Embryotoxic, teratogenic and genotoxic effect in zebrafish (Danio rerio) by exposure to arsenic

Authors

  • Marco Antonio Sánchez Olivares Universidad Autónoma del Estado de Hidalgo
  • Juan Carlos Gaytán-Oyarzun Universidad Autónoma del Estado de Hidalgo https://orcid.org/0000-0003-3498-0441
  • Francisco Prieto-García Universidad Autónoma del Estado de Hidalgo
  • Maria Estela Pérez-Cruz Universidad Nacional Autónoma de México https://orcid.org/0000-0001-5244-8534

Keywords:

erythrocytes, genotoxicity, micronuclei, malformations, teratogenesis

Abstract

Background. Understanding the toxicity mechanism of arsenic has been hampered by biological, chemical factors, including the dose response ratio, the specificity and sensitivity of species used in bioassays from toxicological studies to understand their toxicodynamics. Goals. The purpose of this study was to evaluate the embryotoxic, teratogenic and genotoxic effect caused by exposure to arsenic, through the frequency analysis of malformations and micronuclei in peripheral blood erythrocytes in zebrafish. Methods. The toxicity curve of arsenic in zebrafish embryos was calculated from exposure to concentrations between 0.0031 and 0.05 mg L-1 of sodium arsenite (NaAsO2 ) for 72 hours to determine the mean lethal concentration (LC50) for the embryotoxicity and teratogenesis test. For the genotoxicity test, the calculation of the toxicity curve with adult zebrafish that were exposed to concentrations between 0.035 and 0.044 mg L-1 for 48 hours was previously performed in order to establish LC50. Results. The effect of sodium arsenite was shown to be statistically positive for embryotoxicity and teratogenesis tests at the evaluated concentrations. Exposure to sodium arsenite resulted in abnormal embryonic development at each of the test concentrations, in addition to malformations. And a statistically significant increase in the frequency of micronucleated erythrocytes of 0.035, showing genotoxic damage of arsenic. Conclusions. This study showed that the induction of nuclear abnormalities in erythrocytes, as well as abnormalities in embryonic development, are extremely sensitive indicators in the study of toxicological effects, and suggest that the risk potential of this metalloid should be tested in future research.

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References

Adeyemi, J.A., A. da Cunha Martins-Junior & F. Barbosa. 2015. Teratogenicity, genotoxicity and oxidative stress in zebrafish embryos (Danio rerio) co-exposed to arsenic and atrazine. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 172-173:7-12. DOI:10.1016/j.cbpc.2015.04.001

Ahmed, M.K., M. Habibullah-Al-Mamun, M.A. Hossain, M. Arif, E. Parvin, M.S. Akter & M.M. Islam. 2011. Assessing the genotoxic potentials of arsenic in tilapia (Oreochromis mossambicus) using alkaline comet assay and micronucleus test. Chemosphere 84(1):143-149. DOI:10.1016/j.chemosphere.2011.02.025

ATSDR (Agency for Toxic Substances & Disease Registry). 2007. Toxicological profiles for arsenic. Departamento de Salud y de Servicios Humanos de EUA, Servicio de Salud Pública, Atlanta, Georgia. 493 p. Also available at: Página electrónica (www.atsdr.cdc.gov/ToxProfiles/ tp2.pdf).

Bolognesi, C. & M. Hayashi. 2011. Micronucleus assay in aquatic animals. Mutagenesis 26(1): 205213. DOI:10.1093/mutage/geq073

Bolognesi, C., E. Perrone, P. Roggieri, D. Pampanin & A. Sciutto. 2006. Assessment of micronuclei induction in pheripheral erythrocytes of fish Exposed to xenobiotics under controlled conditions. Aquatic Toxicology 78(1):93-98.

Carbonell-Barrachina, A.A., A.J. Signes-Pastor, L. Vazquez-Araffljo, F. Burlo & B. Sen Gupta. 2009. Presence of arsenic in agricultural products from arsenic-endemic areas and strategies to reduce arsenic intake in rural villages. Molecular Nutrition and Food Research 53(5):531-541. DOI:10.1002/mnfr.200900038

Coelho, P., S. Costa, S. Silva, A. Walter, J. Ranville, A.C.A. Sousa, C. Costa, M. Coelho, J. García-Lestón, M.R. Pastorinho, B. Laffon, E. Pasaro, C. Harrington, A. Taylor & J.P. Teixeira. 2012. Metalloid levels in biological matrices from human populations exposed to mining contamination – Panasqueira mine (Portugal). Journal of Toxicology and Environmental Health Part:A 75(13-15):893-908. DOI:10.1080/152 87394.2012.690705

Das, R.K., A.K. Mitra, P.K. Sengupta, A. Hossain, F. Islam & G.H. Rabbanni. 2004. Arsenic concentration in rice, vegetables and fish in Bangladesh: a preliminary study. Environmental International 30(3):383- 387. DOI:10.1016/j.envint.2003.09.005

Datta, S., D. Ghosh, D.R. Saha, S. Bhattacharaya & S. Mazunmder. 2009. Chronic exposure to low concentration of arsenic is immunotoxic to fish: role of head kidney macrophages arsenic biomarkers of arsenic toxicity to Clarias batrachus. Aquatic toxicology 92(2):86-94. DOI:10.1016/j.aquatox.2009.01.002

Del Razo, L., G. Garcia-Vargas, O. Valenzuela, E. Castellanos, L. Sanchez-Pena, J. Currier, Z. Drobna, D. Loomis & M. Styblo, M. 2011. Exposure to arsenic in drinking water is associated with increased prevalence of diabetes: a cross-sectional study in the Zimapan and Lagunera regions in Mexico. Environmental Health 10:73. DOI:10.1186/ 1476-069X-10-73

Domingues, I., R. Oliveira, J. Lourenҫo, C. Grisolia, S. Mendo & A. Soares. 2010. Biomarkers are a tool to assess chromium effects (VI): comparison of responses in zebrafish early life stages and adults. Comparative Biochemistry and Physiology - Part C: Toxicology & Pharmacology 152(3):338-345. DOI:10.1016/j.cbpc.2010.05.010

Erraguntla, N.K., R.L. Sielken, C. Valdez-Flores & R.L. Grant. 2012. An updated inhalation unit risk factor for arsenic and inorganic arsenic compounds based on a combined analysis of epidemiology studies. Regulatory Toxicology and Pharmacology 64(2):329-341. DOI:10.1016/j.yrtph.2012.07.001

Fenech, M. 2002. Biomarkers of genetic damage for cancer epidemiology. Toxicology 181-182:411-416. DOI:10.1016/s0300- 483x(02)00480-8

Gaworecki, K.M., R.W. Chapman, M.G. Neely, A.R. D’Amico & L.J. Bain. 2012. Arsenic to killifish during embryogenesis alters muscle development. Toxicological Sciences 125(2):522-531. DOI:10.1093/toxsci/ kfr302

Gaytán O.J.C., L. L. González, G. Pulido-Flores, S. Monks, A.J. Gordillo-Martínez, R.B.E. Cabrera–Cruz & E. Pérez-Cruz. 2008. Evaluación de la calidad del agua en la reserva de la biosfera Barranca de Metztitlán, Hidalgo, México, a través de la inducción de malformaciones en columna vertebral en pez cebra (Danio rerio Hamilton, 1982). In: Pulido-Flores, G., A.L. López-Escamilla & M.T. Pulido-Silva (eds.). Estudios biológicos en las áreas naturales del Estado de Hidalgo. Núm. 7. Universidad Autónoma del Estado de Hidalgo. México, pp. 117-124.

Ghobadian, M., M. Nabiuni, K. Parivar, M. Fathi & J. Pazooki. 2015. Toxic effects of magnesium oxide nanoparticles on early developmental and larval stages of zebrafish (Danio rerio). Ecotoxicology and Environmental Safety 122:260-267. DOI:10.1016/j.ecoenv.2015.08.009

González, L.L. 2005. Evaluación del efecto del cloruro de mercurio (HgCl2) en la inducción de malformaciones de columna vertebral del pez cebra (Danio rerio Hamilton, 1982) durante diferentes etapas del desarrollo embrionario. Tesis de Licenciatura. Universidad Autónoma del Estado de Hidalgo. Pachuca. Hidalgo, México. 94 p.

Hallare, A., K. Nagel, H.R. Kohler & R. Triebskorn. 2006. Comparative embryotoxicity and proteotoxicity of three carrier solvents to zebrafish (Danio rerio) embryos. Ecotoxicology and Environmental Safety 63(3):378-388. DOI:10.1016/j.ecoenv.2005.07.006

Hill, A.J., H. Teraoka, W. Heideman & R.E. Peterson. 2005. Zebrafish as a model vertebrate for investigating chemical toxicity. Toxicological Sciences 86(1):6-19. DOI:10.1093/toxsci/kfi110

IBM Corp. Released. 2017. IBM SPSS for Windows. Version 25.0. Armonk, NY: IBM Corp.

Iliná, A., J. Martínez-Hernández, E. Segura-Ceniceros, J. Villarreal- Sánchez & K. Gregorio-Jáuregui. 2009. Biosorción de arsénico en materiales derivados de maracuyá. Revista Internacional de Contaminación Ambiental 25(4):201-216.

Kimmel, C.B., W.W. Ballard, S.R. Kimmel, B. Ullmann & T.F. Schilling. 1995. Stages of embryonic development of the zebrafish. Developmental Dynamics 203:252-310. DOI:10.1002/aja.1002030302

Kousar, S. & M. Javed. 2014. Assessment of DNA damage in peripheral blood erythrocytes of fish exposed to arsenic under laboratory conditions. International Journal of Current Microbiology and Applied Sciencies 3(11):877-888.

Kummar, A., P.K. Vibudh & K.K. Parimal. 2013. Fish micronucleus assay to assess genotoxic potential of arsenic at its guideline exposure in aquatic environment. Biometals 26:337-346. DOI:10.1007/ s10534-013-9620-8

Li, D., C. Lu, J. Wang, W. Hu, Z. Cao, D. Sun, H. Xia & X. Ma. 2009. Developmental mechanisms of arsenite toxicity in zebrafish (Danio rerio) embryos. Aquatic Toxicology 91(3):229-237. DOI:10.1016/j.aquatox.2008.11.007

Li, Y., F. Yang, Z. Chen, L. Shi, B. Zhang, J. Pan, X. Li, D. Sun & H. Yang. 2014. Zebrafish on a chip: a novel platform for real-time monitoring of drug-induced developmental toxicity. PloS One 9(4):1-8. DOI:10.1371/journal.pone.0094792

Liao, C.M., J.W. Tsai, M.P. Ling, H.M. Lain, Y.H. Chou & P.T. Yang. 2004. Organ-specific toxicokinetics and dose-response of arsenic in tilapia Oreochromis mossambicus. Archives of Environment Contamination and Toxicology 47(4): 502–10. DOI:10.1007/s00244-004- 3105-2

Lieschke, G.J. & P.D. Currie. 2007. Animal models of human disease: zebrafish swim into view. Nature 8(5):353-367. DOI:10.1038/nrg2091

Mccollum, C.W., N.A. Ducharme, M. Bondesson & J. Gustafsson. 2011. Developmental toxicity screening in zebrafish. Birth Defects Research Part C: Embryo Today Reviews 93(2):67-114. DOI:10.1002/ bdrc.20210

Oberamm, A. 2000. The use of a refined zebrafish embryo bioassay for the assessment of aquatic toxicity. Lab Animal 29(7):32-40.

Oliveira, R., I. Domingues, C.K. Grisolia & A.M. Soares. 2009. Effects of triclosan on zebrafish early-life stages and adults. Environmental Science and Pollution Research International 16(6):679-688. DOI:10.1007/s11356-009-0119-3

Palhares, D. & G. C. Koppe. 2002. Comparison between the micronucleus frequencies of kidney and gill erythrocytes in tilapia fish, following mitomycin C treatment. Genetics and Molecular Biology 25(3):281- 284. DOI:10.1590/S1415-47572002000300005

Prieto-García, F., O.A. Báez-Ramírez, S. Monks, J.C. Gaytán-Oyarzún & A. Zúñiga-Estrada. 2006. Acumulación, toxicidad y teratogénesis provocada por presencia de arsénico en aguas en el pez cebra (Danio rerio). AquaTIC: Revista Electrónica de Acuicultura 24:72-85.

Raldúa, D., M. André & P. J. Babin. 2008. Clofibrate and gemfibrozil induce an embryonic malabsorption syndrome in zebrafish. Toxicology and Applied Pharmacology 228(3):301-314. DOI:10.1016/j. taap.2007.11.016

Rivera, I. 2006. Determinación de la frecuencia de malformaciones en columna vertebral, opérculo y aleta en Danio rerio Hamilton, 1822, como posibles bioindicadores en la valoración de daño teratogénico. Tesis de Licenciatura. Universidad Autónoma del Estado de Hidalgo. México. 73 p.

Sayed, A.H., H.A.M. Elbaghdady & E. Zahran. 2015. Arsenic-induced genotoxicity in Nile tilapia (Orechromis niloticus); the role of Spirulina platensis extract. Environmental Monitoring and Assessment 187(12):751. DOI: 10.1007/s10661-015-4983-7

Scotto, C., J. Álvarez, C. Llanos, O. Leyva, S. Sotomayor, K. Chávez, E. Justo, O. Casso, C. Larico, W. Mayta & W. Sanga. 2013. Análisis genotóxico de muestras de agua del río Ramis (Departamento de Puno, Perú) utilizando eritrocitos de la sangre periférica del pez Cebra (Danio rerio). Catedra Villareal 1(1):23-26.

Sfakianakis, D.G., E. Ranieri, M. Kentouri & A.M. Tsatsakis. 2015. Effect of heavy metals on fish larvae deformities: a review. Environmental Research 137:246-255. DOI:10.1016/j.envres.2014.12.014

StatSoft Inc. 2011. STATISTICA (data analysis software system). Version 10. www.statsoft.com

Tchounwou, P.B., J.A. Centeno. & A.K. Patlolla. 2004. Arsenic toxicity, mutagenesis, and carcinogenesis – a health risk assessment and management approach. Molecular and Celullar Biochemistry 255(1- 2):47-55. DOI:10.1023/b:mcbi.0000007260.32981.b9

Van-Houcke, J., L. De Groef, E. Dekeyster & L. Moons. 2015. The zebrafish as a gerontology model in nervous system aging, disease, and repair. Ageing Research Reviews 24(Pt B):358-368. DOI:10.1016/j. arr.2015.10.004

Vahter, M., A. Åkesson, C. Lidén, S. Ceccatelli & M. Berglund. 2007. Gender differences in the disposition and toxicity of metals. Environmental Research 104(1):85-95. DOI:10.1016/j.envres.2006.08.003

Westerfield, M. 2007. The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio). University of Oregon Press, Oregon. 385 p.

Yadav, K.K. & S.P. Trivedi. 2009. Sublethal exposure of heavy metals induces micronuclei in fish, Channa punctata. Chemosphere 77(11):1495-500. DOI:10.1016/j.chemosphere.2009.10.022

Yamamura, S. & S. Amachi. 2014. Microbiology of inorganic arsenic: From metabolism to bioremediation. Journal of Bioscience and Bioengineering 118(1):1-9. DOI:10.1016/j.jbiosc.2013.12.011

Yang, F., Z. Chen, J. Pan, X. Li, J. Feng & H. Yang. 2011. An integrated microfluidic array system for evaluating toxicity and teratogenicity of drugs on embryonic zebrafish developmental dynamics. Biomicrofluidics 5(2):24115. DOI:10.1063/1.3605509

Yu, Y.L., H.L. Li, Y.C. Wang & X.G. Qiao. 2011. The effect of thiram on heart development of zebrafish embryos. Journal of Inner Mongolia University for Nationalities 3:1-7. Zhang, C., C. Willett & T. Fremgen. 2003. Zebrafish: an animal model for toxicological studies. Current Protocols in Toxicology 1:1.7.1- 11.0.2. DOI:10.1002/0471140856.tx0107s17

Zhu, Y., J. Wang, Y. Bai & R. Zhang. 2004. Cadmium, chromium, and copper induce polychromatocyte micronuclei in carp (Cyprinus carpio L.). Bulletin of Environmental Contamination and Toxicology 72(1):78- 86. DOI:10.1007/s00128-003-0243-6

Published

2022-02-04

How to Cite

Sánchez Olivares, M. A., Gaytán-Oyarzun, J. C., Prieto-García, F., & Pérez-Cruz, M. E. (2022). Embryotoxic, teratogenic and genotoxic effect in zebrafish (Danio rerio) by exposure to arsenic. HIDROBIOLÓGICA, 31(3). Retrieved from https://hidrobiologica.izt.uam.mx/index.php/revHidro/article/view/1565

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