Carbendazim exposure induces developmental, biochemical and behavioural disturbance in zebrafish embryos

Aquatic Toxicology

Volumn 170, Issue , 2016, Pages 390-399

  Andrade, Thayres S ^a   Henriques, Jorge F ^a   Almeida, Ana Rita ^a   Machado, Ana Luísa ^a   Koba, Olga ^b   Giang, Pham Thai ^b   Soares, Amadeu M V M ^a   Domingues, Inês ^a  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

Author keywords

Biomarkers; Locomotor response; Sublethal; Swimming behaviour; Zebrafish

Indexed keywords

CARBENDAZIM; CATALASE; CHOLINESTERASE; GLUTATHIONE TRANSFERASE; LACTATE DEHYDROGENASE; BENZIMIDAZOLE DERIVATIVE; CARBAMIC ACID DERIVATIVE; FUNGICIDE; WATER POLLUTANT;

BEHAVIORAL RESPONSE; BIOASSAY; BIOCHEMISTRY; BIOMARKER; CARBENDAZIM; ECOLOGICAL IMPACT; EMBRYO; EMBRYONIC DEVELOPMENT; ENVIRONMENTAL STRESS; FISH; LOCOMOTION; POLLUTION EXPOSURE; SUBLETHAL EFFECT; SWIMMING BEHAVIOR; TOXICITY;

ADULT; ANALYSIS OF VARIANCE; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOMATION; CONDUCTANCE; CONTROLLED STUDY; DEGRADATION; EC50; EMBRYO; EMBRYO DEVELOPMENT; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; LETHALITY; LIFE CYCLE; LIQUID CHROMATOGRAPHY; LOCOMOTION; NONHUMAN; PH MEASUREMENT; PHOTOPERIODICITY; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; STEREOMICROSCOPY; SWIMMING; TANDEM MASS SPECTROMETRY; WATER TEMPERATURE; ZEBRA FISH; ANALYSIS; ANIMAL; ANIMAL BEHAVIOR; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LARVA; METABOLISM; NONMAMMALIAN EMBRYO; PHYSIOLOGY; TOXICITY; WATER POLLUTANT;

DANIO RERIO;

ANIMALS; BEHAVIOR, ANIMAL; BENZIMIDAZOLES; CARBAMATES; CATALASE; CHOLINESTERASES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; EMBRYO, NONMAMMALIAN; FUNGICIDES, INDUSTRIAL; GLUTATHIONE TRANSFERASE; LARVA; LOCOMOTION; SWIMMING; TANDEM MASS SPECTROMETRY; WATER POLLUTANTS, CHEMICAL; ZEBRAFISH;

EID: 84951063675     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2015.11.017     Document Type: Article

References (63)

1. Bell A.M. Effects of an endocrine disrupter on courtship and aggressive behaviour of male three-spined stickleback, Gasterosteus aculeatus. Anim. Behav. 2001, 62:775-780. 10.1006/anbe.2001.1824.
2. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
3. Braunbeck T., Kais B., Lammer E., Otte J., Schneider K., Stengel D., Strecker R. The fish embryo test (FET): origin, applications, and future. Environ. Sci. Pollut. Res. Int. 2014, 10.1007/s11356-014-3814-7.
4. Clairborne A. Catalase activity. CRC Handbook of Methods in Oxygen Radical Research 1985, 283-284. CRC Press, Boca Raton, FL. R.A. Greenwald (Ed.).
5. Clotfelter E.D., Bell A.M., Levering K.R. The role of animal behaviour in the study of endocrine-disrupting chemicals. Anim. Behav. 2004, 68:665-676. 10.1016/j.anbehav.2004.05.004.
6. Cuppen J.G.M., Van den Brink P.J., Camps E., Uil K.F., Brock T.C.M. Impact of the fungicide carbendazim in freshwater microcosms. I. Water quality, breakdown of particulate organic matter and responses of macroinvertebrates. Aquat. Toxicol. 2000, 48:233-250. 10.1016/s0166-445x(99)36-3.
7. Cuppen J.G.M., Van den Brink P.J., Camps E., Uil K.F., Brock T.C.M. Impact of the fungicide carbendazim in freshwater microcosms. I. Water quality, breakdown of particulate organic matter and responses of macroinvertebrates. Aquat. Toxicol. 2000, 48:233-250. 10.1016/S0166-445X(99)00036-3.
8. Daam M.A., Satapornvanit K., Van den Brink P.J., Nogueira A.J.A. Direct and indirect effects of the fungicide Carbendazim in tropical freshwater microcosms. Arch. Environ. Contam. Toxicol. 2010, 58:315-324. 10.1007/s00244-009-9367-y.
9. Davidse L.C. Benzimidazole fungicides: mechanism of action and biological impact. Annu. Rev. Phytopathol. 1986, 24:43-65. 10.1146/annurev.py.24.090186.000355.
10. Diamantino T.C., Almeida E., Soares A.M.V.M., Guilhermino L. Lactate dehydrogenase activity as an effect criterion in toxicity tests with Daphnia magna straus. Chemosphere 2001, 45:553-560. 10.1016/S0045-6535(01)00029-7.
11. Domingues I., Guilhermino L., Soares A.M.V.M., Nogueira A.J.A., Monaghan K.A. Influence of exposure scenario on pesticide toxicity in the midge Kiefferulus calligaster (Kieffer). Ecotoxicol. Environ. Saf. 2009, 72:450-457. 10.1016/j.ecoenv.2007.10.009.
12. Domingues I., Oliveira R., Lourenço J., Grisolia C.K., Mendo S., Soares M.V.M. Biomarkers as a tool to assess effects of chromium (VI): comparison of responses in zebrafish early life stages and adults. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2010, 152:338-345. 10.1016/j.cbpc.2010.05.010.
13. Ellman G.L., Courtney K.D., Andres V., Featherstone R.M. A new rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 1961, 7:88-95.
14. Farag A., Ebrahim H., ElMazoudy R., Kadous E. Developmental toxicity of fungicide carbendazim in female mice. Birth Defects Res. B Dev. Reprod. Toxicol. 2011, 92:122-130. 10.1002/bdrb.20290.
15. Ferreira A.L.G., Loureiro S., Soares A.M.V.M. Toxicity prediction of binary combinations of cadmium, carbendazim and low dissolved oxygen on Daphnia magna. Aquat. Toxicol. 2008, 89:28-39. 10.1016/j.aquatox.2008.05.012.
16. Fredriksson A., Pontén E., Gordh T., Eriksson P. Neonatal exposure to a combination of N-methyl-D-aspartate and gamma-aminobutyric acid type A receptor anesthetic agents potentiates apoptotic neurodegeneration and persistent behavioral deficits. Anesthesiology 2007, 107:427-436. 10.1097/01 anes.0000278892.62305.9c.
17. Habig W.H., Jakoby W.B. Assays for differentiation of glutathione S-transferases. Methods Enzymol. 1981, 77:398-405.
18. Handy R., Sims D., Giles A., Campbell H., Musonda M. Metabolic trade-off between locomotion and detoxification for maintenance of blood chemistry and growth parameters by rainbow trout (Oncorhynchus mykiss) during chronic dietary exposure to copper. Aquat. Toxicol. 1999, 47:23-41. 10.1016/S0166-445X(99)00004-1.
19. Hyne R.V., Maher W.A. Invertebrate biomarkers: links to toxicosis that predict population decline. Ecotoxicol. Environ. Saf. 2003, 54:366-374. 10.1016/S0147-6513(02) 00119-7.
20. Ireland C., Gull K., Gutteridge W., Pogson C. The interaction of benzimidazole carbamates with mammalian microtobule protein. Biochem. Pharmacol. 1979.
21. Irons T.D., MacPhail R.C., Hunter D.L., Padilla S. Acute neuroactive drug exposures alter locomotor activity in larval zebrafish. Neurotoxicol. Teratol. 2010, 32:84-90. http://dx.doi.org/10.1016/j.ntt.2009.04.066.
22. Jiang H., Zhang X.-J. Acetylcholinesterase and apoptosis. A novel perspective for an old enzyme. FEBS J. 2008, 275:612-617. 10.1111/j.1742-4658.2007.06236.x.
23. Jiang J., Wu S., Wu C., An X., Cai L., Zhao X. Embryonic exposure to carbendazim induces the transcription of genes related to apoptosis, immunotoxicity and endocrine disruption in zebrafish (Danio rerio). Fish Shellfish Immunol. 2014, 41:493-500. 10.1016/j.fsi.2014.09.037.
24. Jiang J., Wu S., Wang Y., An X., Cai L., Zhao X., Wu C. Carbendazim has the potential to induce oxidative stress, apoptosis, immunotoxicity and endocrine disruption during zebrafish larvae development. Toxicol. In Vitro 2015, 29:1473-1481. 10.1016/j.tiv.2015.06.003.
25. Kim D.-J., Seok S.-H., Baek M.-W., Lee H.-Y., Na Y.-R., Park S.-H., Lee H.-K., Dutta N.K., Kawakami K., Park J.-H. Benomyl induction of brain aromatase and toxic effects in the zebrafish embryo. J. Appl. Toxicol. 2009, 29:289-294. 10.1002/jat.1405.
26. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 1995, 203:253-310. 10.1002/aja.1002030302.
27. Kegley, S.E., Hill, B.R., Orme S., Choi A.H., 2014. PAN Pesticide Database, Pesticide Action Network, North America (Oakland, CA), http:www.pesticideinfo.org (accessed 10.11.15.).
28. Klüver N., König M., Ortmann J., Massei R., Paschke A., Kühne R., Scholz S. Fish embryo toxicity test: identification of compounds with weak toxicity and analysis of behavioral effects to improve prediction of acute toxicity for neurotoxic compounds. Environ. Sci. Technol. 2015, 49:7002-7011. 10.1021/acs.est.5b01910.
29. Lepš, J., Šmilauer, P., 2003. Multivariate analysis of ecological data using CANOCO.
30. Lim J., Miller M.G. The role of the benomyl metabolite carbendazim in benomyl-induced testicular toxicity. Toxicol. Appl. Pharmacol. 1997, 142:401-410. 10.1006/taap.1996.8042.
31. Little E.E., Finger S.E. Swimming behavior as an indicator of sublethal toxicity in fish. Environ. Toxicol. Chem. 1990, 9:13-19. 10.1002/etc.5620090103.
32. Ludwikowska, A., Bojarski, B., Socha, M., Lutnicka, H., Trzeciak, K.B., 2013. The effect of carbendazim on embryonic Prussian carp (Carassius gibelio) development and hatching 367-371. doi:10.2478/aopf-2013-0038.
33. Mallat E., Barceló D., Tauler R. Degradation study of benomyl and carbendazim in water by liquid chromatography and multivariate curve resolution methods. Chromatographia 1997, 46:342-350. 10.1007/bf02490871.
34. Min E.Y., Kang J.-C. Effect of waterborne benomyl on the hematological and antioxidant parameters of the Nile tilapia, Oreochromis niloticus. Pestic. Biochem. Physiol. 2008, 92:138-143. 10.1016/j.pestbp.2008.07.007.
35. Nakai M., Miller M., Carnes K., Hess R. Stage-specific effects of the fungicide carbendazim on Sertoli cell microtubules in rat testis. Tissue Cell 2002, 34:73-80. 10.1016/S0040-8166(02) 00006-X.
36. ® fungicide. Afr. J. Aquat. Sci. 2015, 40:63-71. 10.2989/16085914.2015.1014022.
37. OECD Test No. 236: fish embryo acute toxicity (FET) test. OECD Guidelines for the Testing of Chemicals 2013, OECD Publishing, Section 2. 10.1787/9789264203709-en.
38. Oliveira R., Domingues I., Koppe Grisolia C., Soares A.M.V.M. Effects of triclosan on zebrafish early-life stages and adults. Environ. Sci. Pollut. Res. Int. 2009, 16:679-688. 10.1007/s11356-009-0119-3.
39. Olsen T., Ellerbeck L., Fisher T., Callaghan A., Crane M. Variability in acetylcholinesterase and glutathione S-transferase activities in Chironomus riparius Meigen deployed in situ at uncontaminated field sites. Environ. Toxicol. Chem. 2001, 20:1725-1732.
40. Padilla S., Hunter D.L., Padnos B., Frady S., MacPhail R.C. Assessing locomotor activity in larval zebrafish: influence of extrinsic and intrinsic variables. Neurotoxicol. Teratol. 2011, 33:624-630. 10.1016/j.ntt.2011.08.005.
41. Palanikumar L., Kumaraguru a.K., Ramakritinan C.M., Anand M. Toxicity, biochemical and clastogenic response of chlorpyrifos and carbendazim in milkfish Chanos chanos. Int. J. Environ. Sci. Technol. 2014, 11:765-774. 10.1007/s13762-013-0264-6.
42. Palma G., Sánchez A., Olave Y., Encina F., Palma R., Barra R. Pesticide levels in surface waters in an agricultural-forestry basin in Southern Chile. Chemosphere 2004, 57:763-770. 10.1016/j.chemosphere.2004.08.047.
43. Pontén E., Viberg H., Gordh T., Eriksson P., Fredriksson A. Clonidine abolishes the adverse effects on apoptosis and behaviour after neonatal ketamine exposure in mice. Acta Anaesthesiol. Scand. 2012, 56:1058-1065. 10.1111/j.1399- 6576.2012.02722.x.
44. Puymirat J., Etongue-Mayer P., Dussault J.H. Thyroid hormones stabilize acetylcholinesterase mRNA in neuro-2A cells that overexpress the β1 thyroid receptor. J. Biol. Chem. 1995, 270(51):30651-30656.
45. Core Team R. R: A Language and Environment for Statistical Computing 2014, R Foundation for Statistical Computing, Vienna, Austria.
46. Readman J.W., Albanis T.A., Barcelo D., Galassi S., Tronczynski J., Gabrielides G.P. Fungicide contamination of Mediterranean estuarine waters: Results from a MED POL pilot survey. Mar. Pollut. Bull. 1997, 34:259-263. 10.1016/S0025-326X(97)00101- X.
47. Ribeiro F., Ferreira N.C.G., Ferreira A., Soares A.M.V.M., Loureiro S. Is ultraviolet radiation a synergistic stressor in combined exposures? The case study of Daphnia magna exposure to UV and carbendazim. Aquat. Toxicol. 2011, 102:114-122. 10.1016/j.aquatox.2011.01.007.
48. Rico A., Waichman A.V., Geber-Corrêa R., Van Den Brink P.J. Effects of malathion and carbendazim on Amazonian freshwater organisms: comparison of tropical and temperate species sensitivity distributions. Ecotoxicology 2011, 20:625-634. 10.1007/s10646-011-0601-9.
49. Sárria M.P., Soares J., Vieira M.N., Castro L., Monteiro N.M. Rapid-behaviour responses as a reliable indicator of estrogenic chemical toxicity in zebrafish juveniles. Chemosphere 2011, 85:1543-1547. 10.1016/j.chemosphere.2011.07.048.
50. Scholz S., Fischer S., Gündel U., Küster E., Luckenbach T., Voelker D. The zebrafish embryo model in environmental risk assessment- applications beyond acute toxicity testing. Environ. Sci. Pollut. Res. Int. 2008, 15:394-404. 10.1007/s11356-008-0018-z.
51. Scholz S., Sela E., Blaha L., Braunbeck T., Galay-Burgos M., García-Franco M., Guinea J., Klüver N., Schirmer K., Tanneberger K., Tobor-Kapłon M., Witters H., Belanger S., Benfenati E., Creton S., Cronin M.T.D., Eggen R.I.L., Embry M., Ekman D., Gourmelon A., Halder M., Hardy B., Hartung T., Hubesch B., Jungmann D., Lampi M.A., Lee L., Léonard M., Küster E., Lillicrap A., Luckenbach T., Murk A.J., Navas J.M., Peijnenburg W., Repetto G., Salinas E., Schüürmann G., Spielmann H., Tollefsen K.E., Walter-Rohde S., Whale G., Wheeler J.R., Winter M.J. A European perspective on alternatives to animal testing for environmental hazard identification and risk assessment. Regul. Toxicol. Pharmacol. 2013, 67:506-530. 10.1016/j.yrtph.2013.10.003.
52. Scott G.R., Sloman K.A. The effects of environmental pollutants on complex fish behaviour: integrating behavioural and physiological indicators of toxicity. Aquat. Toxicol. 2004, 68:369-392. 10.1016/j.aquatox.2004.03.016.
53. Selderslaghs I.W.T., Hooyberghs J., De Coen W., Witters H.E. Locomotor activity in zebrafish embryos: a new method to assess developmental neurotoxicity. Neurotoxicol. Teratol. 2010, 32:460-471. 10.1016/j.ntt.2010.03.002.
54. Selmanoğlu G., Barlas N., Songür S., Koçkaya E.A. Carbendazim-induced haematological, biochemical and histopathological changes to the liver and kidney of male rats. Hum. Exp. Toxicol. 2001, 20:625-630.
55. Sharma D.R., Sunkaria A., Bal A., Bhutia Y.D., Vijayaraghavan R., Flora S.J.S., Gill K.D. Neurobehavioral impairments, generation of oxidative stress and release of pro-apoptotic factors after chronic exposure to sulphur mustard in mouse brain. Toxicol. Appl. Pharmacol. 2009, 240:208-218. 10.1016/j.taap.2009.06.015.
56. Soreq H., Seidman S. Acetylcholinesterase- new roles for an old actor. Nat. Rev. Neurosci. 2001, 2:294-302. 10.1038/35067589.
57. Tierney K.B. Behavioural assessments of neurotoxic effects and neurodegeneration in zebrafish. Biochim. Biophys. Acta Mol. Basis Dis. 2011, 1812:381-389. 10.1016/j.bbadis.2010.10.011.
58. Ulhaq M., Örn S., Carlsson G., Morrison D.a., Norrgren L. Locomotor behavior in zebrafish (Danio rerio) larvae exposed to perfluoroalkyl acids. Aquat. Toxicol. 2013, 144-145:332-340. 10.1016/j.aquatox.2013.10.021.
59. Urani C., Chiesara E., Galvani P., Marabini L., Santagostino A., Camatini M. Benomyl affects the microtubule cytoskeleton and the glutathione level of mammalian primary cultured hepatocytes. Toxicol. Lett. 1995, 76:135-144.
60. Van den Brink P.J., Hattink J., Bransen F., Van Donk E., Brock T.C.M. Impact of the fungicide carbendazim in freshwater microcosms. II. Zooplankton, primary producers and final conclusions. Aquat. Toxicol. 2000, 48:251-264. 10.1016/S0166-445X(99) 00037-5.
61. Vassault A. Lactate Dehydrogenase 1983, Academic Press, New York.
62. Yoon C.-S., Jin J.-H., Park J.-H., Yeo C.-Y., Kim S.-J., Hwang Y.-G., Hong S.-J., Cheong S.-W. Toxic effects of carbendazim and n-butyl isocyanate, metabolites of the fungicide benomyl, on early development in the African clawed frog, Xenopus laevis. Environ. Toxicol. 2008, 23:131-144. 10.1002/tox.20338.
63. Zhang X.J., Yang L., Zhao Q., Caen J.P., He H.Y., Jin Q.H., Guo L.H., Alemany M., Zhang L.Y., Shi Y.F. Induction of acetylcholinesterase expression during apoptosis in various cell types. Cell Death Diff. 2002, 9:790-800. 10.1038/sj.cdd.4401034.