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Research Article

The antioxidant and neuroprotective effects of melatonin on glyphosate-based herbicide-induced affective and cognitive impairments in rats

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Pages 354-366 | Received 19 Feb 2024, Accepted 20 Apr 2024, Published online: 01 May 2024

References

  • Myers JP, Antoniou MN, Blumberg B, et al. Concerns over use of glyphosate-based herbicides and risks associated with exposures: a consensus statement. Environ Health Glob Access Sci Source. 2016;15(1):19. doi: 10.1186/s12940-016-0117-0
  • Battaglin WA, Meyer MT, Kuivila KM, et al. Glyphosate and its degradation product AMPA occur frequently and widely in U.S. Soils, surface water, groundwater, and precipitation. JAWRA J Am Water Resour Assoc. 2014;50(2):275–290. doi: 10.1111/jawr.12159
  • Brewster DW, Warren J, Hopkins WE. Metabolism of glyphosate in Sprague-Dawley rats: tissue distribution, identification, and quantitation of glyphosate-derived materials following a single oral dose. Toxicol Sci. 1991;17(1):43–51. doi: 10.1093/toxsci/17.1.43
  • Anadón A, Martínez-Larrañaga MR, Martínez MA, et al. Toxicokinetics of glyphosate and its metabolite aminomethyl phosphonic acid in rats. Toxicol Lett. 2009;190(1):91–95. doi: 10.1016/j.toxlet.2009.07.008
  • Benachour N, Sipahutar H, Moslemi S, et al. Time- and dose-dependent effects of roundup on human embryonic and placental cells. Arch Environ Contam Toxicol. 2007;53(1):126–133. doi: 10.1007/s00244-006-0154-8
  • Wang G, Fan X-N, Tan Y-Y, et al. Parkinsonism after chronic occupational exposure to glyphosate. Parkinsonism Relat Disord. 2011;17(6):486–487. doi: 10.1016/j.parkreldis.2011.02.003
  • Davoren MJ, Schiestl RH. Glyphosate-based herbicides and cancer risk: a post-IARC decision review of potential mechanisms, policy and avenues of research. Carcinogenesis. 2018;39(10):1207–1215. doi: 10.1093/carcin/bgy105
  • Martínez M-A, Ares I, Rodríguez J-L, et al. Neurotransmitter changes in rat brain regions following glyphosate exposure. Environ Res. 2018;161:212–219. doi: 10.1016/j.envres.2017.10.051
  • Mostafalou S, Abdollahi M. The link of organophosphorus pesticides with neurodegenerative and neurodevelopmental diseases based on evidence and mechanisms. Toxicology. 2018;409:44–52. doi: 10.1016/j.tox.2018.07.014
  • Pu Y, Yang J, Chang L, et al. Maternal glyphosate exposure causes autism-like behaviors in offspring through increased expression of soluble epoxide hydrolase. Proc Natl Acad Sci. 2020;117(21):11753–11759. doi: 10.1073/pnas.1922287117
  • Cattani D, Cesconetto PA, Tavares MK, et al. Developmental exposure to glyphosate-based herbicide and depressive-like behavior in adult offspring: implication of glutamate excitotoxicity and oxidative stress. Toxicology. 2017;387:67–80. doi: 10.1016/j.tox.2017.06.001
  • Baier CJ, Gallegos CE, Raisman-Vozari R, et al. Behavioral impairments following repeated intranasal glyphosate-based herbicide administration in mice. Neurotoxicol Teratol. 2017;64:63–72. doi: 10.1016/j.ntt.2017.10.004
  • Ait-Bali Y, Ba-M’hamed S, Gambarotta G, et al. Pre- and postnatal exposure to glyphosate-based herbicide causes behavioral and cognitive impairments in adult mice: evidence of cortical ad hippocampal dysfunction. Arch Toxicol. 2020;94(5):1703–1723. doi: 10.1007/s00204-020-02677-7
  • Rueda-Ruzafa L, Cruz F, Roman P, et al. Gut microbiota and neurological effects of glyphosate. Neurotoxicology. 2019;75:1–8. doi: 10.1016/j.neuro.2019.08.006
  • Winstone JK, Pathak KV, Winslow W, et al. Glyphosate infiltrates the brain and increases pro-inflammatory cytokine TNFα: implications for neurodegenerative disorders. J Neuroinflammation. 2022;19(1):193. doi: 10.1186/s12974-022-02544-5
  • Naïla N, Makthar W, Lamtai M, et al. Effect of intra-hippocampal lead injection on affective and cognitive disorders in male WISTAR rats: possible involvement of oxidative stress. E3S Web Conf. 2021;319:02017. doi: 10.1051/e3sconf/202131902017
  • El Brouzi MY, Lamtai M, Zghari O, et al. Intrahippocampal effects of nickel injection on the affective and cognitive response in Wistar rat: potential role of oxidative stress. Biol Trace Elem Res. 2021;199(9):3382–3392. doi: 10.1007/s12011-020-02457-5
  • Zghari O, Lamtai M, Azirar S, et al. Neuroprotective effects of melatonin against neurotoxicity induced by intrahippocampal injection of aluminum in male Wistar rats: possible involvement of oxidative stress pathway. Adv Anim Vet Sci. 2023;11. doi: 10.17582/journal.aavs/2023/11.5.711.719
  • Zghari O, Azirar S, Lamtai M, et al. Intrahippocampal dose-dependent effects of aluminum injection on affective and cognitive response in male Wistar rat: potential role of oxidative stress. Egypt J Basic Appl Sci. 2023;10(1):460–475. doi: 10.1080/2314808X.2023.2229623
  • Lamtai M, Ouakki S, Zghari O, et al. Neuroprotective effect of melatonin on nickel-induced affective and cognitive disorders and oxidative damage in rats. Environ Anal Health Toxicol. 2020;35(4):e2020025. doi: 10.5620/eaht.2020025
  • Rehman SU, Ikram M, Ullah N, et al. Neurological enhancement effects of melatonin against brain injury-induced oxidative stress, neuroinflammation, and neurodegeneration via AMPK/CREB signaling. Cells. 2019;8(7):760. doi: 10.3390/cells8070760
  • Mahmood D, Muhammad BY, Albdulghani M, et al. Corrigendum to “advancing role of melatonin in the treatment of neuropsychiatric disorders”. Egypt J Basic Appl Sci. 2016;3(4):398–398. doi: 10.1016/j.ejbas.2016.08.005
  • Ouakki S, El Mrabet FZ, El Hessni A, et al. Conversion of L-Tryptophan into melatonin is the possible action pathway involved in the effect of L-Tryptophan on antidepressant-related behavior in female rats: analysis of the influence of treatment duration. J Behav Brain Sci. 2013;3(4):362–372. doi: 10.4236/jbbs.2013.34036
  • El Mrabet FZ, Lagbouri I, Mesfioui A, et al. The influence of Gonadectomy on anxiolytic and antidepressant effects of melatonin in male and female Wistar rats: a possible implication of sex hormones. NM. 2012;3(2):162–173. doi: 10.4236/nm.2012.32021
  • Kocic G, Tomovic K, Kocic H, et al. Antioxidative, membrane protective and antiapoptotic effects of melatonin, in silico study of physico-chemical profile and efficiency of nanoliposome delivery compared to betaine. RSC Adv. 2017;7(3):1271–1281. doi: 10.1039/C6RA24741E
  • Rodriguez C, Mayo JC, Sainz RM, et al. Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res. 2004;36(1):1–9. doi: 10.1046/j.1600-079X.2003.00092.x
  • Picut CA, Ziejewski MK, Stanislaus D. Comparative aspects of pre‐ and postnatal development of the male reproductive system. Birth Defects Res. 2018;110(3):190–227. doi: 10.1002/bdr2.1133
  • Williams GM, Kroes R, Munro IC. Safety evaluation and risk assessment of the herbicide roundup and its active ingredient, glyphosate, for humans. Regul Toxicol Pharmacol. 2000;31(2):117–165. doi: 10.1006/rtph.1999.1371
  • Durand M, Berton O, Aguerre S, et al. Effects of repeated fluoxetine on anxiety-related behaviours, central serotonergic systems, and the corticotropic axis in SHR and WKY rats. Neuropharmacology. 1999;38(6):893–907. doi: 10.1016/S0028-3908(99)00009-X
  • Pellow S, Chopin P, File SE, et al. Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods. 1985;14(3):149–167. doi: 10.1016/0165-0270(85)90031-7
  • Roger DP. Animal models of depression: utility for transgenic research. Rev Neurosci. 2000;11(1):53–58. doi: 10.1515/REVNEURO.2000.11.1.53
  • Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods. 1984;11(1):47–60. doi: 10.1016/0165-0270(84)90007-4
  • Chao CC, Hu S, Molitor TW, et al. Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J Immunol. 1992;149(8):2736–2741. doi: 10.4049/jimmunol.149.8.2736
  • Draper HH, Hadley M. Malondialdehyde determination as index of lipid peroxidation. In: Methods in Enzymology. Elsevier; 1990. p. 421–431. doi: 10.1016/0076-6879(90)86135-I
  • Aebi H. Catalase in vitro. In: Oxygen radicals in biological systems. Academic Press; 1984. p. 121–126. doi: 10.1016/S0076-6879(84)05016-3
  • Bicca DF, Spiazzi CC, Ramalho JB, et al. A subchronic low-dose exposure of a glyphosate-based herbicide induces depressive and anxious-like behavior in mice: quercetin therapeutic approach. Environ Sci Pollut Res. 2021;28(47):67394–67403. doi: 10.1007/s11356-021-15402-3
  • Bali YA, Kaikai N, S B-M, et al. Learning and memory impairments associated to acetylcholinesterase inhibition and oxidative stress following glyphosate based-herbicide exposure in mice. Toxicology. 2019;415:18–25. doi: 10.1016/j.tox.2019.01.010
  • Luna S, Neila LP, Vena R, et al. Glyphosate exposure induces synaptic impairment in hippocampal neurons and cognitive deficits in developing rats. Arch Toxicol. 2021;95(6):2137–2150. doi: 10.1007/s00204-021-03046-8
  • Cattani D, Liz Oliveira Cavalli VL D, Heinz Rieg CE, et al. Mechanisms underlying the neurotoxicity induced by glyphosate-based herbicide in immature rat hippocampus: involvement of glutamate excitotoxicity. Toxicology. 2014;320:34–45. doi: 10.1016/j.tox.2014.03.001
  • Turkmen R, Birdane YO, Demirel HH, et al. Protective effects of resveratrol on biomarkers of oxidative stress, biochemical and histopathological changes induced by sub-chronic oral glyphosate-based herbicide in rats. Toxicol Res. 2019;8(2):238–245. doi: 10.1039/C8TX00287H
  • Szepanowski F, Szepanowski L-P, Mausberg AK, et al. Differential impact of pure glyphosate and glyphosate-based herbicide in a model of peripheral nervous system myelination. Acta Neuropathol (Berl). 2018;136(6):979–982. doi: 10.1007/s00401-018-1938-4
  • Gallegos CE, Bartos M, Gumilar F, et al. Intranasal glyphosate-based herbicide administration alters the redox balance and the cholinergic system in the mouse brain. Neurotoxicology. 2020;77:205–215. doi: 10.1016/j.neuro.2020.01.007
  • Astiz M, MJTD A, Marra CA. Effect of pesticides on cell survival in liver and brain rat tissues. Ecotoxicol Environ Saf. 2009;72(7):2025–2032. doi: 10.1016/j.ecoenv.2009.05.001
  • Castagnola E, Robbins EM, Woeppel KM, et al. Real-time fast scan cyclic voltammetry detection and quantification of exogenously administered melatonin in mice brain. Front Bioeng Biotechnol. 2020;8:602216. doi: 10.3389/fbioe.2020.602216
  • Kopustinskiene DM, Bernatoniene J. Molecular mechanisms of melatonin-mediated cell protection and signaling in health and disease. Pharmaceutics. 2021;13(2):129. doi: 10.3390/pharmaceutics13020129
  • Ahmadi Z, Ashrafizadeh M. Melatonin as a potential modulator of Nrf2. Fundam Clin Pharmacol. 2020;34(1):11–19. doi: 10.1111/fcp.12498
  • Sadek KM, Lebda MA, Abouzed TK. The possible neuroprotective effects of melatonin in aluminum chloride-induced neurotoxicity via antioxidant pathway and Nrf2 signaling apart from metal chelation. Environ Sci Pollut Res. 2019;26(9):9174–9183. doi: 10.1007/s11356-019-04430-9
  • Cattani D, Pierozan P, Zamoner A, et al. Long-term effects of perinatal exposure to a glyphosate-based herbicide on melatonin levels and oxidative brain damage in adult male rats. Antioxidants. 2023;12(10):1825. doi: 10.3390/antiox12101825