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Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Review Article

Current Insights into the Neurotoxicity of Melamine: A Comprehensive Review

In Press, (this is not the final "Version of Record"). Available online 08 April, 2024
Author(s): Reza Naeimi, Fatemeh Safarpour, Hamid Askari and Maryam Ghasemi-Kasman*
Published on: 08 April, 2024

DOI: 10.2174/1570159X22666240320133241

Price: $95

Abstract

Melamine, a heterocyclic nitrogen-rich triazine chemical compound, is widely used in various household products, including furniture, dinnerware, and kitchen appliances. The unauthorized addition of the mixture to various foodstuffs to misrepresent protein content resulted in catastrophic, frequently life-threatening health consequences for kids as well as canines and has garnered international attention. Numerous primary studies and evaluations have been focused on melamine toxicity's implications on kidney function. Despite the profusion of literature on melamine's nephrotoxicity, evidence regarding its toxicity to other organs remains scarce. A number of recent studies suggest melamine can disrupt central nervous system (CNS) function and bring about cognitive impairments, contradicting the commonly held belief that melamine's detrimental effects are limited to the urinary system. The accumulation of melamine in the body is linked to various adverse effects, including depression, impaired synaptic transmission, oxidative stress, and neurodegenerative diseases. Several mechanisms may lead to such complications. However, numerous safeguards against melamine accumulation have been identified. This review could shed light on the potential neurological effects and mechanisms underlying melamine toxicity. Afterward, we will dive into the body's possible protective mechanisms against melamine-induced toxicity.

[1]
Ibhazehiebo, K.; Koibuchi, N. Melamine: An Emerging Neurotoxicant? J. Med. Biomed. Res., 2012, 11(1), 20-28.
[2]
An, L.; Li, Z.; Zhang, T. Reversible effects of vitamins C and E combination on oxidative stress-induced apoptosis in melamine-treated PC12 cells. Free Radic. Res., 2014, 48(2), 239-250.
[http://dx.doi.org/10.3109/10715762.2013.861598] [PMID: 24182201]
[3]
Lu, J.; Xiao, J.; Yang, D.J.; Wang, Z.T.; Jiang, D.G.; Fang, C.R.; Yang, J. Study on migration of melamine from food packaging materials on markets. Biomed. Environ. Sci., 2009, 22(2), 104-108.
[http://dx.doi.org/10.1016/S0895-3988(09)60030-1] [PMID: 19618686]
[4]
Hilts, C.; Pelletier, L. Eds.; Background paper on occurrence of melamine in foods and feed. World Health Organization: Meeting on toxicological and health aspects of melamine and cyanuric acid; Citeseer, 2009.
[5]
Bolden, A.L.; Rochester, J.R.; Kwiatkowski, C.F. Melamine, beyond the kidney: A ubiquitous endocrine disruptor and neurotoxicant? Toxicol. Lett., 2017, 280, 181-189.
[http://dx.doi.org/10.1016/j.toxlet.2017.07.893] [PMID: 28751210]
[6]
An, L.; Sun, W. Prenatal melamine exposure impairs spatial cognition and hippocampal synaptic plasticity by presynaptic and postsynaptic inhibition of glutamatergic transmission in adolescent offspring. Toxicol. Lett., 2017, 269, 55-64.
[http://dx.doi.org/10.1016/j.toxlet.2017.02.005] [PMID: 28185983]
[7]
Shellaiah, M.; Sun, K. Review on nanomaterial-based melamine detection. Chemosensors (Basel), 2019, 7(1), 9.
[http://dx.doi.org/10.3390/chemosensors7010009]
[8]
Yalçin, S.S.; Güneş, B.; Yalçin, S. Presence of melamine in human milk and the evaluation of the effects on mother-infant pairs in a cohort study. Hum. Exp. Toxicol., 2020, 39(5), 624-633.
[http://dx.doi.org/10.1177/0960327119898748] [PMID: 31928232]
[9]
An, L.; Zhang, T. Comparison impairments of spatial cognition and hippocampal synaptic plasticity between prenatal and postnatal melamine exposure in male adult rats. Neurotox. Res., 2016, 29(2), 218-229.
[http://dx.doi.org/10.1007/s12640-015-9578-0] [PMID: 26607910]
[10]
Yang, J.; An, L.; Yao, Y.; Yang, Z.; Zhang, T. Melamine impairs spatial cognition and hippocampal synaptic plasticity by presynaptic inhibition of glutamatergic transmission in infant rats. Toxicology, 2011, 289(2-3), 167-174.
[http://dx.doi.org/10.1016/j.tox.2011.08.011] [PMID: 21867740]
[11]
Wu, Y.T.; Huang, C.M.; Lin, C.C.; Ho, W.A.; Lin, L.C.; Chiu, T.F.; Tarng, D.C.; Lin, C.H.; Tsai, T.H. Determination of melamine in rat plasma, liver, kidney, spleen, bladder and brain by liquid chromatography-tandem mass spectrometry. J. Chromatogr. A, 2009, 1216(44), 7595-7601.
[http://dx.doi.org/10.1016/j.chroma.2009.05.027] [PMID: 19493536]
[12]
Han, Y.; Liu, S.; Zhang, T.; Yang, Z. Induction of apoptosis by melamine in differentiated PC12 cells. Cell. Mol. Neurobiol., 2011, 31(1), 65-71.
[http://dx.doi.org/10.1007/s10571-010-9554-4] [PMID: 20706782]
[13]
Hau, A.K.; Kwan, T.H.; Li, P.K. Melamine toxicity and the kidney. J. Am. Soc. Nephrol., 2009, 20(2), 245-250.
[http://dx.doi.org/10.1681/ASN.2008101065] [PMID: 19193777]
[14]
Yan, Wang Fei Liu; Yuejiao Wei; Daicheng Liu, The effect of exogenous melamine on rat hippocampal neurons. Toxicol. Ind. Health, 2011, 27(6), 571-576.
[http://dx.doi.org/10.1177/0748233710395347] [PMID: 21402658]
[15]
Yang, Y.; Xiong, G.J.; Yu, D.F.; Cao, J.; Wang, L.P.; Xu, L.; Mao, R.R. Acute low-dose melamine affects hippocampal synaptic plasticity and behavior in rats. Toxicol. Lett., 2012, 214(1), 63-68.
[http://dx.doi.org/10.1016/j.toxlet.2012.08.010] [PMID: 22922007]
[16]
An, L.; Li, Z.; Yang, Z.; Zhang, T. Melamine induced cognitive impairment associated with oxidative damage in rat’s hippocampus. Pharmacol. Biochem. Behav., 2012, 102(2), 196-202.
[http://dx.doi.org/10.1016/j.pbb.2012.04.009] [PMID: 22564861]
[17]
An, L.; Li, J.; Luo, L.; Huang, P.; Liu, P.; Tang, C.; Sun, W. Prenatal melamine exposure impairs cognitive flexibility and hippocampal synaptic plasticity in adolescent and adult female rats. Pharmacol. Biochem. Behav., 2019, 186172791.
[http://dx.doi.org/10.1016/j.pbb.2019.172791] [PMID: 31518600]
[18]
Dobson, R.L.M.; Motlagh, S.; Quijano, M.; Cambron, R.T.; Baker, T.R.; Pullen, A.M.; Regg, B.T.; Bigalow-Kern, A.S.; Vennard, T.; Fix, A.; Reimschuessel, R.; Overmann, G.; Shan, Y.; Daston, G.P. Identification and characterization of toxicity of contaminants in pet food leading to an outbreak of renal toxicity in cats and dogs. Toxicol. Sci., 2008, 106(1), 251-262.
[http://dx.doi.org/10.1093/toxsci/kfn160] [PMID: 18689873]
[19]
Wei, Y.; Liu, D. Review of melamine scandal: still a long way ahead. Toxicol. Ind. Health, 2012, 28(7), 579-582.
[http://dx.doi.org/10.1177/0748233711416950] [PMID: 21986885]
[20]
An, L.; Li, Z.; Yang, Z.; Zhang, T. Cognitive deficits induced by melamine in rats. Toxicol. Lett., 2011, 206(3), 276-280.
[http://dx.doi.org/10.1016/j.toxlet.2011.08.009] [PMID: 21888959]
[21]
Hu, P.; Wang, J.; Zhang, M.; Hu, B.; Lu, L.; Zhang, C-R.; Du, P-F. Liver involvement in melamine-associated nephrolithiasis. Arch. Iran Med., 2012, 15(4), 247-248.
[PMID: 22424045]
[22]
Wen, J.G.; Chang, Q.L.; Lou, A.F.; Li, Z.Z.; Lu, S.; Wang, Y.; Wang, Y.L.; Hu, J.H.; Mao, S.P.; Zhang, Y.; Xue, R.; Ren, C.; Xing, L.; Zhang, G.X.; Zhang, S.; Djurhuus, J.C.; Frøkiaer, J. Melamine-related urinary stones in 195 infants and young children: clinical features within 2 years of follow-up. Urol. Int., 2011, 87(4), 429-433.
[http://dx.doi.org/10.1159/000330795] [PMID: 22057293]
[23]
Jia, L.; Shen, Y.; Wang, X.; He, L.; Xin, Y.; Hu, Y. Ultrasonographic diagnosis of urinary calculus caused by melamine in children. Chin. Med. J. (Engl.), 2009, 122(3), 252-256.
[http://dx.doi.org/10.3760/cma.j.issn.0366-6999.2009.03.003] [PMID: 19236799]
[24]
Kamedulski, P.; Lukaszewicz, J.P.; Witczak, L.; Szroeder, P.; Ziolkowski, P. The importance of structural factors for the electrochemical performance of graphene/carbon nanotube/melamine powders towards the catalytic activity of oxygen reduction reaction. Materials (Basel), 2021, 14(9), 2448.
[http://dx.doi.org/10.3390/ma14092448] [PMID: 34065055]
[25]
Wu, Y.T.; Huang, C.M.; Lin, C.C.; Ho, W.A.; Lin, L.C.; Chiu, T.F.; Tarng, D.C.; Lin, C.H.; Tsai, T.H. Oral bioavailability, urinary excretion and organ distribution of melamine in Sprague-Dawley rats by high-performance liquid chromatography with tandem mass spectrometry. J. Agric. Food Chem., 2010, 58(1), 108-111.
[http://dx.doi.org/10.1021/jf902872j] [PMID: 20014856]
[26]
El-Hassar, L.; Milh, M.; Wendling, F.; Ferrand, N.; Esclapez, M.; Bernard, C. Cell domain‐dependent changes in the glutamatergic and GABAergic drives during epileptogenesis in the rat CA1 region. J. Physiol., 2007, 578(1), 193-211.
[http://dx.doi.org/10.1113/jphysiol.2006.119297] [PMID: 17008374]
[27]
Tayem, Y.I.; Veeramuthu, S.V.; Rashid, A.N.; Sequeira, R.P.; Fadel, R.A. Effect of melamine administration during pregnancy on foetal bone ossification. Ital. J. Anat. Embryol., 2019, 124(3), 467-474.
[28]
Olsen, R.K.; Moses, S.N.; Riggs, L.; Ryan, J.D. The hippocampus supports multiple cognitive processes through relational binding and comparison. Front. Hum. Neurosci., 2012, 6, 146.
[http://dx.doi.org/10.3389/fnhum.2012.00146] [PMID: 22661938]
[29]
Todd, A.C.; Hardingham, G.E. The regulation of astrocytic glutamate transporters in health and neurodegenerative diseases. Int. J. Mol. Sci., 2020, 21(24), 9607.
[http://dx.doi.org/10.3390/ijms21249607] [PMID: 33348528]
[30]
An, L.; Sun, W. Acute melamine affects spatial memory consolidation via inhibiting hippocampal NMDAR-dependent LTD in rats. Toxicol. Sci., 2018, 163(2), 385-396.
[http://dx.doi.org/10.1093/toxsci/kfx039] [PMID: 28206646]
[31]
An, L.; Yang, Z.; Zhang, T. Melamine induced spatial cognitive deficits associated with impairments of hippocampal long-term depression and cholinergic system in Wistar rats. Neurobiol. Learn. Mem., 2013, 100, 18-24.
[http://dx.doi.org/10.1016/j.nlm.2012.12.003] [PMID: 23231966]
[32]
Zeng, H.; Chattarji, S.; Barbarosie, M.; Rondi-Reig, L.; Philpot, B.D.; Miyakawa, T.; Bear, M.F.; Tonegawa, S. Forebrain-specific calcineurin knockout selectively impairs bidirectional synaptic plasticity and working/episodic-like memory. Cell, 2001, 107(5), 617-629.
[http://dx.doi.org/10.1016/S0092-8674(01)00585-2] [PMID: 11733061]
[33]
Xu, X.; An, L.; Mi, X.; Zhang, T. Impairment of cognitive function and synaptic plasticity associated with alteration of information flow in theta and gamma oscillations in melamine-treated rats. PLoS One, 2013, 8(10), e77796.
[http://dx.doi.org/10.1371/journal.pone.0077796] [PMID: 24204970]
[34]
Colgin, L.L.; Denninger, T.; Fyhn, M.; Hafting, T.; Bonnevie, T.; Jensen, O.; Moser, M.B.; Moser, E.I. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature, 2009, 462(7271), 353-357.
[http://dx.doi.org/10.1038/nature08573] [PMID: 19924214]
[35]
Colgin, L.L. Slow gamma takes the reins in replay. Neuron, 2012, 75(4), 549-550.
[http://dx.doi.org/10.1016/j.neuron.2012.08.006] [PMID: 22920247]
[36]
An, L.; Zhang, T. Prenatal melamine exposure induces impairments of spatial cognition and hippocampal synaptic plasticity in male adolescent rats. Reprod. Toxicol., 2014, 49, 78-85.
[http://dx.doi.org/10.1016/j.reprotox.2014.07.081] [PMID: 25111974]
[37]
Sun, W.; Wu, Y.; Tang, D.; Li, X.; An, L. Melamine disrupts spatial reversal learning and learning strategy via inhibiting hippocampal BDNF-mediated neural activity. PLoS One, 2021, 16(1), e0245326.
[http://dx.doi.org/10.1371/journal.pone.0245326] [PMID: 33428671]
[38]
Rosas-Vidal, L.E.; Do-Monte, F.H.; Sotres-Bayon, F.; Quirk, G.J. Hippocampal-prefrontal BDNF and memory for fear extinction. Neuropsychopharmacology, 2014, 39(9), 2161-2169.
[http://dx.doi.org/10.1038/npp.2014.64] [PMID: 24625752]
[39]
Yu, S.P.; Canzoniero, L.M.T.; Choi, D.W. Ion homeostasis and apoptosis. Curr. Opin. Cell Biol., 2001, 13(4), 405-411.
[http://dx.doi.org/10.1016/S0955-0674(00)00228-3] [PMID: 11454444]
[40]
Yang, J.J.; Tian, Y.T.; Yang, Z.; Zhang, T. Effect of melamine on potassium currents in rat hippocampal CA1 neurons. Toxicol. In Vitro, 2010, 24(2), 397-403.
[http://dx.doi.org/10.1016/j.tiv.2009.10.019] [PMID: 19895883]
[41]
Schröder, W.; Hinterkeuser, S.; Seifert, G.; Schramm, J.; Jabs, R.; Wilkin, G.P.; Steinhäuser, C. Functional and molecular properties of human astrocytes in acute hippocampal slices obtained from patients with temporal lobe epilepsy. Epilepsia, 2000, 41(s6)(Suppl. 6), S181-S184.
[http://dx.doi.org/10.1111/j.1528-1157.2000.tb01578.x] [PMID: 10999541]
[42]
Yang, J.J.; Yang, Z.; Zhang, T. Action potential changes associated with impairment of functional properties of sodium channels in hippocampal neurons induced by melamine. Toxicol. Lett., 2010, 198(2), 171-176.
[http://dx.doi.org/10.1016/j.toxlet.2010.06.013] [PMID: 20599599]
[43]
Mast, R.W.; Jeffcoat, A.R.; Sadler, B.M.; Kraska, R.C.; Friedman, M.A. Metabolism, disposition and excretion of [14C]melamine in male Fischer 344 rats. Food Chem. Toxicol., 1983, 21(6), 807-810.
[http://dx.doi.org/10.1016/0278-6915(83)90216-8] [PMID: 6686586]
[44]
Erisgin, Z. Melamine exposure from the weaning period causes apoptosis, inflammation, and damage to the blood-brain barrier. J. Chem. Neuroanat., 2021, 113101939.
[http://dx.doi.org/10.1016/j.jchemneu.2021.101939] [PMID: 33639231]
[45]
Guo, C.; He, Z.; Wen, L.; Zhu, L.; Lu, Y.; Deng, S.; Yang, Y.; Wei, Q.; Yuan, H. Cytoprotective effect of trolox against oxidative damage and apoptosis in the NRK‐52e cells induced by melamine. Cell Biol. Int., 2012, 36(2), 183-188.
[http://dx.doi.org/10.1042/CBI20110036] [PMID: 21939437]
[46]
Wilcox, C.S. Oxidative stress and nitric oxide deficiency in the kidney: a critical link to hypertension? Am. J. Physiol. Regul. Integr. Comp. Physiol., 2005, 289(4), R913-R935.
[http://dx.doi.org/10.1152/ajpregu.00250.2005] [PMID: 16183628]
[47]
An, L.; Fu, J.; Zhang, T. Reversible effects of vitamins C and E combination on cognitive deficits and oxidative stress in the hippocampus of melamine-exposed rats. Pharmacol. Biochem. Behav., 2015, 132, 152-159.
[http://dx.doi.org/10.1016/j.pbb.2015.03.009] [PMID: 25802127]
[48]
Fu, J.; Wang, H.; Gao, J.; Yu, M.; Wang, R.; Yang, Z.; Zhang, T. Rapamycin Effectively Impedes Melamine-Induced Impairments of Cognition and Synaptic Plasticity in Wistar Rats. Mol. Neurobiol., 2017, 54(2), 819-832.
[http://dx.doi.org/10.1007/s12035-016-9687-7] [PMID: 26768596]
[49]
Guo, C.; Yuan, H.; He, Z. Melamine causes apoptosis of rat kidney epithelial cell line (NRK‐52e cells) via excessive intracellular ROS (reactive oxygen species) and the activation of p38 MAPK pathway. Cell Biol. Int., 2012, 36(4), 383-389.
[http://dx.doi.org/10.1042/CBI20110504] [PMID: 22150157]
[50]
Kuo, F.C.; Tseng, Y.T.; Wu, S.R.; Wu, M.T.; Lo, Y.C. Melamine activates NFκB/COX-2/PGE2 pathway and increases NADPH oxidase–dependent ROS production in macrophages and human embryonic kidney cells. Toxicol. In Vitro, 2013, 27(6), 1603-1611.
[http://dx.doi.org/10.1016/j.tiv.2013.04.011] [PMID: 23643631]
[51]
Leeman, J.R.; Gilmore, T.D. Alternative splicing in the NF-κB signaling pathway. Gene, 2008, 423(2), 97-107.
[http://dx.doi.org/10.1016/j.gene.2008.07.015] [PMID: 18718859]
[52]
Calabrese, V.; Cornelius, C.; Dinkova-Kostova, A.T.; Calabrese, E.J. Vitagenes, cellular stress response, and acetylcarnitine: Relevance to hormesis. Biofactors, 2009, 35(2), 146-160.
[http://dx.doi.org/10.1002/biof.22] [PMID: 19449442]
[53]
Calabrese, V.; Cornelius, C.; Dinkova-Kostova, A.T.; Calabrese, E.J.; Mattson, M.P. Cellular stress responses, the hormesis paradigm, and vitagenes: novel targets for therapeutic intervention in neurodegenerative disorders. Antioxid. Redox Signal., 2010, 13(11), 1763-1811.
[http://dx.doi.org/10.1089/ars.2009.3074] [PMID: 20446769]
[54]
Azad, N.; Iyer, A.; Vallyathan, V.; Wang, L.; Castranova, V.; Stehlik, C.; Rojanasakul, Y. Role of oxidative/nitrosative stress‐mediated Bcl‐2 regulation in apoptosis and malignant transformation. Ann. N. Y. Acad. Sci., 2010, 1203(1), 1-6.
[http://dx.doi.org/10.1111/j.1749-6632.2010.05608.x] [PMID: 20716276]
[55]
Contestabile, A.; Ciani, E. Role of nitric oxide in the regulation of neuronal proliferation, survival and differentiation. Neurochem. Int., 2004, 45(6), 903-914.
[http://dx.doi.org/10.1016/j.neuint.2004.03.021] [PMID: 15312985]
[56]
Mungrue, I.N.; Bredt, D.S. nNOS at a glance: implications for brain and brawn. J. Cell Sci., 2004, 117(13), 2627-2629.
[http://dx.doi.org/10.1242/jcs.01187] [PMID: 15169833]
[57]
Choi, Y.B.; Tenneti, L.; Le, D.A.; Ortiz, J.; Bai, G.; Chen, H.S.V.; Lipton, S.A. Molecular basis of NMDA receptor-coupled ion channel modulation by S-nitrosylation. Nat. Neurosci., 2000, 3(1), 15-21.
[http://dx.doi.org/10.1038/71090] [PMID: 10607390]
[58]
Zhou, P.; Qian, L.; Iadecola, C. Nitric oxide inhibits caspase activation and apoptotic morphology but does not rescue neuronal death. J. Cereb. Blood Flow Metab., 2005, 25(3), 348-357.
[http://dx.doi.org/10.1038/sj.jcbfm.9600036] [PMID: 15660100]
[59]
Mancuso, C.; Bonsignore, A.; Di Stasio, E.; Mordente, A.; Motterlini, R. Bilirubin and S-nitrosothiols interaction: evidence for a possible role of bilirubin as a scavenger of nitric oxide. Biochem. Pharmacol., 2003, 66(12), 2355-2363.
[http://dx.doi.org/10.1016/j.bcp.2003.08.022] [PMID: 14637193]
[60]
Calabrese, V.; Butterfield, D.A.; Scapagnini, G.; Stella, A.M.G.; Maines, M.D. Redox regulation of heat shock protein expression by signaling involving nitric oxide and carbon monoxide: relevance to brain aging, neurodegenerative disorders, and longevity. Antioxid. Redox Signal., 2006, 8(3-4), 444-477.
[http://dx.doi.org/10.1089/ars.2006.8.444] [PMID: 16677090]
[61]
Calabrese, V.; Mancuso, C.; Calvani, M.; Rizzarelli, E.; Butterfield, D.A.; Giuffrida Stella, A.M. Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat. Rev. Neurosci., 2007, 8(10), 766-775.
[http://dx.doi.org/10.1038/nrn2214] [PMID: 17882254]
[62]
Chu, C.Y.; Chu, K.O.; Chan, J.Y.W.; Liu, X.Z.; Ho, C.S.; Wong, C.K.; Lau, C.M.; Ting, T.L.; Fok, T.F.; Fung, K.P.; Wang, C.C. Distribution of melamine in rat foetuses and neonates. Toxicol. Lett., 2010, 199(3), 398-402.
[http://dx.doi.org/10.1016/j.toxlet.2010.10.004] [PMID: 20934493]
[63]
Jingbin, W.; Ndong, M.; Kai, H.; Matsuno, K.; Kayama, F. Placental transfer of melamine and its effects on rat dams and fetuses. Food Chem. Toxicol., 2010, 48(7), 1791-1795.
[http://dx.doi.org/10.1016/j.fct.2010.03.043] [PMID: 20362637]
[64]
Sun, W.; Liu, P.; Tang, C.; An, L. Melamine disrupts acetylcholine-mediated neural information flow in the hippocampal CA3–CA1 pathway. Front. Behav. Neurosci., 2021, 15594907.
[http://dx.doi.org/10.3389/fnbeh.2021.594907] [PMID: 33679339]
[65]
An, L.; Zhang, T. Vitamins C and E reverse melamine-induced deficits in spatial cognition and hippocampal synaptic plasticity in rats. Neurotoxicology, 2014, 44, 132-139.
[http://dx.doi.org/10.1016/j.neuro.2014.06.009] [PMID: 24960222]
[66]
Zhang, H.; Wang, H.; Xiao, X.; Zhang, T. Melamine alters glutamatergic synaptic transmission of CA3-CA1 synapses presynaptically through autophagy activation in the rat hippocampus. Neurotox. Res., 2016, 29(1), 135-142.
[http://dx.doi.org/10.1007/s12640-015-9570-8] [PMID: 26530910]
[67]
Sun, W.; Li, X.; Tang, D.; Wu, Y.; An, L. Subacute melamine exposure disrupts task-based hippocampal information flow via inhibiting the subunits 2 and 3 of AMPA glutamate receptors expression. Hum. Exp. Toxicol., 2021, 40(6), 928-939.
[http://dx.doi.org/10.1177/0960327120975821] [PMID: 33243008]
[68]
Catterall, W.A. Cellular and molecular biology of voltage-gated sodium channels. Physiol. Rev., 1992, 72(4), S15-S48.
[http://dx.doi.org/10.1152/physrev.1992.72.suppl_4.S15] [PMID: 1332090]
[69]
Yao, H.; Zhao, D.; Khan, S.H.; Yang, L. Role of autophagy in prion protein-induced neurodegenerative diseases. Acta Biochim. Biophys. Sin. (Shanghai), 2013, 45(6), 494-502.
[http://dx.doi.org/10.1093/abbs/gmt022] [PMID: 23459558]
[70]
Iheanacho, S.C.; Igberi, C.; Amadi-Eke, A.; Chinonyerem, D.; Iheanacho, A.; Avwemoya, F. Biomarkers of neurotoxicity, oxidative stress, hepatotoxicity and lipid peroxidation in Clarias gariepinus exposed to melamine and polyvinyl chloride. Biomarkers, 2020, 25(7), 603-610.
[http://dx.doi.org/10.1080/1354750X.2020.1821777] [PMID: 32962424]
[71]
Wang, H.; Gao, N.; Li, Z.; Yang, Z.; Zhang, T. Autophagy alleviates melamine-induced cell death in PC12 cells via decreasing ROS level. Mol. Neurobiol., 2016, 53(3), 1718-1729.
[http://dx.doi.org/10.1007/s12035-014-9073-2] [PMID: 25724280]
[72]
Caccamo, A.; De Pinto, V.; Messina, A.; Branca, C.; Oddo, S. Genetic reduction of mammalian target of rapamycin ameliorates Alzheimer’s disease-like cognitive and pathological deficits by restoring hippocampal gene expression signature. J. Neurosci., 2014, 34(23), 7988-7998.
[http://dx.doi.org/10.1523/JNEUROSCI.0777-14.2014] [PMID: 24899720]
[73]
Xie, Z.; Klionsky, D.J. Autophagosome formation: core machinery and adaptations. Nat. Cell Biol., 2007, 9(10), 1102-1109.
[http://dx.doi.org/10.1038/ncb1007-1102] [PMID: 17909521]
[74]
Singh, R.; Xiang, Y.; Wang, Y.; Baikati, K.; Cuervo, A.M.; Luu, Y.K.; Tang, Y.; Pessin, J.E.; Schwartz, G.J.; Czaja, M.J. Autophagy regulates adipose mass and differentiation in mice. J. Clin. Invest., 2009, 119(11), 3329-3339.
[http://dx.doi.org/10.1172/JCI39228] [PMID: 19855132]
[75]
Ugland, H.; Naderi, S.; Brech, A.; Collas, P.; Blomhoff, H.K. cAMP induces autophagy via a novel pathway involving ERK, cyclin E and Beclin 1. Autophagy, 2011, 7(10), 1199-1211.
[http://dx.doi.org/10.4161/auto.7.10.16649] [PMID: 21750416]
[76]
Yu, L.; Chen, Y.; Tooze, S.A. Autophagy pathway: Cellular and molecular mechanisms. Autophagy, 2018, 14(2), 207-215.
[http://dx.doi.org/10.1080/15548627.2017.1378838] [PMID: 28933638]
[77]
Tanida, I.; Tanida-Miyake, E.; Ueno, T.; Kominami, E. The human homolog of Saccharomyces cerevisiae Apg7p is a Protein-activating enzyme for multiple substrates including human Apg12p, GATE-16, GABARAP, and MAP-LC3. J. Biol. Chem., 2001, 276(3), 1701-1706.
[http://dx.doi.org/10.1074/jbc.C000752200] [PMID: 11096062]
[78]
Mizushima, N.; Sugita, H.; Yoshimori, T.; Ohsumi, Y. A new protein conjugation system in human. The counterpart of the yeast Apg12p conjugation system essential for autophagy. J. Biol. Chem., 1998, 273(51), 33889-33892.
[http://dx.doi.org/10.1074/jbc.273.51.33889] [PMID: 9852036]

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