scholar
  39. Im J, Löffler FE (2016) Fate of Bisphenol A in terrestrial and aquatic environments. Environ Sci Technol 50:8403–8416.  https://doi.org/10.1021/acs.est.6b00877 CrossRefGoogle Scholar
  40. Inaba K, Morisawa S, Morisawa M (1998) Proteasomes regulate the motility of salmonid fish sperm through modulation of cAMP-dependent phosphorylation of an outer arm dyne in light chain. J Cell Sci 111(Pt 8):1105–1115Google Scholar
  41. Jalal N, Surendranath AR, Pathak JL et al. (2018) Bisphenol A (BPA) the mighty and the mutagenic. Toxicol Rep 5:76–84.  https://doi.org/10.1016/j.toxrep.2017.12.013 CrossRefGoogle Scholar
  42. Kang J-H, Kondo F, Katayama Y (2006) Human exposure to bisphenol A. Toxicology 226:79–89.  https://doi.org/10.1016/j.tox.2006.06.009 CrossRefGoogle Scholar
  43. Kourouma A, Peng D, Chao Q et al. (2014) Bisphenol A induced reactive oxygen species (ROS) in the liver and affect epididymal semen quality in adults Sprague-Dawley rats. J Toxicol Environ Health Sci 6:103–112.  https://doi.org/10.5897/JTEHS2014.0309 CrossRefGoogle Scholar
  44. Lahnsteiner F, Mansour N, Berger B (2004) The effect of inorganic and organic pollutants on sperm motility of some freshwater teleosts. J Fish Biol 65:1283–1297.  https://doi.org/10.1111/j.0022-1112.2004.00528.x CrossRefGoogle Scholar
  45. Lamirande EDe, Gagnon C (1995) Impact of reactive oxygen species on spermatozoa: a balancing act between beneficial and detrimental effects. Hum Reprod 10:15–21CrossRefGoogle Scholar
  46. Li D, Chen Q, Cao J et al. (2016) The chronic effects of lignin-derived bisphenol and bisphenol A in Japanese medaka Oryzias latipes. Aquat Toxicol 170:199–207.  https://doi.org/10.1016/j.aquatox.2015.11.024 CrossRefGoogle Scholar
  47. Li P, Li Z-H, Dzyuba B et al. (2010) Evaluating the impacts of osmotic and oxidative stress on Common Carp (Cyprinus carpio, L.) sperm caused by cryopreservation techniques. Biol Reprod 83:852–858.  https://doi.org/10.1095/biolreprod.110.085852 CrossRefGoogle Scholar
  48. Liu Y, Tam NFY, Guan Y et al. (2011) Acute toxicity of nonylphenols and bisphenol A to the embryonic development of the abalone Haliotis diversicolor supertexta. Ecotoxicology 20:1233–1245.  https://doi.org/10.1007/s10646-011-0672-7 CrossRefGoogle Scholar
  49. Lopes FM, Varela Junior AS, Corcini CD et al. (2014) Effect of glyphosate on the sperm quality of zebrafish Danio rerio. Aquat Toxicol 155:322–326.  https://doi.org/10.1016/j.aquatox.2014.07.006 CrossRefGoogle Scholar
  50. Lv Y, Lu S, Dai Y et al. (2017) Higher dermal exposure of cashiers to BPA and its association with DNA oxidative damage. Environ Int 98:69–74.  https://doi.org/10.1016/j.envint.2016.10.001 CrossRefGoogle Scholar
  51. Maćczak A, Cyrkler M, Bukowska B, Michałowicz J (2017a) Bisphenol A, bisphenol S, bisphenol F and bisphenol AF induce different oxidative stress and damage in human red blood cells (in vitro study). Toxicol In Vitro 41:143–149.  https://doi.org/10.1016/j.tiv.2017.02.018 CrossRefGoogle Scholar
  52. Maćczak A, Duchnowicz P, Sicińska P et al. (2017b) The in vitro comparative study of the effect of BPA, BPS, BPF and BPAF on human erythrocyte membrane; perturbations in membrane fluidity, alterations in conformational state and damage to proteins, changes in ATP level and Na+/K+ATPase and AChE activities. Food Chem Toxicol 110:351–359.  https://doi.org/10.1016/j.fct.2017.10.028 CrossRefGoogle Scholar
  53. Michałowicz J, Mokra K, Bak A (2015) Bisphenol A and its analogs induce morphological and biochemical alterations in human peripheral blood mononuclear cells (in vitro study). Toxicol In Vitro 29:1464–1472.  https://doi.org/10.1016/j.tiv.2015.05.012 CrossRefGoogle Scholar
  54. Mokra K, Kuźmińska-Surowaniec A, Woźniak K, Michałowicz J (2017) Evaluation of DNA-damaging potential of bisphenol A and its selected analogs in human peripheral blood mononuclear cells (in vitro study). Food Chem Toxicol 100:62–69.  https://doi.org/10.1016/j.fct.2016.12.003 CrossRefGoogle Scholar
  55. Myridakis A, Chalkiadaki G, Fotou M et al. (2016) Exposure of Preschool-Age Greek Children (RHEA Cohort) to bisphenol A, parabens, phthalates, and organophosphates. Environ Sci Technol 50:932–941.  https://doi.org/10.1021/acs.est.5b03736 CrossRefGoogle Scholar
  56. Nakagawa Y, Tayama S (2000) Metabolism and cytotoxicity of bisphenol A and other bisphenols in isolated rat hepatocytes. Arch Toxicol 74:99–105CrossRefGoogle Scholar
  57. OECD (1993) OECD Guidelines for the Testing of Chemicals. Test 203: Fish, Acute Toxicity Test. OECD PublishingGoogle Scholar
  58. Pasqualotto FF, Sharma RK, Nelson DR et al. (2000) Relationship between oxidative stress, semen characteristics, and clinical diagnosis in men undergoing infertility investigation. Fertil Steril 73:459–464CrossRefGoogle Scholar
  59. Petrunkina AM, Volker G, Weitze K-F et al. (2005) Detection of cooling-induced membrane changes in the response of boar sperm to capacitating conditions. Theriogenology 63:2278–2299.  https://doi.org/10.1016/j.theriogenology.2004.10.008 CrossRefGoogle Scholar
  60. Piehler E, Petrunkina AM, Ekhlasi-Hundrieser M, Töpfer-Petersen E (2006) Dynamic quantification of the tyrosine phosphorylation of the sperm surface proteins during capacitation. Cytometry Part A 69A:1062–1070.  https://doi.org/10.1002/cyto.a.20338 CrossRefGoogle Scholar
  61. Qiu W, Chen J, Li Y et al. (2016) Oxidative stress and immune disturbance after long-term exposure to bisphenol A in juvenile common carp (Cyprinus carpio). Ecotoxicol Environ Saf 130:93–102.  https://doi.org/10.1016/j.ecoenv.2016.04.014 CrossRefGoogle Scholar
  62. Riu A, Maire A, Grimaldi M et al. (2011) Characterization of novel ligands of ER a, Er b, and PPAR c: the case of halogenated bisphenol A and their conjugated. Metabolites 122:372–382.  https://doi.org/10.1093/toxsci/kfr132 Google Scholar
  63. Rocco L, Frenzilli G, Zito G et al. (2012) Genotoxic effects in fish induced by pharmacological agents present in the sewage of some Italian water-treatment plants. Environ Toxicol 27:18–25.  https://doi.org/10.1002/tox.20607 CrossRefGoogle Scholar
  64. Rurangwa E, Kime D, Ollevier F, Nash J (2004) The measurement of sperm motility and factors affecting sperm quality in cultured fish. Aquaculture 234:1–28.  https://doi.org/10.1016/J.AQUACULTURE.2003.12.006 CrossRefGoogle Scholar
  65. Saalfeld GQ, Varela Junior AS, Castro T et al. (2018) Low atrazine dosages reduce sperm quality of Calomys laucha mice. Environ Sci Pollut Res 25:2924–2931.  https://doi.org/10.1007/s11356-017-0657-z CrossRefGoogle Scholar
  66. Schulz RW, de França LR, Lareyre JJ et al. (2010) Spermatogenesis in fish. Gen Comp Endocrinol 165:390–411.  https://doi.org/10.1016/j.ygcen.2009.02.013 CrossRefGoogle Scholar
  67. Sergent O, Ekroos K, Lefeuvre-Orfila L et al. (2009) Ximelagatran increases membrane fluidity and changes membrane lipid composition in primary human hepatocytes. Toxicol In Vitro 23:1305–1310.  https://doi.org/10.1016/j.tiv.2009.07.019 CrossRefGoogle Scholar
  68. Shao B, Zhu L, Dong M et al. (2012) DNA damage and oxidative stress induced by endosulfan exposure in zebrafish (Danio rerio). Ecotoxicology 21:1533–1540.  https://doi.org/10.1007/s10646-012-0907-2 CrossRefGoogle Scholar
  69. Shimada N, Yamauchi K (2004) Characteristics of 3,5,3′-triiodothyronine (T3)-uptake system of tadpole red blood cells: effect of endocrine-disrupting chemicals on cellular T3 response. J Endocrinol 183:627–637.  https://doi.org/10.1677/joe.1.05893 CrossRefGoogle Scholar
  70. Shrader EA, Henry TR, Greeley MS, Bradley BP (2003) Proteomics in zebrafish exposed to endocrine disrupting chemicals. Ecotoxicology 12:485–488CrossRefGoogle Scholar
  71. Sikka SC (2001) Relative impact of oxidative stress on male reproductive function. Curr Med Chem 8:851–862CrossRefGoogle Scholar
  72. Sorensen AM (1979) Repro lab: a laboratory manual for animal reproduction. American Press, Boston, MA, USAGoogle Scholar
  73. Tao S, Zhang Y, Yuan C et al. (2016) Oxidative stress and immunotoxic effects of bisphenol A on the larvae of rare minnow Gobiocypris rarus. Ecotoxicol Environ Saf 124:377–385.  https://doi.org/10.1016/j.ecoenv.2015.11.014 CrossRefGoogle Scholar
  74. Tiwari D, Kamble J, Chilgunde S et al. (2012) Clastogenic and mutagenic effects of bisphenol A: an endocrine disruptor. Mutat Res - Genet Toxicol Environ Mutagen 743:83–90.  https://doi.org/10.1016/j.mrgentox.2011.12.023 CrossRefGoogle Scholar
  75. Vandenberg LN, Hunt PA, Myers JP, vom Saal FS (2013) Human exposures to bisphenol A: mismatches between data and assumptions. Rev Environ Health 28:37–58.  https://doi.org/10.1515/reveh-2012-0034 CrossRefGoogle Scholar
  76. Vandenberg LN, Maffini MV, Sonnenschein C et al. (2009) Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr Rev 30:75–95.  https://doi.org/10.1210/er.2008-0021 CrossRefGoogle Scholar
  77. Vernet P, Aitken R, Drevet J (2004) Antioxidant strategies in the epididymis. Mol Cell Endocrinol 216:31–39.  https://doi.org/10.1016/j.mce.2003.10.069 CrossRefGoogle Scholar
  78. Verstegen J, Iguer-Ouada M, Onclin K (2002) Computer assisted semen analyzers in andrology research and veterinary practice. Theriogenology 57:149–179CrossRefGoogle Scholar
  79. Yamamoto T, Yasuhara A, Shiraishi H, Nakasugi O (2001) Bisphenol A in hazardous waste landfill leachates. Chemosphere 42:415–418.  https://doi.org/10.1016/S0045-6535(00)00079-5 CrossRefGoogle Scholar
  80. Zhang T, Liu Y, Chen H et al. (2017) The DNA methylation status alteration of two steroidogenic genes in gonads of rare minnow after bisphenol A exposure. Comp Biochem Physiol Part - C Toxicol Pharm 198:9–18.  https://doi.org/10.1016/j.cbpc.2017.05.001 CrossRefGoogle Scholar
  81. Zhao H, Wei J, Xiang L, Cai Z (2018) Mass spectrometry investigation of DNA adduct formation from bisphenol A quinone metabolite and MCF-7 cell DNA. Talanta 182:583–589.  https://doi.org/10.1016/j.talanta.2018.02.037 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • C. R. Silveira
    • 1
  • A. S. Varela Junior
    • 1
  • C. D. Corcini
    • 2
  • S. L. Soares
    • 2
  • A. N. Anciuti
    • 2
  • M. T. Kütter
    • 1
  • P. E. Martínez
    • 1
    Email author
  1. 1.Reprodução Animal Comparada, Instituto de Ciências BiológicasUniversidade Federal do Rio GrandeRio GrandeBrazil
  2. 2.Reprodução Animal, Faculdade de VeterináriaUniversidade Federal de PelotasPelotasBrazil

Personalised recommendations