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Research Articles

Pre-imaginal exposure to mancozeb induces morphological and behavioral deficits and oxidative damage in Drosophila melanogaster

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Pages 575-587 | Received 14 Oct 2021, Accepted 19 Mar 2022, Published online: 02 May 2022

References

  • Aebi, H., 1984. Catalase in vitro. Methods in Enzymology, 105, 121–126.
  • Algarve, T.D., et al., 2018. Parental and preimaginal exposure to methylmercury disrupts locomotor activity and circadian rhythm of adult Drosophila melanogaster. Drug and Chemical Toxicology, 22, 1–11.
  • Bendavit, G., et al., 2016. Nrf2 transcription factor can directly regulate mTOR: linking cytoprotective gene expression to a major metabolic regulator that generates redox activity. The Journal of Biological Chemistry, 291 (49), 25476–25488.
  • Biagini, G., Sala, D., and Zini, I., 1995. Diethyldithiocarbamate, a superoxide dismutase inhibitor, counteracts the maturation of ischemic-like lesions caused by endothelin-1 intrastriatal injection. Neuroscience Letters, 190 (3), 212–216.
  • Bland, N.D., et al., 2009. Locomotor and geotactic behavior of Drosophila melanogaster over-expressing neprilysin 2. Peptides, 30 (3), 571–574.
  • Bouabid, S., et al., 2014. Manganese-induced atypical parkinsonism is associated with altered Basal Ganglia activity and changes in tissue levels of monoamines in the rat. PLoS One, 9 (6), e98952.
  • Bradford, M.M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.
  • Broughton, S.J., et al., 2005. Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proceedings of the National Academy of Sciences of the United States of America, 102 (8), 3105–3110.
  • Bushey, D., et al., 2010. Sleep, aging, and lifespan in Drosophila. B.M.C. Neuroscience, 11 (56).doi:10.1186/1471-2202-11-56
  • Calviello, G., et al., 2006. D.N.A. damage and apoptosis induction by the pesticide Mancozeb in rat cells: involvement of the oxidative mechanism. Toxicology and Applied Pharmacology, 211 (2), 87–96.
  • Carvalho, N.R., et al., 2017. Eugenia uniflora leaf essential oil promotes mitochondrial dysfunction in Drosophila melanogaster through the inhibition of oxidative phosphorylation. Toxicology Research, 6 (4), 526–534.
  • Castro, V.L., et al., 1999. Cytogenetic and teratological effects of mancozeb pre natal exposure on rats. Brazilian Archives of Biology and Technology, 42 (2). doi:10.1590/S1516-89131999000200001
  • Costa-Silva, D.G., et al., 2018. Mancozeb exposure results in manganese accumulation and Nrf2-related antioxidant responses in the brain of common carp Cyprinus carpio. Environmental Science and Pollution Research International, 25 (16), 15529–15540.
  • Davies, K.J.A., 2000. Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems. IUBMB Life, 50 (4-5), 279–289.
  • Deardfield, K.L., 1994. Ethylene thiourea (ETU): a review of the genetic toxicity studies. Mutation Research, 317, 111–132.
  • Dibble, C.C., and Cantley, L.C., 2015. Regulation of mTORC1 by P13K signaling. Trends in Cell Biology., 25 (9), 545–555.
  • Donkena, K.V., Young, C.Y., and Tindall, D.J., 2010. Oxidative stress and DNA methylation in prostate cancer. Obstetrics and Gynecology International, 2010, 302051.
  • Fitsanakis, V.A., et al., 2002. Catalysis of catechol oxidation by metal-dithiocarbamate complexes in pesticides. Free Radical Biology & Medicine, 33 (12), 1714–1723.
  • Frank, M.G., and Heller, H.C., 2019. The function(s) of sleep. Handbook of Experimental Pharmacology, 253, 3–34.
  • Fuhriman, S., et al., 2022. Recent pesticide exposure affects sleep: a cross-sectional study among smallholder farmers in Uganda. Environment International, 158, 106878.
  • Gilestro, G.F., and Cirelli, C., 2009. PySolo: a complete suite for sleep analysis in Drosophila. Bioinformatics (Oxford, England), 25 (11), 1466–1467.
  • Gnaiger, E., 2009. Capacity of oxidative phosphorylation in human skeletal muscle: new perspectives of mitochondrial physiology. The International Journal of Biochemistry & Cell Biology, 41 (10), 1837–1845.
  • Goldner, W.S., et al., 2010. Pesticide use and thyroid disease among women in the agricultural health study. American Journal of Epidemiology, 171 (4), 455–464.
  • Goldoni, A., and da Silva, L.B., 2012. Mutagenic potential of the fungicide mancozeb in Astyanax jacuhiensis (Teleostei: Characidae). ResearchGate, 28, 297–301.
  • Gullino, M.L., et al., 2010. Mancozeb: past, present, and future. Plant Disease, 94 (9), 1076–1087.
  • Habig, W.H., and Jakoby, W.B., 1981. Assays for differentiation of glutathione S transferases. Methods in Enzymology, 77, 398–405.
  • Harrison Brody, A., et al., 2013. Mancozeb-induced behavioral deficits precede structural neural degeneration. Neurotoxicology, 34, 74–81.
  • Hissin, P.J., and Hilf, R., 1976. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Analytical Biochemistry, 74 (1), 214–226.
  • Hogarth, G., 2012. Metal-dithiocarbamate complexes: chemistry and biological activity. Mini Reviews in Medicinal Chemistry, 12 (12), 1202–1215.
  • Iorio, R., et al., 2015. Mancozeb affects mitochondrial activity, redox status and ATP production in mouse granulosa cells. Toxicology in Vitro: An International Journal Published in Association with BIBRA, 30 (1 Pt B), 438–445.
  • Klotz, L.O., et al., 2015. Redox regulation of FoxO transcription factors. Redox Biology, 6, 51–72.
  • Kohyama-Koganeya, A., and Hirabayashi, Y., 2010. The Drosophila 7-pass transmembrane glycoprotein boss and metabolic regulation: what Drosophila can teach us about human energy metabolism. Methods in Enzymology, 480, 525–538.
  • Kostyuk, V.A., and Potapovich, A.I., 1989. Superoxide–driven oxidation of quercetin and a simple sensitive assay for determination of superoxide dismutase. Biochemistry International, 19 (5), 1117–1124.
  • Macedo, G.E., et al., 2017. Senecio brasiliensis impairs eclosion rate and induces apoptotic cell death in larvae of Drosophila melanogaster. Comparative Biochemistry and Physiology. Toxicology & Pharmacology: CBP, 198, 45–67.
  • Navarro-Yepes, J., et al., 2014. Oxidative stress, redox signaling, and autophagy: cell death versus survival. Antioxidants & Redox Signaling, 21 (1), 66–85.
  • Negga, R., et al., 2011. Exposure to Mn/Zn ethylene-bis-dithiocarbamate and glyphosate pesticides leads to neurodegeneration in Caenorhabditis elegans. NeuroToxicology, 32 (3), 331–341.
  • Nordby, K.C., et al., 2005. Indicators of Mancozeb exposure in relation to thyroid cancer and neural tube defects in farmers’ families. Scandinavian Journal of Work, Environment & Health, 31 (2), 89–96.
  • Baumert, B.O., et al., 2018. Sleep apnea and pesticide exposure in a study of U.S. farmers. Sleep Health, 4 (1), 20–26.
  • O’Brien, J., et al., 2000. Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. European Journal of Biochemistry, 267 (17), 5421–5426.
  • Ohkawa, H., Ohishi, N., and Yagi, K., 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry, 95 (2), 351–358.
  • Ijomone, O.M., et al., 2020. Epigenetic influence of environmentally neurotoxic metals. Neurotoxicology, 81, 51–65.
  • Paula, M.T., et al., 2014. Effects of Hg(II) exposure on MAPK phosphorylation and antioxidant system in D. melanogaster. Environmental Toxicology, 29 (6), 621–630.
  • Pérez-Severiano, F., et al., 2004. S-Allylcysteine, a garlic-derived antioxidant, ameliorates quinolinic acid-induced neurotoxicity and oxidative damage in rats. Neurochemistry International, 45 (8), 1175–1183.
  • Phom, L., et al., 2014. Curcumin’s neuroprotective efficacy in Drosophila model of idiopathic Parkinson’s disease is phase specific: implication of its therapeutic effectiveness. Rejuvenation Research, 17 (6), 481–489.
  • Rodrigues, N.R., et al., 2018. Short-term sleep deprivation with exposure to nocturnal light alters mitochondrial bioenergetics in Drosophila. Free Radical Biology & Medicine, 120, 395–406.
  • Román, G.C., 2007. Autism: transient in utero hypothyroxinemia related to maternal flavonoid ingestion during pregnancy and to other environmental antithyroid agents. Journal of the Neurological Sciences, 262 (1-2), 15–26.
  • Roussel, B., and Renaud, B., 1977. Effect of chronic manganese intoxication on the sleep wake cycle in the rat. Neuroscience Letters, 4 (1), 55–60.
  • Saraiva, M.A., et al., 2018. Exposure of Drosophila melanogaster to Mancozeb induces oxidative damage and modulates Nrf2 and HSP70/83. Oxidative Medicine and Cellular Longevity, 2018, 5456911–5456928.
  • Saraiva, M.A., et al., 2021. Mancozeb impairs mitochondri and bioenergetic activity in Drosophila melanogaster. Heliyon, 7 (1), e06007.
  • Sehgal, A., et al., 2007. Molecular analysis of sleep:wake cycles in Drosophila. Cold Spring Harbor Symposia on Quantitative Biology, LXXII, 557–564.
  • Sehgal, A., and Mignot, E., 2011. Genetics of sleep and sleep disorders. Cell, 146 (2), 120–194.
  • Sha, J.Y., et al., 2019. Maltol (3-hydroxy-2-methyl-4-pyrone) slows D-galactose-induced brain aging process by damping the Nrf2/HO-1 meditated oxidative stress in mice. Journal of Agricultural and Food Chemistry, 67 (37), 10342–10351.
  • Srivastava, A.K., et al., 2012. Mancozeb-induced genotoxicity and apoptosis in cultured human lymphocytes. Life Sciences, 90 (21-22), 815–824.
  • Sun, J., et al., 2018. Neural control of startle-induced locomotion by the mushroom bodies and associated neurons in Drosophila. Frontiers in Systems Neuroscience, 12, article–articl6.
  • Ternes, A.P., et al., 2014. Drosophila melanogaster – an embryonic model for studying behavioral and biochemical effects of manganese exposure. EXCLI Journal, 21, 1239–1253.
  • Todt, C.E., et al., 2016. Acute exposure to a Mn/Zn ethylene-bis-dithiocarbamate fungicide leads to mitochondrial dysfunction and increased reactive oxygen species production in Caenorhabditis elegans. NeuroToxicology, 57, 112–120.
  • United States Environmental Protection Agency, 2005. Reregistration eligibility decision for Mancozeb. List B Case No. 0643, E.P.A. 738-R-04-012. Available from: http://www.epa.gov/oppsrrd1/REDs/mancozeb_red.pdf [Accessed 5 September 2018].
  • Uttara, B., et al., 2009. Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Current Neuropharmacology, 7 (1), 65–74.
  • Valko, M., et al., 2006. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chemico-Biological Interactions, 160 (1), 1–40.
  • Wang, L., et al., 2013. Aberration in epigenetic gene regulation in hippocampal neurogenesis by developmental exposure to manganese chloride in mice. Toxicological Sciences: An Official Journal of the Society of Toxicology, 136 (1), 154–165.
  • Yasugi, T., Yamada, T., and Nishimura, T., 2017. Adaptation to dietary conditions by trehalose metabolism in Drosophila. Scientific Reports, 7, 2–10.
  • Zhang, J., et al., 2003. Manganese ethylene-bis-dithiocarbamate and selective dopaminergic neurodegeneration in rat: a link through mitochondrial dysfunction. Journal of Neurochemistry, 84 (2), 336–346.
  • Zhang, Z., et al., 2017. Role of histone acetylation in activation of  nuclear factor erythroid 2-related factor 2/heme oxygenase 1 pathway by manganese chloride. Toxicology and Applied Pharmacology, 336, 94–100.
  • Zhou, Y., et al., 2004. Proteasomal inhibition induced by manganese ethylene-bis-dithiocarbamate: relevance to Parkinson’s disease. Neuroscience, 128 (2), 281–291.

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