Mechanisms of oxidative stress in methylmercury-induced neurodevelopmental toxicity

NeuroToxicology - Tập 85 - Trang 33-46 - 2021
Xiaoyang Li1, Jingjing Pan1, Yanfeng Wei1, Linlin Ni1, Bin Xu1, Yu Deng1, Tianyao Yang1, Wei Liu1
1Department of Environmental Health, School of Public Health, China Medical University, Shenyang, China

Tài liệu tham khảo

Al Osman, 2019, Exposure routes and health effects of heavy metals on children, Biometals, 32, 563, 10.1007/s10534-019-00193-5 Alexandrov, 2018, Synergism in aluminum and mercury neurotoxicity, Integr. Food Nutr. Metab., 5 Ali, 2018, Natural dietary supplementation of anthocyanins via pi3k/akt/nrf2/ho-1 pathways mitigate oxidative stress, neurodegeneration, and memory impairment in a mouse model of alzheimer’s disease, Mol. Neurobiol., 55, 6076, 10.1007/s12035-017-0798-6 Al-Osaimi, 2018, Therapeutic and protective potency of bee pollen against neurotoxic effects induced by prenatal exposure of rats to methyl mercury, J. Mol. Neurosci., 65, 327, 10.1007/s12031-018-1107-1 Al-Saleh, 2016, Alterations in biochemical markers due to mercury (hg) exposure and its influence on infant’s neurodevelopment, Int. J. Hyg. Environ. Health, 219, 898, 10.1016/j.ijheh.2016.07.002 Antunes Dos Santos, 2018, Oxidative stress in methylmercury-induced cell toxicity, Toxics, 6 Aschner, 2007, Involvement of glutamate and reactive oxygen species in methylmercury neurotoxicity, Braz. J. Med. Biol. Res., 40, 285, 10.1590/S0100-879X2007000300001 Bakir, 1973, Methylmercury poisoning in iraq, Science, 181, 230, 10.1126/science.181.4096.230 Baraldi, 2002, Cognitive deficits and changes in gene expression of nmda receptors after prenatal methylmercury exposure, Environ. Health Perspect., 110, 855, 10.1289/ehp.02110s5855 Ben Bacha, 2020, The therapeutic and protective effects of bee pollen against prenatal methylmercury induced neurotoxicity in rat pups, Metab. Brain Dis., 35, 215, 10.1007/s11011-019-00496-z Berezovska, 1999, Notch1 inhibits neurite outgrowth in postmitotic primary neurons, Neuroscience, 93, 433, 10.1016/S0306-4522(99)00157-8 Bjørklund, 2017, The toxicology of mercury: current research and emerging trends, Environ. Res., 159, 545, 10.1016/j.envres.2017.08.051 Björklund, 2007, The effects of methylmercury on motor activity are sex- and age-dependent, and modulated by genetic deletion of adenosine receptors and caffeine administration, Toxicology, 241, 119, 10.1016/j.tox.2007.08.092 Black, 2011, Modulation of the effects of methylmercury on rat neurodevelopment by co-exposure with labrador tea (rhododendron tomentosum ssp. Subarcticum), Food Chem. Toxicol., 49, 2336, 10.1016/j.fct.2011.06.035 Bland, 2006, Methylmercury induces activation of notch signaling, Neurotoxicology, 27, 982, 10.1016/j.neuro.2006.04.005 Bose, 2012, Inherited effects of low-dose exposure to methylmercury in neural stem cells, Toxicol. Sci., 130, 383, 10.1093/toxsci/kfs257 Boucher, 2012, Prenatal methylmercury, postnatal lead exposure, and evidence of attention deficit/hyperactivity disorder among inuit children in arctic quebec, Environ. Health Perspect., 120, 1456, 10.1289/ehp.1204976 Branco, 2017, Biomarkers of mercury toxicity: past, present, and future trends, J. Toxicol. Environ. Health B Crit. Rev., 20, 119, 10.1080/10937404.2017.1289834 Bridges, 2017, Mechanisms involved in the transport of mercuric ions in target tissues, Arch. Toxicol., 91, 63, 10.1007/s00204-016-1803-y Caballero, 2017, Methylmercury-induced developmental toxicity is associated with oxidative stress and cofilin phosphorylation. Cellular and human studies, Neurotoxicology, 59, 197, 10.1016/j.neuro.2016.05.018 Cambier, 2018, A likely placental barrier against methylmercury in pregnant rats exposed to fish-containing diets, Food Chem. Toxicol., 122, 11, 10.1016/j.fct.2018.09.066 Carratù, 2006, Acute exposure to methylmercury at two developmental windows: focus on neurobehavioral and neurochemical effects in rat offspring, Neuroscience, 141, 1619, 10.1016/j.neuroscience.2006.05.017 Ceccatelli, 2010, Methylmercury-induced neurotoxicity and apoptosis, Chem. Biol. Interact., 188, 301, 10.1016/j.cbi.2010.04.007 Chang, 2013, Methylmercury induces caspase-dependent apoptosis and autophagy in human neural stem cells, J. Toxicol. Sci., 38, 823, 10.2131/jts.38.823 Chang, 2015, Activation of sonic hedgehog signaling enhances cell migration and invasion by induction of matrix metalloproteinase-2 and -9 via the phosphoinositide-3 kinase/akt signaling pathway in glioblastoma, Mol. Med. Rep., 12, 6702, 10.3892/mmr.2015.4229 Chang, 2019, Plant components can reduce methylmercury toxication: a mini-review, Biochim. Biophys. Acta Gen. Subj., 1863, 10.1016/j.bbagen.2019.01.012 Charton, 1999, Cellular and subcellular localization of the 2b-subunit of the nmda receptor in the adult rat telencephalon, Brain Res., 816, 609, 10.1016/S0006-8993(98)01243-8 Chen, 2014, Curcumin increased the differentiation rate of neurons in neural stem cells via wnt signaling in vitro study, J. Surg. Res., 192, 298, 10.1016/j.jss.2014.06.026 Cheng, 2001, Rat glutathione s-transferase m4-4: an isoenzyme with unique structural features including a redox-reactive cysteine-115 residue that forms mixed disulphides with glutathione, Biochem. J., 356, 403, 10.1042/bj3560403 Cheng, 2013, Neurobehavioral effects, c-fos/jun expression and tissue distribution in rat offspring prenatally co-exposed to mehg and pfoa: pfoa impairs hg retention, Chemosphere, 91, 758, 10.1016/j.chemosphere.2013.02.016 Cheng, 2015, Assessing pre/post-weaning neurobehavioral development for perinatal exposure to low doses of methylmercury, J. Environ. Sci. (China), 38, 36, 10.1016/j.jes.2015.05.027 Choi, 1978, Abnormal neuronal migration, deranged cerebral cortical organization, and diffuse white matter astrocytosis of human fetal brain: a major effect of methylmercury poisoning in utero, J. Neuropathol. Exp. Neurol., 37, 719, 10.1097/00005072-197811000-00001 Cialfi, 2014, Loss of notch1-dependent p21(waf1/cip1) expression influences the notch1 outcome in tumorigenesis, Cell Cycle, 13, 2046, 10.4161/cc.29079 Clarkson, 2002, The three modern faces of mercury, Environ. Health Perspect., 110, 11, 10.1289/ehp.02110s111 Cohen, 2005, A quantitative analysis of prenatal intake of n-3 polyunsaturated fatty acids and cognitive development, Am. J. Prev. Med., 29, 366, 10.1016/j.amepre.2005.06.008 Cosentino-Gomes, 2012, Cell signaling through protein kinase c oxidation and activation, Int. J. Mol. Sci., 13, 10697, 10.3390/ijms130910697 Costa, 2004, Developmental neuropathology of environmental agents, Annu. Rev. Pharmacol. Toxicol., 44 Dansen, 2009, Redox-sensitive cysteines bridge p300/cbp-mediated acetylation and foxo4 activity, Nat. Chem. Biol., 5, 664, 10.1038/nchembio.194 Daré, 2001, Methylmercury and h(2)o(2) provoke lysosomal damage in human astrocytoma d384 cells followed by apoptosis, Free Radic. Biol. Med., 30, 1347, 10.1016/S0891-5849(01)00526-3 Daré, 2003, Effects of prenatal exposure to methylmercury on dopamine-mediated locomotor activity and dopamine d2 receptor binding, Naunyn Schmiedebergs Arch. Pharmacol., 367, 500, 10.1007/s00210-003-0716-5 Debes, 2006, Impact of prenatal methylmercury exposure on neurobehavioral function at age 14 years, Neurotoxicol. Teratol., 28, 363, 10.1016/j.ntt.2006.02.004 Denu, 2016, Effects of oxidative stress on mesenchymal stem cell biology, Oxid. Med. Cell. Longev., 2016, 10.1155/2016/2989076 Deroma, 2013, Neuropsychological assessment at school-age and prenatal low-level exposure to mercury through fish consumption in an italian birth cohort living near a contaminated site, Int. J. Hyg. Environ. Health, 216, 486, 10.1016/j.ijheh.2013.02.004 Eliasson, 2010, The hematopoietic stem cell niche: low in oxygen but a nice place to be, J. Cell. Physiol., 222, 17, 10.1002/jcp.21908 Engel, 2014, The notch target e(spl)mδ is a muscle-specific gene involved in methylmercury toxicity in motor neuron development, Neurotoxicol. Teratol., 43, 11, 10.1016/j.ntt.2014.03.001 Erdogan, 2018, Midkine downregulation increases the efficacy of quercetin on prostate cancer stem cell survival and migration through pi3k/akt and mapk/erk pathway, Biomed. Pharmacother., 107, 793, 10.1016/j.biopha.2018.08.061 Espitia-Pérez, 2018, Neurobehavioral and oxidative stress alterations following methylmercury and retinyl palmitate co-administration in pregnant and lactating rats and their offspring, Neurotoxicology, 69, 164, 10.1016/j.neuro.2018.10.004 Falluel-Morel, 2012, N-acetyl cysteine treatment reduces mercury-induced neurotoxicity in the developing rat hippocampus, J. Neurosci. Res., 90, 743, 10.1002/jnr.22819 Fang, 2005, The mapk signalling pathways and colorectal cancer, Lancet Oncol., 6, 322, 10.1016/S1470-2045(05)70168-6 Farina, 2017, Methylmercury-induced neurotoxicity: focus on pro-oxidative events and related consequences, Adv. Neurobiol., 18, 267, 10.1007/978-3-319-60189-2_13 Farina, 2019, Glutathione antioxidant system and methylmercury-induced neurotoxicity: an intriguing interplay, Biochim. Biophys. Acta Gen. Subj., 1863, 10.1016/j.bbagen.2019.01.007 Farina, 2011, Oxidative stress in mehg-induced neurotoxicity, Toxicol. Appl. Pharmacol., 256, 405, 10.1016/j.taap.2011.05.001 Faustman, 2002, Investigations of methylmercury-induced alterations in neurogenesis, Environ. Health Perspect., 110, 859, 10.1289/ehp.02110s5859 Forsyth, 2006, Physiologic oxygen enhances human embryonic stem cell clonal recovery and reduces chromosomal abnormalities, Cloning Stem Cells, 8, 16, 10.1089/clo.2006.8.16 Franco, 2006, Cerebellar thiol status and motor deficit after lactational exposure to methylmercury, Environ. Res., 102, 22, 10.1016/j.envres.2006.02.003 Franco, 2007, Mercurial-induced hydrogen peroxide generation in mouse brain mitochondria: protective effects of quercetin, Chem. Res. Toxicol., 20, 1919, 10.1021/tx7002323 Franco, 2009, Methylmercury neurotoxicity is associated with inhibition of the antioxidant enzyme glutathione peroxidase, Free Radic. Biol. Med., 47, 449, 10.1016/j.freeradbiomed.2009.05.013 Fujimura, 2018, Methylmercury induces oxidative stress and subsequent neural hyperactivity leading to cell death through the p38 mapk-creb pathway in differentiated sh-sy5y cells, Neurotoxicology, 67, 226, 10.1016/j.neuro.2018.06.008 Fujimura, 2020, Methylmercury-mediated oxidative stress and activation of the cellular protective system, Antioxidants (Basel), 9 Fujimura, 2009, Methylmercury exposure downregulates the expression of racl and leads to neuritic degeneration and ultimately apoptosis in cerebrocortical neurons, Neurotoxicology, 30, 16, 10.1016/j.neuro.2008.10.002 Fujimura, 2009, Methylmercury induces neuropathological changes with tau hyperphosphorylation mainly through the activation of the c-jun-n-terminal kinase pathway in the cerebral cortex, but not in the hippocampus of the mouse brain, Neurotoxicology, 30, 1000, 10.1016/j.neuro.2009.08.001 Gao, 2008, Effects of methylmercury on postnatal neurobehavioral development in mice, Neurotoxicol. Teratol., 30, 462, 10.1016/j.ntt.2008.07.004 Grandjean, 2011, Methylmercury and brain development: imprecision and underestimation of developmental neurotoxicity in humans, Mt. Sinai J. Med., 78, 107, 10.1002/msj.20228 Grandjean, 1997, Cognitive deficit in 7-year-old children with prenatal exposure to methylmercury, Neurotoxicol. Teratol., 19, 417, 10.1016/S0892-0362(97)00097-4 Granitzer, 2021, Amino acid transporter lat1 (slc7a5) mediates mehg-induced oxidative stress defense in the human placental cell line htr-8/svneo, Int. J. Mol. Sci., 22 Gray, 1995, A physiologically based pharmacokinetic model for methyl mercury in the pregnant rat and fetus, Toxicol. Appl. Pharmacol., 132, 91, 10.1006/taap.1995.1090 Gribble, 2005, The magnitude of methylmercury-induced cytotoxicity and cell cycle arrest is p53-dependent, Birth Defects Res. Part A Clin. Mol. Teratol., 73, 29, 10.1002/bdra.20104 Hahn, 2015, Nrf2 and nrf2-related proteins in development and developmental toxicity: insights from studies in zebrafish (danio rerio), Free Radic. Biol. Med., 88, 275, 10.1016/j.freeradbiomed.2015.06.022 Han, 2008, Sirt1 regulates apoptosis and nanog expression in mouse embryonic stem cells by controlling p53 subcellular localization, Cell Stem Cell, 2, 241, 10.1016/j.stem.2008.01.002 Hashemi, 2016, Synthesis and cyto-genotoxicity evaluation of graphene on mice spermatogonial stem cells, Colloids Surf. B Biointerfaces, 146, 770, 10.1016/j.colsurfb.2016.07.019 Hassan, 2012, The effect of methylmercury exposure on early central nervous system development in the zebrafish (danio rerio) embryo, J. Appl. Toxicol., 32, 707, 10.1002/jat.1675 Heimfarth, 2018, Developmental neurotoxicity of the hippocampus following in utero exposure to methylmercury: impairment in cell signaling, Arch. Toxicol., 92, 513, 10.1007/s00204-017-2042-6 Holben, 1999, The diverse role of selenium within selenoproteins: a review, J. Am. Diet. Assoc., 99, 836, 10.1016/S0002-8223(99)00198-4 Huang, 2011, Neurotoxicological effects of low-dose methylmercury and mercuric chloride in developing offspring mice, Toxicol. Lett., 201, 196, 10.1016/j.toxlet.2010.12.016 Imayoshi, 2011, The role of notch signaling in adult neurogenesis, Mol. Neurobiol., 44, 7, 10.1007/s12035-011-8186-0 Inaba, 2009, Porphyromonas gingivalis invades human trophoblasts and inhibits proliferation by inducing g1 arrest and apoptosis, Cell. Microbiol., 11, 1517, 10.1111/j.1462-5822.2009.01344.x Inaba, 2018, Cell cycle arrest and apoptosis induced by porphyromonas gingivalis require jun n-terminal protein kinase- and p53-mediated p38 activation in human trophoblasts, Infect. Immun., 86 Itoh, 1999, Regulatory mechanisms of cellular response to oxidative stress, Free Radic. Res., 31, 319, 10.1080/10715769900300881 Jacob, 2019, Extenuation of in utero toxic effects of mehg in the developing neurons by fisetin via modulating the expression of synaptic transmission and plasticity regulators in hippocampus of the rat offspring, Chem. Biol. Interact., 305 Jacob, 2017, Effect of gestational intake of fisetin (3,3’,4’,7-tetrahydroxyflavone) on developmental methyl mercury neurotoxicity in f generation rats, Biol. Trace Elem. Res., 177, 297, 10.1007/s12011-016-0886-x Jacob, 2018, Fisetin impedes developmental methylmercury neurotoxicity via downregulating apoptotic signalling pathway and upregulating rho gtpase signalling pathway in hippocampus of f generation rats, Int. J. Dev. Neurosci., 69, 88, 10.1016/j.ijdevneu.2018.07.002 Janssen-Heininger, 2008, Redox-based regulation of signal transduction: principles, pitfalls, and promises, Free Radic. Biol. Med., 45 Jomova, 2010, Metals, oxidative stress and neurodegenerative disorders, Mol. Cell. Biochem., 345 Joshi, 2014, Reversal of methylmercury-induced oxidative stress, lipid peroxidation, and DNA damage by the treatment of n-acetyl cysteine: a protective approach, J. Environ. Pathol. Toxicol. Oncol., 33, 167, 10.1615/JEnvironPatholToxicolOncol.2014010291 Karri, 2018, An in vitro cytotoxic approach to assess the toxicity of heavy metals and their binary mixtures on hippocampal ht-22 cell line, Toxicol. Lett., 282, 25, 10.1016/j.toxlet.2017.10.002 Kaur, 2006, Glutathione modulation influences methyl mercury induced neurotoxicity in primary cell cultures of neurons and astrocytes, Neurotoxicology, 27, 492, 10.1016/j.neuro.2006.01.010 Ke, 2019, Post-translational modifications in mehg-induced neurotoxicity, Biochim. Biophys. Acta Mol. Basis Dis., 1865, 2068, 10.1016/j.bbadis.2018.10.024 Khan, 2003, Developmental changes in murine brain antioxidant enzymes, Pediatr. Res., 54, 77, 10.1203/01.PDR.0000065736.69214.20 Kim, 2007, The inhibitory mechanism of methylmercury on differentiation of human neuroblastoma cells, Toxicology, 234, 1, 10.1016/j.tox.2007.01.003 Kim, 2016, Hypoxia suppresses spontaneous mineralization and osteogenic differentiation of mesenchymal stem cells via igfbp3 up-regulation, Int. J. Mol. Sci., 17, 10.3390/ijms17091389 Kingham, 2009, Distinct roles for isoforms of the catalytic subunit of class-ia pi3k in the regulation of behaviour of murine embryonic stem cells, J. Cell. Sci., 122, 2311, 10.1242/jcs.046557 Kishi, 2017, The hokkaido birth cohort study on environment and children’s health: cohort profile-updated 2017, Environ. Health Prev. Med., 22, 46, 10.1186/s12199-017-0654-3 Kondo, 2005, Pkc/mapk signaling suppression by retinal pericyte conditioned medium prevents retinal endothelial cell proliferation, J. Cell. Physiol., 203, 378, 10.1002/jcp.20237 Kumagai, 2013, The role of the keap1/nrf2 pathway in the cellular response to methylmercury, Oxid. Med. Cell. Longev., 2013, 10.1155/2013/848279 Laplante, 2012, Mtor signaling in growth control and disease, Cell, 149, 274, 10.1016/j.cell.2012.03.017 Laugeray, 2018, Perinatal exposure to the cyanotoxin beta-n-methylamino-l-alanine (bmaa) results in long-lasting behavioral changes in offspring-potential involvement of DNA damage and oxidative stress, Neurotox. Res., 33, 87, 10.1007/s12640-017-9802-1 Lee, 2017, Adverse effects of methylmercury (mehg) on life parameters, antioxidant systems, and mapk signaling pathways in the rotifer brachionus koreanus and the copepod paracyclopina nana, Aquat. Toxicol., 190, 181, 10.1016/j.aquatox.2017.07.006 Li, 2019, Curcumin promotes proliferation of adult neural stem cells and the birth of neurons in alzheimer’s disease mice via notch signaling pathway, Cell. Reprogram., 21, 152, 10.1089/cell.2018.0027 Li, 2020, High cholesterol induces apoptosis and autophagy through the ros-activated akt/foxo1 pathway in tendon-derived stem cells, Stem Cell Res. Ther., 11, 131, 10.1186/s13287-020-01643-5 Liang, 2014, Stem cells, redox signaling, and stem cell aging, Antioxid. Redox Signal., 20, 1902, 10.1089/ars.2013.5300 Liu, 2017, Memantine, a low-affinity nmda receptor antagonist, protects against methylmercury-induced cytotoxicity of rat primary cultured cortical neurons, involvement of ca dyshomeostasis antagonism, and indirect antioxidation effects, Mol. Neurobiol., 54, 5034, 10.1007/s12035-016-0020-2 Liu, 2017, Memantine, a low-affinity nmda receptor antagonist, protects against methylmercury-induced cytotoxicity of rat primary cultured cortical neurons, involvement of ca(2+) dyshomeostasis antagonism, and indirect antioxidation effects, Mol. Neurobiol., 54, 5034, 10.1007/s12035-016-0020-2 Liu, 2019, Methyl-mercury induces apoptosis through ros-mediated endoplasmic reticulum stress and mitochondrial apoptosis pathways activation in rat cortical neurons, Free Radic. Res., 53, 26, 10.1080/10715762.2018.1546852 Lohren, 2016, Effects on and transfer across the blood-brain barrier in vitro-comparison of organic and inorganic mercury species, BMC Pharmacol. Toxicol., 17, 63, 10.1186/s40360-016-0106-5 Lu, 2009, Selenoproteins, J. Biol. Chem., 284, 723, 10.1074/jbc.R800045200 Lu, 2011, Involvement of oxidative stress-mediated erk1/2 and p38 activation regulated mitochondria-dependent apoptotic signals in methylmercury-induced neuronal cell injury, Toxicol. Lett., 204, 71, 10.1016/j.toxlet.2011.04.013 Lucena, 2010, Cipura paludosa attenuates long-term behavioral deficits in rats exposed to methylmercury during early development, Ecotoxicol. Environ. Saf., 73, 1150, 10.1016/j.ecoenv.2010.04.008 Lucena, 2013, Ethanolic extract from bulbs of cipura paludosa reduced long-lasting learning and memory deficits induced by prenatal methylmercury exposure in rats, Dev. Cogn. Neurosci., 3 Maia, 2009, Interference of ethanol and methylmercury in the developing central nervous system, Neurotoxicology, 30, 23, 10.1016/j.neuro.2008.11.008 Manfroi, 2004, Maternal milk as methylmercury source for suckling mice: neurotoxic effects involved with the cerebellar glutamatergic system, Toxicol. Sci., 81, 172, 10.1093/toxsci/kfh201 Marchiani, 2014, Curcumin and curcumin-like molecules: from spice to drugs, Curr. Med. Chem., 21, 204, 10.2174/092986732102131206115810 Marty, 1997, Pathways mediating ca2+ entry in rat cerebellar granule cells following in vitro exposure to methyl mercury, Toxicol. Appl. Pharmacol., 147, 319, 10.1006/taap.1997.8262 McCubrey, 2007, Roles of the raf/mek/erk pathway in cell growth, malignant transformation and drug resistance, Biochim. Biophys. Acta, 1773, 1263, 10.1016/j.bbamcr.2006.10.001 Melov, 1999, Mitochondrial disease in superoxide dismutase 2 mutant mice, Proc. Natl. Acad. Sci. U. S. A., 96, 846, 10.1073/pnas.96.3.846 Mendoza, 2002, P21(waf1/cip1) inhibits cell cycle progression but not g2/m-phase transition following methylmercury exposure, Toxicol. Appl. Pharmacol., 178, 117, 10.1006/taap.2001.9267 Merchant, 2011, The redox-sensitive transcription factor nrf2 regulates murine hematopoietic stem cell survival independently of ros levels, Blood, 118, 6572, 10.1182/blood-2011-05-355362 Miyamoto, 2001, Involvement of enhanced sensitivity of n-methyl-d-aspartate receptors in vulnerability of developing cortical neurons to methylmercury neurotoxicity, Brain Res., 901, 252, 10.1016/S0006-8993(01)02281-8 Miyashita, 2015, Effects of in utero exposure to polychlorinated biphenyls, methylmercury, and polyunsaturated fatty acids on birth size, Sci. Total Environ., 533, 256, 10.1016/j.scitotenv.2015.06.108 Myers, 2003, Prenatal methylmercury exposure from ocean fish consumption in the seychelles child development study, Lancet, 361, 1686, 10.1016/S0140-6736(03)13371-5 Nava, 2000, Melatonin attenuates acute renal failure and oxidative stress induced by mercuric chloride in rats, Am. J. Physiol. Renal Physiol., 279, F910, 10.1152/ajprenal.2000.279.5.F910 Ng, 2015, Mercury, apoe, and child behavior, Chemosphere, 120, 123, 10.1016/j.chemosphere.2014.06.003 Ni, 2011, Comparative study on the response of rat primary astrocytes and microglia to methylmercury toxicity, Glia, 59, 810, 10.1002/glia.21153 Nishigaki, 1975, Methylmercury and selenium in umbilical cords of inhabitants of the minamata area, Nature, 258, 324, 10.1038/258324a0 Nishioku, 2000, Involvement of caspase 3-like protease in methylmercury-induced apoptosis of primary cultured rat cerebral microglia, Brain Res., 871, 160, 10.1016/S0006-8993(00)02436-7 Nogara, 2019, Methylmercury’s chemistry: from the environment to the mammalian brain, Biochim. Biophys. Acta Gen. Subj., 1863, 10.1016/j.bbagen.2019.01.006 Olguín, 2018, Neurotransmitter amines and antioxidant agents in neuronal protection against methylmercury-induced cytotoxicity in primary cultures of mice cortical neurons, Neurotoxicology, 69, 278, 10.1016/j.neuro.2018.07.020 Orrenius, 2011, Cell death mechanisms and their implications in toxicology, Toxicol. Sci., 119 Ou, 1999, Induction of the cell cycle regulatory gene p21 (waf1, cip1) following methylmercury exposure in vitro and in vivo, Toxicol. Appl. Pharmacol., 157, 203, 10.1006/taap.1999.8685 Ou, 2018, Physiologically based pharmacokinetic (pbpk) modeling of human lactational transfer of methylmercury in china, Environ. Int., 115, 180, 10.1016/j.envint.2018.03.018 Paithankar, 2021, Heavy metal associated health hazards: an interplay of oxidative stress and signal transduction, Chemosphere, 262, 10.1016/j.chemosphere.2020.128350 Paletz, 2006, Gestational exposure to methylmercury and n-3 fatty acids: effects on high- and low-rate operant behavior in adulthood, Neurotoxicol. Teratol., 28, 59, 10.1016/j.ntt.2005.11.003 Paling, 2004, Regulation of embryonic stem cell self-renewal by phosphoinositide 3-kinase-dependent signaling, J. Biol. Chem., 279, 48063, 10.1074/jbc.M406467200 Papp, 2007, From selenium to selenoproteins: synthesis, identity, and their role in human health, Antioxid. Redox Signal., 9, 775, 10.1089/ars.2007.1528 Patel, 2013, Methylmercury impairs motor function in early development and induces oxidative stress in cerebellar granule cells, Toxicol. Lett., 222, 265, 10.1016/j.toxlet.2013.08.002 Peyvandi, 2018, Deferoxamine promotes mesenchymal stem cell homing in noise-induced injured cochlea through pi3k/akt pathway, Cell Prolif., 51, 10.1111/cpr.12434 Pierozan, 2017, Neurotoxicity of methylmercury in isolated astrocytes and neurons: the cytoskeleton as a main target, Mol. Neurobiol., 54, 5752, 10.1007/s12035-016-0101-2 Pinho, 2017, Antioxidant and mercury chelating activity of psidium guajava var. Pomifera l. Leaves hydroalcoholic extract, J. Toxicol. Environ. Health A, 80, 1301, 10.1080/15287394.2017.1382408 Prince, 2017, Notch target gene e(spl)mδ is a mediator of methylmercury-induced myotoxicity in drosophila, Front. Genet., 8, 233, 10.3389/fgene.2017.00233 Raciti, 2019, Nrxn1 deletion and exposure to methylmercury increase astrocyte differentiation by different notch-dependent transcriptional mechanisms, Front. Genet., 10, 593, 10.3389/fgene.2019.00593 Ramkissoon, 2013, Developmental role of nuclear factor e2-related factor 2 in mitigating methamphetamine fetal toxicity and postnatal neurodevelopmental deficits, Free Radic. Biol. Med., 65, 620, 10.1016/j.freeradbiomed.2013.07.043 Ray, 2012, Reactive oxygen species (ros) homeostasis and redox regulation in cellular signaling, Cell. Signal., 24, 981, 10.1016/j.cellsig.2012.01.008 Rodrigues, 2019, Aqueous coriandrum sativum l. Extract promotes neuroprotection against motor changes and oxidative damage in rat progeny after maternal exposure to methylmercury, Food Chem. Toxicol., 133, 10.1016/j.fct.2019.110755 Rothenberg, 2011, Low-level maternal methylmercury exposure through rice ingestion and potential implications for offspring health, Environ. Pollut., 159, 1017, 10.1016/j.envpol.2010.12.024 Ryu, 2015, Regulation of stem cell fate by ros-mediated alteration of metabolism, Int. J. Stem Cells, 8, 24, 10.15283/ijsc.2015.8.1.24 Sakamoto, 2002, Evaluation of changes in methylmercury accumulation in the developing rat brain and its effects: a study with consecutive and moderate dose exposure throughout gestation and lactation periods, Brain Res., 949, 51, 10.1016/S0006-8993(02)02964-5 Sanders, 2015, Perinatal and childhood exposure to cadmium, manganese, and metal mixtures and effects on cognition and behavior: a review of recent literature, Curr. Environ. Health Rep., 2, 284, 10.1007/s40572-015-0058-8 Sargis, 2006, Protection of membrane cholesterol by sphingomyelin against free radical-mediated oxidation, Free Radic. Biol. Med., 40, 2092, 10.1016/j.freeradbiomed.2006.02.005 Savickiene, 1999, Modulation of apoptosis of proliferating and differentiating hl-60 cells by protein kinase inhibitors: suppression of pkc or pka differently affects cell differentiation and apoptosis, Cell Death Differ., 6, 698, 10.1038/sj.cdd.4400541 Sethi, 2009, Curcumin attenuates aluminium-induced functional neurotoxicity in rats, Pharmacol. Biochem. Behav., 93, 31, 10.1016/j.pbb.2009.04.005 Sfakianakis, 2015, Effect of heavy metals on fish larvae deformities: a review, Environ. Res., 137, 246, 10.1016/j.envres.2014.12.014 Shimura, 2017, A comparison of radiation-induced mitochondrial damage between neural progenitor stem cells and differentiated cells, Cell Cycle, 16, 565, 10.1080/15384101.2017.1284716 Simon, 2008, The role of oxygen availability in embryonic development and stem cell function, Nat. Rev. Mol. Cell Biol., 9, 285, 10.1038/nrm2354 Sirois, 2000, Methylmercury affects multiple subtypes of calcium channels in rat cerebellar granule cells, Toxicol. Appl. Pharmacol., 167 Snoj Tratnik, 2017, Prenatal mercury exposure, neurodevelopment and apolipoprotein e genetic polymorphism, Environ. Res., 152, 375, 10.1016/j.envres.2016.08.035 Sobolewski, 2018, Endocrine active metals, prenatal stress and enhanced neurobehavioral disruption, Horm. Behav., 101, 36, 10.1016/j.yhbeh.2018.01.004 Steinbrenner, 2009, Protection against reactive oxygen species by selenoproteins, Biochim. Biophys. Acta, 1790, 1478, 10.1016/j.bbagen.2009.02.014 Steuerwald, 2000, Maternal seafood diet, methylmercury exposure, and neonatal neurologic function, J. Pediatr., 136, 599, 10.1067/mpd.2000.102774 Straka, 2016, Mercury toxicokinetics of the healthy human term placenta involve amino acid transporters and abc transporters, Toxicology, 340, 34, 10.1016/j.tox.2015.12.005 Stringari, 2008, Prenatal methylmercury exposure hampers glutathione antioxidant system ontogenesis and causes long-lasting oxidative stress in the mouse brain, Toxicol. Appl. Pharmacol., 227, 147, 10.1016/j.taap.2007.10.010 Su, 2019, Reactive oxygen species-induced lipid peroxidation in apoptosis, autophagy, and ferroptosis, Oxid. Med. Cell. Longev., 2019, 10.1155/2019/5080843 Suzuki, 2015, Molecular basis of the keap1-nrf2 system, Free Radic. Biol. Med., 88 Takahashi, 2017, Methylmercury causes blood-brain barrier damage in rats via upregulation of vascular endothelial growth factor expression, PLoS One, 12, 10.1371/journal.pone.0170623 Takahata, 2009, Functional expression of beta2 adrenergic receptors responsible for protection against oxidative stress through promotion of glutathione synthesis after nrf2 upregulation in undifferentiated mesenchymal c3h10t1/2 stem cells, J. Cell. Physiol., 218, 268, 10.1002/jcp.21594 Tamm, 2008, Methylmercury inhibits differentiation of rat neural stem cells via notch signalling, Neuroreport, 19, 339, 10.1097/WNR.0b013e3282f50ca4 Tatsuta, 2017, Psychomotor ability in children prenatally exposed to methylmercury: the 18-month follow-up of tohoku study of child development, Tohoku J. Exp. Med., 242, 1, 10.1620/tjem.242.1 Tofighi, 2011, Non-dioxin-like polychlorinated biphenyls interfere with neuronal differentiation of embryonic neural stem cells, Toxicol. Sci., 124, 192, 10.1093/toxsci/kfr221 Toyama, 2007, Cytoprotective role of nrf2/keap1 system in methylmercury toxicity, Biochem. Biophys. Res. Commun., 363, 645, 10.1016/j.bbrc.2007.09.017 Uchikawa, 2011, Chlorella suppresses methylmercury transfer to the fetus in pregnant mice, J. Toxicol. Sci., 36, 675, 10.2131/jts.36.675 Valko, 2005, Metals, toxicity and oxidative stress, Curr. Med. Chem., 12, 1161, 10.2174/0929867053764635 Vejrup, 2018, Prenatal mercury exposure, maternal seafood consumption and associations with child language at five years, Environ. Int., 110, 71, 10.1016/j.envint.2017.10.008 Villaseñor, 2017, Region-specific permeability of the blood-brain barrier upon pericyte loss, J. Cereb. Blood Flow Metab., 37, 3683, 10.1177/0271678X17697340 Wagner, 2010, In vivo and in vitro inhibition of mice thioredoxin reductase by methylmercury, Biometals, 23, 1171, 10.1007/s10534-010-9367-4 Wagner, 2010, Comparative study of quercetin and its two glycoside derivatives quercitrin and rutin against methylmercury (mehg)-induced ros production in rat brain slices, Arch. Toxicol., 84, 89, 10.1007/s00204-009-0482-3 Wakabayashi, 2010, Regulation of notch1 signaling by nrf2: implications for tissue regeneration, Sci. Signal., 3 Wakabayashi, 2015, Crosstalk between nrf2 and notch signaling, Free Radic. Biol. Med., 88, 158, 10.1016/j.freeradbiomed.2015.05.017 Wang, 2009, Trichosanthin suppresses hela cell proliferation through inhibition of the pkc/mapk signaling pathway, Cell Biol. Toxicol., 25, 479, 10.1007/s10565-008-9102-x Wang, 2013, Redox homeostasis: the linchpin in stem cell self-renewal and differentiation, Cell Death Dis., 4, e537, 10.1038/cddis.2013.50 Wang, 2014, Postnatal exposure to methyl mercury and neuropsychological development in 7-year-old urban inner-city children exposed to lead in the united states, Child Neuropsychol., 20, 527, 10.1080/09297049.2013.824955 Wang, 2016, Low-dose methylmercury-induced apoptosis and mitochondrial DNA mutation in human embryonic neural progenitor cells, Oxid. Med. Cell. Longev., 2016, 10.1155/2016/5137042 Wang, 2016, Low-dose methylmercury-induced genes regulate mitochondrial biogenesis via mir-25 in immortalized human embryonic neural progenitor cells, Int. J. Mol. Sci., 17 Wang, 2018, Curcumin pretreatment prevents hydrogen peroxide-induced oxidative stress through enhanced mitochondrial function and deactivation of akt/erk signaling pathways in rat bone marrow mesenchymal stem cells, Mol. Cell. Biochem., 443, 37, 10.1007/s11010-017-3208-5 Wang, 2019, Curcumin pretreatment protects against hypoxia/reoxgenation injury via improvement of mitochondrial function, destabilization of hif-1α and activation of epac1-akt pathway in rat bone marrow mesenchymal stem cells, Biomed. Pharmacother., 109, 1268, 10.1016/j.biopha.2018.11.005 Yan, 1997, Oxidative damage during aging targets mitochondrial aconitase, Proc. Natl. Acad. Sci. U. S. A., 94, 11168, 10.1073/pnas.94.21.11168 Yang, 2016, Protective effects of alpha-lipoic acid on mehg-induced oxidative damage and intracellular ca(2+) dyshomeostasis in primary cultured neurons, Free Radic. Res., 50, 542, 10.3109/10715762.2016.1152362 Yang, 2019, Curcumin protects against methylmercury-induced cytotoxicity in primary rat astrocytes by activating the nrf2/are pathway independently of pkcδ, Toxicology, 425, 10.1016/j.tox.2019.152248 Yoshida, 2014, Neurobehavioral changes in response to alterations in gene expression profiles in the brains of mice exposed to low and high levels of mercury vapor during postnatal development, J. Toxicol. Sci., 39, 561, 10.2131/jts.39.561 Yu, 2016, Proliferation, survival and metabolism: the role of pi3k/akt/mtor signalling in pluripotency and cell fate determination, Development, 143, 3050, 10.1242/dev.137075 Zareba, 2007, Thimerosal distribution and metabolism in neonatal mice: comparison with methyl mercury, J. Appl. Toxicol., 27, 511, 10.1002/jat.1272 Zhang, 2016, Ros and ros-mediated cellular signaling, Oxid. Med. Cell. Longev., 2016, 10.1155/2016/4350965 Zhang, 2018, Hydrogen ameliorates oxidative stress via pi3k-akt signaling pathway in uvb-induced hacat cells, Int. J. Mol. Med., 41, 3653 Zhang, 2020, Neuroprotective effects of astaxanthin against oxygen and glucose deprivation damage via the pi3k/akt/gsk3β/nrf2 signalling pathway in vitro, J. Cell. Mol. Med. Zhuang, 2019, Resveratrol attenuates oxidative stress-induced intestinal barrier injury through pi3k/akt-mediated nrf2 signaling pathway, Oxid. Med. Cell. Longev., 2019, 10.1155/2019/7591840 Zou, 2014, Nrf2 is involved in maintaining hepatocyte identity during liver regeneration, PLoS One, 9, 10.1371/journal.pone.0107423