Rapamycin Effectively Impedes Melamine-Induced Impairments of Cognition and Synaptic Plasticity in Wistar Rats

Molecular Neurobiology

Volumn 54, Issue 2, 2017, Pages 819-832

  Fu, Jingxuan ^a   Wang, Hui ^a   Gao, Jing ^a   Yu, Mei ^a   Wang, Rubin ^b   Yang, Zhuo ^a   Zhang, Tao ^a  

^a NANKAI UNIVERSITY   (China)

^b EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Depotentiation; LTP; Melamine; Oxidative stress; Rapamycin; Rats

Indexed keywords

BECLIN 1; CASPASE 3; MALONALDEHYDE; MELAMINE; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN LIGHT CHAIN 3; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; POSTSYNAPTIC DENSITY PROTEIN 95; RAPAMYCIN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; TRIAZINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; COGNITIVE DEFECT; CONTROLLED STUDY; DEPTH PERCEPTION; ENZYME ACTIVITY; HIPPOCAMPUS; LEARNING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MORRIS WATER MAZE TEST; NERVE CELL; NERVE CELL PLASTICITY; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; RAT; SPATIAL LEARNING; TREATMENT DURATION; ANIMAL; CHEMICALLY INDUCED; DRUG EFFECTS; MAZE TEST; METABOLISM; PHYSIOLOGY; TREATMENT OUTCOME; WISTAR RAT;

ANIMALS; COGNITION DISORDERS; MALE; MAZE LEARNING; NEURONAL PLASTICITY; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; SIROLIMUS; TREATMENT OUTCOME; TRIAZINES;

EID: 84954419716     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-016-9687-7     Document Type: Article

References (64)

1. Han YG, Liu SC, Zhang T, Yang Z (2011) Induction of apoptosis by melamine in differentiated PC12 cells. Cell Mol Neurobiol 31(1):65–71. doi:10.1007/s10571-010-9554-4
2. Wang Y, Liu F, Wei Y, Liu D (2011) The effect of exogenous melamine on rat hippocampal neurons. Toxicol Ind Health 27:571–576
3. Yang J, An L, Yao Y, Yang Z, Zhang T (2011) Melamine impairs spatial cognition and hippocampal synaptic plasticity by presynaptic inhibition of glutamatergic transmission in infant rats. Toxicology 289(2–3):167–174. doi:10.1016/j.tox.2011.08.011
4. Yang JJ, Tian YT, Yang Z, Zhang T (2010) Effect of melamine on potassium currents in rat hippocampal CA1 neurons. Toxicol in Vitro 24(2):397–403. doi:10.1016/j.tiv.2009.10.019
5. Yang JJ, Yang Z, Zhang T (2010) Action potential changes associated with impairment of functional properties of sodium channels in hippocampal neurons induced by melamine. Toxicol Lett 198(2):171–176
6. Wu YT, Huang CM, Lin CC, Ho WA, Lin LC, Chiu TF, Tarng DC, Lin CH et al (2009) Determination of melamine in rat plasma, liver, kidney, spleen, bladder and brain by liquid chromatography-tandem mass spectrometry. J Chromatogr A 1216(44):7595–7601
7. An L, Li Z, Yang Z, Zhang T (2011) Cognitive deficits induced by melamine in rats. Toxicol Lett 206(3):276–280. doi:10.1016/j.toxlet.2011.08.009
8. An L, Yang Z, Zhang T (2013) Melamine induced spatial cognitive deficits associated with impairments of hippocampal long-term depression and cholinergic system in Wistar rats. Neurobiol Learn Mem 100:18–24. doi:10.1016/j.nlm.2012.12.003
9. Ma C, Kang H, Liu Q, Zhu R, Cao Z (2011) Insight into potential toxicity mechanisms of melamine: an in silico study. Toxicology 283(2–3):96–100. doi:10.1016/j.tox.2011.02.009
10. Guo C, He Z, Wen L, Zhu L, Lu Y, Deng S, Yang Y, Wei Q et al (2012) Cytoprotective effect of trolox against oxidative damage and apoptosis in the NRK-52e cells induced by melamine. Cell Biol Int 36(2):183–188. doi:10.1042/CBI20110036
11. An L, Li Z, Zhang T (2014) Reversible effects of vitamins C and E combination on oxidative stress-induced apoptosis in melamine-treated PC12 cells. Free Radic Res 48(2):239–250. doi:10.3109/10715762.2013.861598
12. Kemp A, Manahan-Vaughan D (2007) Hippocampal long-term depression: master or minion in declarative memory processes? Trends Neurosci 30(3):111–118. doi:10.1016/j.tins.2007.01.002
13. Kulla A, Reymann KG, Manahan-Vaughan D (1999) Time-dependent induction of depotentiation in the dentate gyrus of freely moving rats: involvement of group 2 metabotropic glutamate receptors. Eur J Neurosci 11(11):3864–3872. doi:10.1046/j.1460-9568.1999.00807.x
14. Huang YZ, Rothwell JC, Lu CS, Chuang WL, Lin WY, Chen RS (2010) Reversal of plasticity-like effects in the human motor cortex. J Physiol 588(Pt 19):3683–3693. doi:10.1113/jphysiol.2010.191361
15. Citri A, Malenka RC (2008) Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 33(1):18–41. doi:10.1038/sj.npp.1301559
16. Ehrlich I, Klein M, Rumpel S, Malinow R (2007) PSD-95 is required for activity-driven synapse stabilization. Proc Natl Acad Sci U S A 104(10):4176–4181. doi:10.1073/pnas.0609307104
17. Li J, Kim SG, Blenis J (2014) Rapamycin: one drug, many effects. Cell Metab 19(3):373–379. doi:10.1016/j.cmet.2014.01.001
18. Martinez-Vicente M, Talloczy Z, Kaushik S, Massey AC, Mazzulli J, Mosharov EV, Hodara R, Fredenburg R et al (2008) Dopamine-modified alpha-synuclein blocks chaperone-mediated autophagy. J Clin Invest 118(2):777–788. doi:10.1172/JCI32806
19. Caccamo A, Majumder S, Richardson A, Strong R, Oddo S (2010) Molecular interplay between mammalian target of rapamycin (mTOR), amyloid-beta, and Tau: effects on cognitive impairments. J Biol Chem 285(17):13107–13120. doi:10.1074/jbc.M110.100420
20. Lipton JO, Sahin M (2014) The neurology of mTOR. Neuron 84(2):275–291. doi:10.1016/j.neuron.2014.09.034
21. Glick D, Barth S, Macleod KF (2010) Autophagy: cellular and molecular mechanisms. J Pathol 221(1):3–12. doi:10.1002/path.2697
22. Levine B, Yuan J (2005) Autophagy in cell death: an innocent convict? J Clin Invest 115(10):2679–2688. doi:10.1172/JCI26390
23. Carloni S, Buonocore G, Balduini W (2008) Protective role of autophagy in neonatal hypoxia-ischemia induced brain injury. Neurobiol Dis 32(3):329–339. doi:10.1016/j.nbd.2008.07.022
24. Pimplikar SW, Nixon RA, Robakis NK, Shen J, Tsai LH (2010) Amyloid-independent mechanisms in Alzheimer’s disease pathogenesis. J Neurosci 30(45):14946–14954. doi:10.1523/JNEUROSCI.4305-10.2010
25. Lin MT, Beal MF (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443(7113):787–795. doi:10.1038/nature05292
26. Knecht E, Criado-Garcia O, Aguado C, Gayarre J, Duran-Trio L, Garcia-Cabrero AM, Vernia S, San Millan B et al (2012) Malin knockout mice support a primary role of autophagy in the pathogenesis of Lafora disease. Autophagy 8(4):701–703. doi:10.4161/auto.19522
27. Li L, Ishdorj G, Gibson SB (2012) Reactive oxygen species regulation of autophagy in cancer: implications for cancer treatment. Free Radic Biol Med 53(7):1399–1410. doi:10.1016/j.freeradbiomed.2012.07.011
28. Azad MB, Chen Y, Gibson SB (2009) Regulation of autophagy by reactive oxygen species (ROS): implications for cancer progression and treatment. Antioxid Redox Signal 11(4):777–790. doi:10.1089/ARS.2008.2270
29. Wang H, Gao N, Li Z, Yang Z, Zhang T (2015) Autophagy alleviates melamine-induced cell death in PC12 cells via decreasing ROS level. Mol Neurobiol. doi:10.1007/s12035-014-9073-2
30. Han G, An L, Yang B, Si L, Zhang T (2014) Nicotine-induced impairments of spatial cognition and long-term potentiation in adolescent male rats. Hum Exp Toxicol 33(2):203–213. doi:10.1177/0960327113494902
31. An L, Yang Z, Zhang T (2013) Imbalanced synaptic plasticity induced spatial cognition impairment in male offspring rats treated with chronic prenatal ethanol exposure. Alcohol Clin Exp Res 37(5):763–770
32. Tang G, Gudsnuk K, Kuo SH, Cotrina ML, Rosoklija G, Sosunov A, Sonders MS, Kanter E et al (2014) Loss of mTOR-dependent macroautophagy causes autistic-like synaptic pruning deficits. Neuron 83(5):1131–1143. doi:10.1016/j.neuron.2014.07.040
33. An L, Zhang T (2014) Vitamins C and E reverse melamine-induced deficits in spatial cognition and hippocampal synaptic plasticity in rats. Neurotoxicology 44:132–139. doi:10.1016/j.neuro.2014.06.009
34. Yu M, Zhang Y, Chen X, Zhang T (2015) Antidepressant-like effects and possible mechanisms of amantadine on cognitive and synaptic deficits in depression rats. Stress. doi:10.3109/10253890.2015.1108302
35. Liu C, Xu X, Gao J, Zhang T, Yang Z (2015) Hydrogen sulfide prevents synaptic plasticity from VD-induced damage via Akt/GSK-3beta pathway and notch signaling pathway in rats. Mol Neurobiol. doi:10.1007/s12035-015-9324-x
36. Vorhees CV, Williams MT (2006) Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1(2):848–858. doi:10.1038/nprot.2006.116
37. An L, Li Z, Yang Z, Zhang T (2012) Melamine induced cognitive impairment associated with oxidative damage in rat’s hippocampus. Pharmacol Biochem Behav 102(2):196–202. doi:10.1016/j.pbb.2012.04.009
38. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361(6407):31–39. doi:10.1038/361031a0
39. Qi Y, Hu NW, Rowan MJ (2013) Switching off LTP: mGlu and NMDA receptor-dependent novelty exploration-induced depotentiation in the rat hippocampus. Cereb Cortex 23(4):932–939. doi:10.1093/cercor/bhs086
40. Li B, Otsu Y, Murphy TH, Raymond LA (2003) Developmental decrease in NMDA receptor desensitization associated with shift to synapse and interaction with postsynaptic density-95. J Neurosci 23(35):11244–11254
41. Yao H, Zhao D, Khan SH, Yang L (2013) Role of autophagy in prion protein-induced neurodegenerative diseases. Acta Biochim Biophys Sin 45(6):494–502. doi:10.1093/abbs/gmt022
42. Mizushima N (2007) Autophagy: process and function. Genes Dev 21(22):2861–2873. doi:10.1101/gad.1599207
43. McCormack FX, Inoue Y, Moss J, Singer LG, Strange C, Nakata K, Barker AF, Chapman JT et al (2011) Efficacy and safety of sirolimus in lymphangioleiomyomatosis. N Engl J Med 364(17):1595–1606. doi:10.1056/NEJMoa1100391
44. Sahin M (2012) Targeted treatment trials for tuberous sclerosis and autism: no longer a dream. Curr Opin Neurobiol 22(5):895–901. doi:10.1016/j.conb.2012.04.008
45. Franz DN (2013) Everolimus in the treatment of subependymal giant cell astrocytomas, angiomyolipomas, and pulmonary and skin lesions associated with tuberous sclerosis complex. Biologics: targets & therapy 7:211–221. doi:10.2147/BTT.S25095
46. Ehninger D, Han S, Shilyansky C, Zhou Y, Li W, Kwiatkowski DJ, Ramesh V, Silva AJ (2008) Reversal of learning deficits in a Tsc2+/− mouse model of tuberous sclerosis. Nat Med 14(8):843–848. doi:10.1038/nm1788
47. Caccamo A, De Pinto V, Messina A, Branca C, Oddo S (2014) Genetic reduction of mammalian target of rapamycin ameliorates Alzheimer’s disease-like cognitive and pathological deficits by restoring hippocampal gene expression signature. J Neurosci 34(23):7988–7998. doi:10.1523/JNEUROSCI.0777-14.2014
48. Pryor WM, Biagioli M, Shahani N, Swarnkar S, Huang WC, Page DT, MacDonald ME, Subramaniam S (2014) Huntingtin promotes mTORC1 signaling in the pathogenesis of Huntington’s disease. Sci Signal 7(349), ra103. doi:10.1126/scisignal.2005633
49. Nikoletopoulou V, Papandreou ME, Tavernarakis N (2015) Autophagy in the physiology and pathology of the central nervous system. Cell Death Differ 22(3):398–407. doi:10.1038/cdd.2014.204
50. Li L, Zhang Q, Tan J, Fang Y, An X, Chen B (2014) Autophagy and hippocampal neuronal injury. Sleep Breath = Schlaf & Atmung 18(2):243–249. doi:10.1007/s11325-013-0930-4
51. Chen Q, Niu Y, Zhang R, Guo H, Gao Y, Li Y, Liu R (2010) The toxic influence of paraquat on hippocampus of mice: involvement of oxidative stress. Neurotoxicology 31(3):310–316. doi:10.1016/j.neuro.2010.02.006
52. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M et al (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441(7095):880–884. doi:10.1038/nature04723
53. Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, Scaravilli F, Easton DF et al (2004) Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 36(6):585–595. doi:10.1038/ng1362
54. Milisav I, Suput D, Ribaric S (2015) Unfolded protein response and macroautophagy in Alzheimer’s, Parkinson’s and prion diseases. Molecules 20(12):22718–22756. doi:10.3390/molecules201219865
55. Mizushima N, Komatsu M (2011) Autophagy: renovation of cells and tissues. Cell 147(4):728–741. doi:10.1016/j.cell.2011.10.026
56. Sarkar S, Ravikumar B, Floto RA, Rubinsztein DC (2009) Rapamycin and mTOR-independent autophagy inducers ameliorate toxicity of polyglutamine-expanded huntingtin and related proteinopathies. Cell Death Differ 16(1):46–56. doi:10.1038/cdd.2008.110
57. Fagundes LS, Fleck AD, Zanchi AC, Saldiva PH, Rhoden CR (2015) Direct contact with particulate matter increases oxidative stress in different brain structures. Inhalation toxicology. 1–6. doi:10.3109/08958378.2015.1060278
58. Haorah J, Ramirez SH, Floreani N, Gorantla S, Morsey B, Persidsky Y (2008) Mechanism of alcohol-induced oxidative stress and neuronal injury. Free Radic Biol Med 45(11):1542–1550. doi:10.1016/j.freeradbiomed.2008.08.030
59. Lemasters JJ (2005) Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging. Rejuvenation Res 8(1):3–5. doi:10.1089/rej.2005.8.3
60. Yuan Y, Zhang X, Zheng Y, Chen Z (2015) Regulation of mitophagy in ischemic brain injury. Neurosci Bull 31(4):395–406. doi:10.1007/s12264-015-1544-6
61. Thanan R, Oikawa S, Hiraku Y, Ohnishi S, Ma N, Pinlaor S, Yongvanit P, Kawanishi S et al (2015) Oxidative stress and its significant roles in neurodegenerative diseases and cancer. Int J Mol Sci 16(1):193–217. doi:10.3390/ijms16010193
62. Kamalinia G, Khodagholi F, Atyabi F, Amini M, Shaerzadeh F, Sharifzadeh M, Dinarvand R (2013) Enhanced brain delivery of deferasirox-lactoferrin conjugates for iron chelation therapy in neurodegenerative disorders: in vitro and in vivo studies. Mol Pharm 10(12):4418–4431. doi:10.1021/mp4002014
63. Riedl SJ, Shi Y (2004) Molecular mechanisms of caspase regulation during apoptosis. Nat Rev Mol Cell Biol 5(11):897–907. doi:10.1038/nrm1496
64. Tang SJ, Reis G, Kang H, Gingras AC, Sonenberg N, Schuman EM (2002) A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc Natl Acad Sci U S A 99(1):467–472. doi:10.1073/pnas.012605299