Exposure to the herbicide 2,4-dichlorophenoxyacetic acid impairs mitochondrial function, oxidative status, and behavior in adult zebrafish.

2,4-D Behavior Herbicides Mitochondrial energy metabolism Oxidative status Zebrafish

Journal

Environmental science and pollution research international
ISSN: 1614-7499
Titre abrégé: Environ Sci Pollut Res Int
Pays: Germany
ID NLM: 9441769

Informations de publication

Date de publication:
Dec 2020
Historique:
received: 25 05 2020
accepted: 12 08 2020
pubmed: 18 8 2020
medline: 27 11 2020
entrez: 18 8 2020
Statut: ppublish

Résumé

2,4-Dichlorophenoxyacetic acid (2,4-D) is one of the most commonly used herbicides worldwide. While the effects of 2,4-D in target organisms are well known, its consequences in nontarget organisms are not fully explained. Therefore, the purpose of this study was to investigate the effects of the herbicide on mitochondrial energy metabolism, oxidative status, and exploratory behavior in adult zebrafish. Animal exposure to 2,4-D increased cytochrome c oxidase and catalase activities and reduced SOD/CAT ratio, moreover, increased the total distance traveled and the number of crossings. Finally, animals exposed to 2,4-D spent more time in the upper zone of the tank and traveled a long distance in the upper zone. Overall, our results indicate the 2,4-D can provoke disabling effects in nontarget organisms. The obtained data showed that exposure to 2,4-D at environmentally relevant concentrations alters mitochondrial metabolism and antioxidant status and disturbs the zebrafish innate behavior.

Identifiants

pubmed: 32803608
doi: 10.1007/s11356-020-10497-6
pii: 10.1007/s11356-020-10497-6
doi:

Substances chimiques

Herbicides 0
2,4-Dichlorophenoxyacetic Acid 2577AQ9262

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

45874-45882

Références

Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/s0076-6879(84)05016-3
Barja G (1999) Mitochondrial oxygen radical generation and leak: sites of production in states 4 and 3, organ specificity, and relation to aging and longevity. J Bioenerg Biomembr 31:347–366
doi: 10.1023/A:1005427919188
Barja G, Herrero A (1998) Localization at complex I and mechanism of the higher free radical production of brain nonsynaptic mitochondria in the short-lived rat than in the longevous pigeon. J Bioenerg Biomembr 30:235–243
doi: 10.1023/A:1020592719405
Bevilaqua F, Sachett A, Chitolina R, Garbinato C, Gasparetto H, Marcon M, Mocelin R, Dallegrave E, Conterato G, Piato A, Siebel AM (2020) A mixture of fipronil and fungicides induces alterations on behavioral and oxidative stress parameters in zebrafish. Ecotoxicology 29(2):140–147. https://doi.org/10.1007/s10646-019-02146-7
doi: 10.1007/s10646-019-02146-7
Bongiovanni B, De Lorenzi P, Ferri A, Konjuh C, Rassetto M, Evangelista de Duffard AM, Cardinali DP, Duffard R (2007) Melatonin decreases the oxidative stress produced by 2,4-dichlorophenoxyacetic acid in rat cerebellar granule cells. Neurotox Res 11:93–99
doi: 10.1007/BF03033388
Browne AM, Moore PA (2014) The effects of eublethal levels of 2,4-dichlorophenoxyacetic acid herbicide (2,4-D) on feeding behaviors of the crayfish O. rusticus. Arch Environ Contam Toxicol 67:234–244. https://doi.org/10.1007/s00244-014-0032-8
doi: 10.1007/s00244-014-0032-8
Brzezinski P, Gennis RB (2008) Cytochrome c oxidase: exciting progress and remaining mysteries. J Bioenerg Biomembr 40:521–531. https://doi.org/10.1007/s10863-008-9181-7
doi: 10.1007/s10863-008-9181-7
Buczyńska A, Szadkowska-Stańczyk I (2005) Identification of health hazards to rural population living near pesticide dump sites in Poland. Int J Occup Med Environ Health 18:331–339
Cheney MA, Fiorillo R, Criddle RS (1997) Herbicide and estrogen effects on the metabolic activity of Elliptio complanata measured by calorespirometry. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology 118:159–164. https://doi.org/10.1016/S0742-8413(97)00102-3
doi: 10.1016/S0742-8413(97)00102-3
de Arcaute C, Soloneski S, Larramendy ML (2016) Toxic and genotoxic effects of the 2,4-dichlorophenoxyacetic acid (2,4-D)-based herbicide on the Neotropical fish Cnesterodon decemmaculatus. Ecotoxicol Environ Saf 128:222–229. https://doi.org/10.1016/j.ecoenv.2016.02.027
doi: 10.1016/j.ecoenv.2016.02.027
Dehnert GK, Karasov WH, Wolman MA (2019) 2,4-Dichlorophenoxyacetic acid containing herbicide impairs essential visually guided behaviors of larval fish. Aquat Toxicol 209:1–12. https://doi.org/10.1016/j.aquatox.2019.01.015
doi: 10.1016/j.aquatox.2019.01.015
Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82(1):70–77.  https://doi.org/10.1016/0003-9861(59)90090-6
Ejomah AJ, Uyi OO, Ekaye S-O (2020) Exposure of the African mound building termite, Macrotermes bellicosus workers to commercially formulated 2,4-D and atrazine caused high mortality and impaired locomotor response. PLOS ONE 15:e0230664. https://doi.org/10.1371/journal.pone.0230664
doi: 10.1371/journal.pone.0230664
EPA (2005) Reregistration Eligibility Decision (RED) 2,4-D; EPA 738-R-05-002. U.S. Environmental Protection Agency, Office of Prevention, Pesticides and Toxic Substances, Office of Pesticide Programs, U.S. Government Printing Office, Washington, DC
Evangelista de Duffard AM, Brusco A, Duffard R, García G, Pecci Saavedra J (1995) Changes in serotonin-immunoreactivity in the dorsal and median raphe nuclei of rats exposed to 2,4-dichlorophenoxyacetic acid through lactation. Mol Chem Neuropathol 26:187–193
doi: 10.1007/BF02815012
Fridovich I (1995) Superoxide radical and superoxide dismutases. Ann Rev Biochem 64:97–112. https://doi.org/10.1146/annurev.bi.64.070195.000525
doi: 10.1146/annurev.bi.64.070195.000525
Gaaied S, Oliveira M, Le Bihanic F, Cachot J, Banni M (2019) Gene expression patterns and related enzymatic activities of detoxification and oxidative stress systems in zebrafish larvae exposed to the 2,4-dichlorophenoxyacetic acid herbicide. Chemosphere 224:289–297. https://doi.org/10.1016/j.chemosphere.2019.02.125
doi: 10.1016/j.chemosphere.2019.02.125
Garcia G, Tagliaferro P, Bortolozzi A, Madariaga MJ, Brusco A, Evangelista de Duffard AM, Duffard R, Pecci Saavedra J (2001) Morphological study of 5-T neurons and astroglial cells on brain of adult rats perinatal or chronically exposed to 2,4-dichlorophenoxyacetic acid. Neurotoxicology 22:733–741. https://doi.org/10.1016/S0161-813X(01)00059-6
doi: 10.1016/S0161-813X(01)00059-6
Halliwell B, Gutteridge JMC (2015) Free radicals in biology and medicine, 5th edn. Oxford University Press, Oxford
doi: 10.1093/acprof:oso/9780198717478.001.0001
Han D, Antunes F, Canali R, Rettori D, Cadenas E (2003) Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol. J Biol Chem 278:5557–5563. https://doi.org/10.1074/jbc.M210269200
doi: 10.1074/jbc.M210269200
Islam F, Wang J, Farooq MA, Khan MSS, Xu L, Zhu J, Zhao M, Muños S, Li QX, Zhou W (2018) Potential impact of the herbicide 2,4-dichlorophenoxyacetic acid on human and ecosystems. Environ Int 111:332–351. https://doi.org/10.1016/j.envint.2017.10.020
doi: 10.1016/j.envint.2017.10.020
Jones DP, Carlson JL, Mody VC, Cai J, Lynn MJ, Sternberg P (2000) Redox state of glutathione in human plasma. Free Radic Biol Med 28:625–635
doi: 10.1016/S0891-5849(99)00275-0
Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biology 8:e1000412. https://doi.org/10.1371/journal.pbio.1000412
doi: 10.1371/journal.pbio.1000412
Kysil EV, Meshalkina DA, Frick EE, Echevarria DJ, Rosemberg DB, Maximino C, Lima MG, Abreu MS, Giacomini AC, Barcellos LJG, Song C, Kalueff AV (2017) Comparative analyses of zebrafish anxiety-like behavior using conflict-based novelty tests. Zebrafish 14:197–208. https://doi.org/10.1089/zeb.2016.1415
doi: 10.1089/zeb.2016.1415
Latini A, da Silva CG, Ferreira GC, Schuck PF, Scussiato K, Sarkis JJ, Dutra Filho CS, Wyse ATS, Wannmacher CMD, Wajner M (2005) Mitochondrial energy metabolism is markedly impaired by d-2-hydroxyglutaric acid in rat tissues. Mol Genet Metab 86:188–199. https://doi.org/10.1016/j.ymgme.2005.05.002
doi: 10.1016/j.ymgme.2005.05.002
Leão MB, Gonçalves DF, Miranda GM, da Paixão GMX, Dalla Corte CL (2019) Toxicological evaluation of the herbicide Palace® in Drosophila melanogaster. J Toxicol Environ Health A 82:1172–1185. https://doi.org/10.1080/15287394.2019.1709109
doi: 10.1080/15287394.2019.1709109
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275
Marcon M, Herrmann AP, Mocelin R, Rambo CL, Koakoski G, Abreu MS, Conterato GMM, Kist LW, Bogo MR, Zanatta L, Barcellos LJG, Piato AL (2016) Prevention of unpredictable chronic stress-related phenomena in zebrafish exposed to bromazepam, fluoxetine and nortriptyline. Psychopharmacology 233:3815–3824. https://doi.org/10.1007/s00213-016-4408-5
doi: 10.1007/s00213-016-4408-5
Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247(10):3170–3175
Mocelin R, Herrmann AP, Marcon M, Rambo CL, Rohden A, Bevilaqua F, de Abreu MS, Zanatta L, Elisabetsky E, Barcellos LJG, Lara DR, Piato AL (2015) N-acetylcysteine prevents stress-induced anxiety behavior in zebrafish. Pharmacol Biochem Behav 139:121–126. https://doi.org/10.1016/j.pbb.2015.08.006
doi: 10.1016/j.pbb.2015.08.006
Nault ME, Netherland MD, Mikulyuk A, Skogerboe JG, Asplund T, Hauxwell J, Toshner P (2014) Efficacy, selectivity, and herbicide concentrations following a whole-lake 2,4-D application targeting Eurasian watermilfoil in two adjacent northern Wisconsin lakes. Lake Reserv Manag 30:1–10. https://doi.org/10.1080/10402381.2013.862586
doi: 10.1080/10402381.2013.862586
OECD (2019) TG 248: Xenopus eleutheroembryonic thyroid assay (XETA), OECD Guidelines for the testing of chemicals, Section 2. OECD. https://doi.org/10.1787/a13f80ee-en
Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–358.  https://doi.org/10.1016/0003-2697(79)90738-3
Özaslan MS, Demir Y, Aksoy M, Küfrevioğlu ÖI, Beydemir Ş (2018) Inhibition effects of pesticides on glutathione- S -transferase enzyme activity of Van Lake fish liver. J Biochem Mol Toxicol 32:e22196. https://doi.org/10.1002/jbt.22196
doi: 10.1002/jbt.22196
Pasandi MF, Shirazi FH, Gholami MR et al (2017) Epi/perineural and Schwann cells as well as perineural sheath integrity are affected following 2,4-D exposure. Neurotox Res 32:624–638. https://doi.org/10.1007/s12640-017-9777-y
doi: 10.1007/s12640-017-9777-y
Pompermaier A, Kirsten K, Soares SM, Fortuna M, Kalichak F, Idalencio R, Koakoski G, Barreto RE, Barcellos LJG (2020) Waterborne agrichemicals compromise the anti-predatory behavior of zebrafish. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-020-09862-2
Sachett A, Bevilaqua F, Chitolina R,  Garbinato C, Gasparetto H, Dal Magro J, Conterato GM, Siebel AM (2018) Ractopamine hydrochloride induces behavioral alterations and oxidative status imbalance in zebrafish. J Toxicol Environ Health A 81(7):194–201.  https://doi.org/10.1080/15287394.2018.1434848
Salla BGF, Bracht L, Parizotto VA, Comar JF, Peralta RM, Bracht F, Bracht A (2019) Kinetics of the metabolic effects, distribution spaces and lipid-bilayer affinities of the organo-chlorinated herbicides 2,4-D and picloram in the liver. Toxicol Lett 313:137–149. https://doi.org/10.1016/j.toxlet.2019.06.008
doi: 10.1016/j.toxlet.2019.06.008
Song Y (2014) Insight into the mode of action of 2,4-dichlorophenoxyacetic acid (2,4-D) as an herbicide: 2,4-D works as herbicide. J Integr Plant Biol 56:106–113. https://doi.org/10.1111/jipb.12131
doi: 10.1111/jipb.12131
Tagert MLM, Massey JH, Shaw DR (2014) Water quality survey of Mississippi’s Upper Pearl River. Sci Total Environ 481:564–573. https://doi.org/10.1016/j.scitotenv.2014.02.084
doi: 10.1016/j.scitotenv.2014.02.084
Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552:335–344. https://doi.org/10.1113/jphysiol.2003.049478
doi: 10.1113/jphysiol.2003.049478
Turrens JF, Boveris A (1980) Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem J 191:421–427. https://doi.org/10.1042/bj1910421
doi: 10.1042/bj1910421
World Health Organization (2017) Guidelines for drinking-water quality
Yoshikawa S, Muramoto K, Shinzawa-Itoh K, Aoyama H, Tsukihara T, Shimokata K, Katayama Y, Shimada H (2006) Proton pumping mechanism of bovine heart cytochrome c oxidase. Biochim Biophys Acta (BBA) - Bioenerg 1757:1110–1116. https://doi.org/10.1016/j.bbabio.2006.06.004
doi: 10.1016/j.bbabio.2006.06.004

Auteurs

Nathana Andressa Thiel (NA)

Laboratório de Genética e Ecotoxicologia Molecular, Programa de Pós-Graduação em Ciências Ambientais, Universidade Comunitária da Região de Chapecó, Servidão Anjo da Guarda, 295-D, Efapi, Chapecó, SC, 89809-900, Brazil.

Adrieli Sachett (A)

Laboratório de Psicofarmacologia e Comportamento, Programa de Pós-Graduação em Neurociências, Universidade Federal do Rio Grande do Sul, Sarmento Leite, 500, Centro Histórico, Porto Alegre, RS, 90050-170, Brazil.

Sabrina Ester Schneider (SE)

Laboratório de Genética e Ecotoxicologia Molecular, Curso de Ciências Biológicas, Universidade Comunitária da Região de Chapecó, Servidão Anjo da Guarda, 295-D, Efapi, Chapecó, SC, 89809-900, Brazil.

Cristiane Garbinato (C)

Laboratório de Genética e Ecotoxicologia Molecular, Programa de Pós-Graduação em Ciências Ambientais, Universidade Comunitária da Região de Chapecó, Servidão Anjo da Guarda, 295-D, Efapi, Chapecó, SC, 89809-900, Brazil.

Laura Decui (L)

Laboratório de Genética e Ecotoxicologia Molecular, Curso de Ciências Biológicas, Universidade Comunitária da Região de Chapecó, Servidão Anjo da Guarda, 295-D, Efapi, Chapecó, SC, 89809-900, Brazil.

Tuany Eichwald (T)

Laboratório de Bioenergética e Estresse Oxidativo, Departamento de Bioquímica, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina, Campus Universitário Trindade, Florianópolis, SC, 88040-900, Brazil.

Greicy M M Conterato (GMM)

Laboratório de Fisiologia da Reprodução Animal, Departamento de Agricultura, Biodiversidade e Floresta, Universidade Federal de Santa Catarina, Campus de Curitibanos, Rodovia Ulysses Gaboardi, Curitibanos, SC, 89520-000, Brazil.

Alexandra Latini (A)

Laboratório de Bioenergética e Estresse Oxidativo, Departamento de Bioquímica, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina, Campus Universitário Trindade, Florianópolis, SC, 88040-900, Brazil.

Angelo Piato (A)

Laboratório de Psicofarmacologia e Comportamento, Programa de Pós-Graduação em Neurociências, Universidade Federal do Rio Grande do Sul, Sarmento Leite, 500, Centro Histórico, Porto Alegre, RS, 90050-170, Brazil.

Anna Maria Siebel (AM)

Laboratório de Genética e Ecotoxicologia Molecular, Programa de Pós-Graduação em Ciências Ambientais, Universidade Comunitária da Região de Chapecó, Servidão Anjo da Guarda, 295-D, Efapi, Chapecó, SC, 89809-900, Brazil. anna.siebel@unochapeco.edu.br.
Laboratório de Genética e Ecotoxicologia Molecular, Curso de Ciências Biológicas, Universidade Comunitária da Região de Chapecó, Servidão Anjo da Guarda, 295-D, Efapi, Chapecó, SC, 89809-900, Brazil. anna.siebel@unochapeco.edu.br.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH