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Low Doses of Imidacloprid Induce Oxidative Stress and Neural Cell Disruption in Earthworm Eisenia fetida

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Abstract:

Imidacloprid is a widely used pesticide that belongs to the class of neonicotinoids. There is a piece of rising evidence that neonicotinoids exert cytotoxic effects in non-target organisms including vertebrate species such as mammals. Nevertheless, dose-limiting toxicity and molecular mechanisms of neonicotinoids' deleterious effects are still poorly understood. In accord to imidacloprid fate in the environment, the most of used pesticide is absorbed in the soil. Therefore, earthworms, which are prevailing soil organisms, could be considered as a target of neonicotinoids toxicity. The earthworm’s simple nervous system is a prospective model for neurotoxicological studies. We exposed earthworms to imidacloprid in a paper contact test with a doses range of 0.1‑0.4 µg/cm2 for 14 days. In the present work, we studied the imidacloprid effect on oxidative stress generation and neuronal marker neuron-specific enolase (NSE) expression. The exposure to imidacloprid induced a dose-dependent decrease in NSE. Both reactive oxygen species production and lipid peroxidation level were upregulated as well. Observed NSE decline suggests imidacloprid-caused disturbance in earthworm neuron cells. Obtained data have shown that relatively low doses of imidacloprid are potent to induce cytotoxicity in neurons. Furthermore, neurotoxicity could be recognized as one of an individual scenario of the general imidacloprid toxicity. Thus, presented results suggest the cytotoxicity of imidacloprid low doses in non-target organisms and hypothesize that NSE downregulation could be estimated as a biomarker of neonicotinoid cytotoxicity in a nervous system of non-insect species.

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Periodical:
International Letters of Natural Sciences (Volume 84)
Pages:
1-11
Citation:
A. Huslystyi et al., "Low Doses of Imidacloprid Induce Oxidative Stress and Neural Cell Disruption in Earthworm Eisenia fetida", International Letters of Natural Sciences, Vol. 84, pp. 1-11, 2021
Online since:
December 2021
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[1] E.E. Ewere et al., Uptake, depuration and sublethal effects of the neonicotinoid, imidacloprid, exposure in Sydney rock oysters, Chemosphere. 230 (2019) 1–13.

DOI: https://doi.org/10.1016/j.chemosphere.2019.05.045

[2] E.A.D. Mitchell et al., A worldwide survey of neonicotinoids in honey, Science (New York, N.Y.). 358(6359) (2017) 109–111.

[3] Ph. Wexler (Ed.) Encyclopedia of Toxicology, Academic Press, Elsevier Inc., (2014).

[4] I.Y. Abd-Elhakim et al., Imidacloprid impacts on neurobehavioral performance, oxidative stress, and apoptotic events in the brain of adolescent and adult rats, Journal of Agricultural and Food Chemistry. 66(51) (2018) 13513–13524.

DOI: https://doi.org/10.1021/acs.jafc.8b05793

[5] L. Donnarumma et al., Preliminary study on persistence in soil and residues in maize of imidacloprid, Journal of Environmental Science and Health, Part B. 46(6) (2011) 469–472.

[6] P. Wu et al., The imidacloprid remediation, soil fertility enhancement and microbial community change in soil by Rhodopseudomonas capsulata using effluent as carbon source, Environmental Pollution. 267 (2020) 114254.

DOI: https://doi.org/10.1016/j.envpol.2020.114254

[7] X. Wang et al., Multi-level ecotoxicological effects of imidacloprid on earthworm (Eisenia fetida), Chemosphere. 219 (2019) 923–932.

DOI: https://doi.org/10.1016/j.chemosphere.2018.12.001

[8] J.D. Knoepp et al., Imidacloprid movement in soils and impacts on soil microarthropods in southern Appalachian eastern hemlock stands, Journal of Environmental Quality. 41(2) (2012) 469–478.

DOI: https://doi.org/10.2134/jeq2011.0306

[9] T. Bhadauria, K.G. Saxena, Role of earthworms in soil fertility maintenance through the production of biogenic structures, Applied and Environmental Soil Science. 2010 (2009) 816073.

DOI: https://doi.org/10.1155/2010/816073

[10] W. Ge et al., Oxidative stress and DNA damage induced by imidacloprid in zebrafish (Danio rerio), Journal of Agricultural and Food Chemistry. 63(6) (2015) 1856–1862.

DOI: https://doi.org/10.1021/jf504895h

[11] N. Malhotra et al., Physiological effects of neonicotinoid insecticides on non-target aquatic animals – an updated review, International Journal of Molecular Sciences. 22(17) (2021) 9591.

[12] R. Miglani, S.S. Bisht, World of earthworms with pesticides and insecticides. Interdisciplinary Toxicology, 12(2) (2019) 71–82.

DOI: https://doi.org/10.2478/intox-2019-0008

[13] C. Pelosi et al., Pesticides and earthworms. A review, Agronomy for Sustainable Development. 34 (2014) 199–228.

[14] Q. Zhang, B. Zhang, C. Wang, Ecotoxicological effects on the earthworm Eisenia fetida following exposure to soil contaminated with imidacloprid, Environmental Science and Pollution Research International. 21(21) (2014) 12345–12353.

DOI: https://doi.org/10.1007/s11356-014-3178-z

[15] B. Bradford et al., Neonicotinoid-containing insecticide disruption of growth, locomotion, and fertility in Caenorhabditis elegans, PLoS One. 15(9) (2020) e0238637.

DOI: https://doi.org/10.1371/journal.pone.0238637

[16] D. Goulson, An overview of the environmental risks posed by neonicotinoid insecticides, Journal of Applied Ecology. 50(4) (2013) 977–987.

DOI: https://doi.org/10.1111/1365-2664.12111

[17] Y. Capowiez, A. Bérard, Assessment of the effects of imidacloprid on the behavior of two earthworm species (Aporrectodea nocturna and Allolobophora icterica) using 2D terraria, Ecotoxicology and Environmental Safety. 64(2) (2006) 198–206.

DOI: https://doi.org/10.1016/j.ecoenv.2005.02.013

[18] F. Chevillot et al., Selective bioaccumulation of neonicotinoids and sub-lethal effects in the earthworm Eisenia andrei exposed to environmental concentrations in an artificial soil, Chemosphere. 186 (2017) 839–847.

DOI: https://doi.org/10.1016/j.chemosphere.2017.08.046

[19] C. de Lima e Silva at al., Comparative toxicity of imidacloprid and thiacloprid to different species of soil invertebrates, Ecotoxicology. 26(4) (2017) 555–564.

DOI: https://doi.org/10.1007/s10646-017-1790-7

[20] C. de Lima e Silva at al., Toxicity in neonicotinoids to Folsima candida and Eisenia andrei, Environmental Toxicology and Chemistry. 39(3) (2020) 548–555.

DOI: https://doi.org/10.1002/etc.4634

[21] V.D. Dani et al., Comparison of metabolomic responses of earthworms to sub-lethal imidacloprid exposure in contact and soil tests, Environmental Science and Pollution Research International. 26(18) (2019) 18846–18855.

DOI: https://doi.org/10.1007/s11356-019-05302-y

[22] H. Zhang et al., Differences in kinetic metabolomics in Eisenia fetida under single and dual exposure of imidacloprid and dinotefuran at environmentally relevant concentrations, Journal of Hazardous Materials. 417 (2021) 126001.

DOI: https://doi.org/10.1016/j.jhazmat.2021.126001

[23] V.S. Nedzvetsky et al., Soluble curcumin ameliorates motility, adhesiveness and abrogate parthanatos in cadmium-exposed retinal pigment epithelial cells, Biosystems Diversity. 29(3) (2021) 235–243.

DOI: https://doi.org/10.15421/012129

[24] M. Rusz et al., Morpho‐metabotyping the oxidative stress response, Scientific Reports. 11 (2021) 15471.

[25] Y. Zang et al., Genotoxicity of two novel pesticides for the earthworm, Eisenia fetida, Environmental Pollution. 108(2) (2000) 271–278.

DOI: https://doi.org/10.1016/s0269-7491(99)00191-8

[26] T. Liu et al., Biochemical and genetic toxicity of dinotefuran on earthworms (Eisenia fetida). Chemosphere. 176 (2017) 156–164.

DOI: https://doi.org/10.1016/j.chemosphere.2017.02.113

[27] Y. Liu et al., Thiamethoxam exposure induces endoplasmic reticulum stress and affects ovarian function and oocyte development in mice, Journal of Agricultural and Food Chemistry. 69(6) (2021) 1942–(1952).

[28] M. Liu et al., From the cover: exposing imidacloprid interferes with neurogenesis through impacting on chick neural tube cell survival, Toxicological Sciences. 153(1) (2016) 137–148.

DOI: https://doi.org/10.1093/toxsci/kfw111

[29] R. Mesnage et al., Evaluation of neonicotinoid insecticides for oestrogenic, thyroidogenic and adipogenic activity reveals imidacloprid causes lipid accumulation, Journal of Applied Toxicology. 38(12) (2018) 1483–1491.

DOI: https://doi.org/10.1002/jat.3651

[30] V.S. Nedzvetsky et al., Low doses of imidacloprid induce disruption of intercellular adhesion and initiate proinflammatory changes in Caco-2 cells, Regulatory Mechanisms in Biosystems. 12(3) (2021) 430–437.

DOI: https://doi.org/10.15421/022159

[31] J. Kim et al., Imidacloprid, a neonicotinoid insecticide, induces insulin resistance, The Journal of Toxicological Sciences. 38(5) (2013) 655–660.

DOI: https://doi.org/10.2131/jts.38.655

[32] M. Abou-Donia et al., Imidacloprid induces neurobehavioral deficits and increases expression of glial fibrillary acidic protein in the motor cortex and hippocampus in offspring rats following in utero exposure, Journal of Toxicology and Environmental Health, Part A. 71(2) (2008) 119–130.

DOI: https://doi.org/10.1080/15287390701613140

[33] S.M. Rawi, A.S. Al-Logmani, R.Z. Hamza, Neurological alterations induced by formulated imidacloprid toxicity in Japanese quails, Metabolic Brain Disease. 34(2) (2019) 443–450.

DOI: https://doi.org/10.1007/s11011-018-0377-1

[34] V.Ya. Gasso et al., Biomarkers of the influence of pyrethroids and neonicotinoids on amphibian larvae, Ecology and Noospherology. 31(1) (2020) 46–51.

DOI: https://doi.org/10.15421/032007

[35] V.Y. Gasso et al., Local industrial pollution induces astrocyte cytoskeleton rearrangement in the dice snake brain: GFAP as a biomarker, Biosystems Diversity. 28(3) (2020) 250–256.

DOI: https://doi.org/10.15421/012033

[36] M. Kirici et al., Sublethal doses of copper sulphate initiate deregulation of glial cytoskeleton, NF-kappa B and PARP expression in Capoeta umbla brain tissue, Regulatory Mechanisms in Biosystems. 10(1) (2019) 103–110.

DOI: https://doi.org/10.15421/021916

[37] V.S. Nedzvetsky et al., Influence of the insecticide λ-cyhalothrin on oxidative stress and expression of replicative protein A in the brain of fish, Agrology. 3(4) 2020 214–218.

DOI: https://doi.org/10.32819/020025

[38] R. Cliff et al., Effect of diesel exhaust inhalation on blood markers of inflammation and neurotoxicity: a controlled, blinded crossover study, Inhalation Toxicology. 28(3) (2016) 145–153.

DOI: https://doi.org/10.3109/08958378.2016.1145770

[39] A. Ramirez-Celis et al., Peptides of neuron specific enolase as potential ASD biomarkers: from discovery to epitope mapping, Brain, Behavior, and Immunity. 84 (2020) 200–208.

DOI: https://doi.org/10.1016/j.bbi.2019.12.002

[40] M.A. Isgrò, P. Bottoni, R. Scatena, Neuron-specific enolase as a biomarker: biochemical and clinical aspects, Advances in Experimental Medicine and Biology. 867 (2015) 125–143.

DOI: https://doi.org/10.1007/978-94-017-7215-0_9

[41] M.Z. Jeddi et al., Towards a systematic use of effect biomarkers in population and occupational biomonitoring, Environment International. 146 (2021) 106257.

[42] V.B. Archibong et al., The effect of codeine administration on oxidative stress biomarkers and the expression of the neuron-specific enolase in the brain of Wistar rats, Naunyn-Schmiedeberg's Archives of Pharmacology. 394(8) (2021) 1665–1673.

DOI: https://doi.org/10.1007/s00210-021-02094-2

[43] OECD, Test No. 207: Earthworm, Acute Toxicity Tests, OECD Guidelines for the Testing of Chemicals, Section 2, OECD Publishing, Paris, (1984).

DOI: https://doi.org/10.1787/9789264070042-en

[44] H. Ohkawa, N. Ohishi, K. Yagi, Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction, Analytical Biochemistry. 95(2) (1979) 351–358.

DOI: https://doi.org/10.1016/0003-2697(79)90738-3

[45] T.S. Hnasko, R.M. Hnasko, The Western blot, Methods in Molecular Biology. 1318 (2015) 87–96.

DOI: https://doi.org/10.1007/978-1-4939-2742-5_9

[46] J. Wang et al., DNA damage and oxidative stress induced by imidacloprid exposure in the earthworm Eisenia fetida, Chemosphere. 144 (2016) 510–517.

DOI: https://doi.org/10.1016/j.chemosphere.2015.09.004
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