Glutamate excitotoxicity activates the MAPK/ERK signaling pathway and induces the survival of rat hippocampal neurons in vivo

Journal of Molecular Neuroscience

Volumn 52, Issue 3, 2014, Pages 366-377

  Ortuño Sahagún, Daniel ^a   González, Raúl Montes ^b   Verdaguer, Ester ^c   Huerta, Verónica Chaparro ^b   Torres Mendoza, Blanca M ^a   Lemus, Lourdes ^d   Rivera Cervantes, Martha Catalina ^a   Camins, A ^c   Zárate, C Beas ^a,b  

^a UNIVERSITY OF GUADALAJARA   (Mexico)

^b INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^c UNIVERSITY OF BARCELONA   (Spain)

^d HOSPITAL DE PEDIATRÍA   (Mexico)

Author keywords

Glutamate; Hippocampus; MAPK ERK; Neuroprotection; Neurotoxicity

Indexed keywords

ACTION POTENTIALS; ANIMALS; CA1 REGION, HIPPOCAMPAL; CELL SURVIVAL; CELLS, CULTURED; GLUTAMIC ACID; MAP KINASE SIGNALING SYSTEM; NEURONS; RATS; RATS, WISTAR;

EID: 84894334326     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-013-0157-7     Document Type: Article

References (66)

1. Akhtar RS, Ness JM, Roth KA (2004) Bcl-2 family regulation of neuronal development and neurodegeneration. Biochim Biophys Acta 1644:189-203
2. Almeida RD, Manadas BJ, Melo CV et al (2005) Neuroprotection by BDNF against glutamate-induced apoptotic cell death is mediated by ERK and PI3-kinase pathways. Cell Death Differ 12:1329-1343
3. Anderson CN, Tolkovsky AM (1999) A role for MAPK/ERK in sympathetic neuron survival: protection against a p53-dependent, JNK-independent induction of apoptosis by cytosine arabinoside. J Neurosci 19:664-673
4. André VM, Cepeda C, Levine MS (2010) Dopamine and glutamate in Huntington's disease: a balancing act. CNS Neurosci Ther 16:163-178
5. Asomugha CO, Linn DM, Linn CL (2010) ACh receptors link two signaling pathways to neuroprotection against glutamate-induced excitotoxicity in isolated RGCs. J Neurochem 112:214-226
6. Babai N, Atlasz T, Tamás A et al (2006) Search for the optimal monosodium glutamate treatment schedule to study the neuroprotective effects of PACAP in the retina. Ann NY Acad Sci 1070:149-155
7. Barnes JW, Tischkau SA, Barnes JA et al (2003) Requirement of mammalian timeless for circadian rhythmicity. Science 302:439-442
8. Beas-Zárate C, Schliebs R, Ortuño-Sahagún D, Morales-Villagrán A, Feria-Velasco A (1994) Effect of systemic monosodium l-glutamate on muscarinic cholinergic receptors in selected rat brain regions during development. Arch Med Res 25:341-346
9. Berkeley JL, Decker MJ, Levey AI (2002) The role of muscarinic acetylcholine receptor-mediated activation of extracellular signal-regulated kinase 1/2 in pilocarpine-induced seizures. J Neurochem 82:192-201
10. Boscia F, Esposito CL, Di Crisci A, de Franciscis V, Annunziato L, Cerchia L (2009) GDNF selectively induces microglial activation and neuronal survival in CA1/CA3 hippocampal regions exposed to NMDA insult through Ret/ERK signalling. PLoS One 4:e6486
11. Chen T, Cao L, Dong W et al (2012) Protective effects of mGluR5 positive modulators against traumatic neuronal injury through PKC-dependent activation of MEK/ERK pathway. Neurochem Res 37:983-990
12. Cortese BM, Phan KL (2005) The role of glutamate in anxiety and related disorders. CNS Spectr 10:820-830
13. Dhandapani KM, Wade FM, Wakade C, Mahesh VB, Brann DW (2005) Neuroprotection by stem cell factor in rat cortical neurons involves AKT and NFkappaB. J Neurochem 95:9-19
14. Dong M, Wu Y, Fan Y, Xu M, Zhang J (2006) c-fos modulates brain-derived neurotrophic factor mRNA expression in mouse hippocampal CA3 and dentate gyrus neurons. Neurosci Lett 400:177-180
15. Dong X-X, Wang Y, Qin Z-H (2009) Molecular mechanisms of excitotoxicity and their relevance to pathogenesis of neurodegenerative diseases. Acta Pharmacol Sinica 30:379-387
16. Duncia JV, Santella JB 3rd, Higley CA et al (1998) MEK inhibitors: the chemistry and biological activity of U0126, its analogs, and cyclization products. Bioorg Med Chem Lett 8:2839-2844
17. Esposito E, Cuzzocrea S (2010) New therapeutic strategy for Parkinson's and Alzheimer's disease. Curr Med Chem 17:2764-2774
18. Feng H, Xiang H, Mao YW et al (2004) Human Bcl-2 activates ERK signaling pathway to regulate activating protein-1, lens epithelium-derived growth factor and downstream genes. Oncogene 23:7310-7321
19. Ferrer I, Blanco R, Carmona M (2001) Differential expression of active, phosphorylation-dependent MAP kinases, MAPK/ERK, SAPK/JNK and p38, and specific transcription factor substrates following quinolinic acid excitotoxicity in the rat. Brain Res Mol Brain Res 94:48-58
20. Ferrer I, Blanco R, Carmona M, Puig B, Domínguez I, Viñals F (2002) Active, phosphorylation-dependent MAP kinases, MAPK/ERK, SAPK/JNK and p38, and specific transcription factor substrates are differentially expressed following systemic administration of kainic acid to the adult rat. Acta Neuropathol 103:391-407
21. Giovannini MG, Cerbai F, Bellucci A et al (2008) Differential activation of mitogen-activated protein kinase signalling pathways in the hippocampus of CRND8 transgenic mouse, a model of Alzheimer's disease. Neuroscience 153:618-633
22. Gladding CM, Fitzjohn SM, Molnár E (2009) Metabotropic glutamate receptor-mediated long-term depression: molecular mechanisms. Pharmacol Rev 61:395-412
23. Grewer C, Gameiro A, Zhang Z, Tao Z, Braams S, Rauen T (2008) Glutamate forward and reverse transport: from molecular mechanism to transporter-mediated release after ischemia. IUBMB Life 60:609-619
24. Hetman M, Kanning K, Cavanaugh JE, Xia Z (1999) Neuroprotection by brain-derived neurotrophic factor is mediated by extracellular signal-regulated kinase and phosphatidylinositol 3-kinase. J Biol Chem 274:22569-22580
25. Hetman M, Gozdz A (2004) Role of extracellular signal regulated kinases 1 and 2 in neuronal survival. Eur J Biochem 271:2050-2055
26. Jiang X, Zhu D, Okagaki P et al (2003) N-methyl-d-aspartate and TrkB receptor activation in cerebellar granule cells: an in vitro model of preconditioning to stimulate intrinsic survival pathways in neurons. Ann N Y Acad Sci 993:134-145
27. Karmarkar SW, Bottum KM, Krager SL, Tischkau SA (2011) ERK/MAPK is essential for endogenous neuroprotection in SCN2.2 cells. PLoS One 6:e23493
28. Kew JN, Kemp JA (2005) Ionotropic and metabotropic glutamate receptor structure and pharmacology. Psychopharmacol (Berl) 179:4-29
29. Kim EK, Choi E-J (2010) Pathological roles of MAPK signaling pathways in human diseases. Biochim Biophys Acta 1802:396-405
30. Kullmann DM, Lamsa K (2008) Roles of distinct glutamate receptors in induction of anti-Hebbian long-term potentiation. J Physiol 586:1481-1486
31. Lau A, Tymianski M (2010) Glutamate receptors, neurotoxicity and neurodegeneration. Pflugers Arch 460:525-542. doi: 10.1007/s00424-010-0809-1
32. Lee HG, Zhu X, O'Neill MJ et al (2004) The role of metabotropic glutamate receptors in Alzheimer's disease. Acta Neurobiol Exp (Wars) 64:89-98
33. Lei K, Davis RJ (2003) JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc Natl Acad Sci U S A 100:2432-2437. doi: 10.1073/pnas.0438011100
34. Ma Y, Liu W, Wang Y et al (2011) VEGF protects rat cortical neurons from mechanical trauma injury induced apoptosis via the MEK/ERK pathway. Brain Res Bull 86:441-446
35. Maiese K, Chong ZZ, Li F (2005) Driving cellular plasticity and survival through the signal transduction pathways of metabotropic glutamate receptors. Curr Neurovasc Res 2:425-446
36. Malik SZ, Motamedi S, Royo NC, LeBold D, Watson DJ (2011) Identification of potentially neuroprotective genes upregulated by neurotrophin treatment of CA3 neurons in the injured brain. J Neurotrauma 28:415-430
37. Matsuzaki H, Tamatani M, Yamaguchi A et al (2001) Vascular endothelial growth factor rescues hippocampal neurons from glutamate-induced toxicity: signal transduction cascades. FASEB J 15:1218-1220
38. Melo CV, Okumoto S, Gomes JR et al (2013) Spatiotemporal resolution of BDNF neuroprotection against glutamate excitotoxicity in cultured hippocampal neurons. Neuroscience 237:66-86
39. Naoi M, Maruyama W (2010) Monoamine oxidase inhibitors as neuroprotective agents in age-dependent neurodegenerative disorders. Curr Pharm Des 16:2799-2817
40. Numakawa T, Suzuki S, Kumamaru E, Adachi N, Richards M, Kunugi H (2010) BDNF function and intracellular signaling in neurons. Histol Histopathol 25:237-258
41. O'Sullivan AW, Wang JH, Redmond HP (2009) p38 MAP kinase inhibition promotes primary tumour growth via VEGF independent mechanism. World J Surg Oncol 7:89
42. Ortega F, Pérez-Sen R, Delicado EG, Teresa M-PM (2011) ERK1/2 activation is involved in the neuroprotective action of P2Y13 and P2X7 receptors against glutamate excitotoxicity in cerebellar granule neurons. Neuropharmacol 61:1210-1221
43. Ortuño-Sahagún D, Beas-Zárate C, Adame-Gonzalez G, Feria-Velasco A (1997) Effect of l-glutamate on cholinergic neurotransmission in various brain regions and during the development of rats, when administered perinatally. Neurochem Int 31:683-692
44. Ortuño-Sahagún D, Rivera-Cervantes MC, Gudino-Cabrera G et al (2010) Microarray analysis of rat hippocampus exposed to excitotoxicity: reversal Na(+)/Ca(2+) exchanger NCX3 is overexpressed in glial cells. Hippocampus 22:128-140
45. Park MA, Zhang G, Mitchell C et al (2008) Mitogen-activated protein kinase kinase 1/2 inhibitors and 17-allylamino-17-demethoxygeldanamycin synergize to kill human gastrointestinal tumor cells in vitro via suppression of c-FLIP-s levels and activation of CD95. Mol Cancer Ther 7:2633-2648
46. Paschen W (1996) Glutamate excitotoxicity in transient global cerebral ischemia. Acta Neurobiol Exp (Wars) 56:313-322
47. Peng CH, Chiou SH, Chen SJ et al (2008) Neuroprotection by imipramine against lipopolysaccharide-induced apoptosis in hippocampus-derived neural stem cells mediated by activation of BDNF and the MAPK pathway. Eur Neuropsychopharmacol 18:128-140
48. Petegnief V, Saura J, de Gregorio-Rocasolano N, Paul SM (2001) Neuronal injury-induced expression and release of apolipoprotein E in mixed neuron/glia co-cultures: nuclear factor kappaB inhibitors reduce basal and lesion-induced secretion of apolipoprotein E. Neuroscience 104:223-234
49. Rogers A, Schmuck G, Scholz G, Williams DC (2004) c-fos mRNA expression in rat cortical neurons during glutamate-mediated excitotoxicity. Toxicol Sci 82:562-569
50. Sahota P, Savitz SI (2011) Investigational therapies for ischemic stroke: neuroprotection and neurorecovery. Neurotherapeutics 8:434-451
51. Sánchez A, Tripathy D, Yin X, Luo J, Martínez J, Grammas P (2012) Pigment epithelium-derived factor (PEDF) protects cortical neurons in vitro from oxidant injury by activation of extracellular signal-regulated kinase (ERK) 1/2 and induction of Bcl-2. Neurosci Res 72:1-8
52. Satoh T, Nakatsuka D, Watanabe Y, Nagata I, Kikuchi H, Namura S (2000) Neuroprotection by MAPK/ERK kinase inhibition with U0126 against oxidative stress in a mouse neuronal cell line and rat primary cultured cortical neurons. Neurosci Lett 288:163-166
53. Schousboe A, Waagepetersen HS (2005) Role of astrocytes in glutamate homeostasis: implications for excitotoxicity. Neurotox Res 8:221-225
54. Segura Torres JE, Chaparro-Huerta V, Rivera Cervantes MC, Montes-González R, Flores Soto ME, Beas-Zárate C (2006) Neuronal cell death due to glutamate excitotoxicity is mediated by p38 activation in the rat cerebral cortex. Neurosci Lett 403:233-238
55. Son TG, Park HR, Kim SJ et al (2009) Senescence marker protein 30 is up-regulated in kainate-induced hippocampal damage through ERK-mediated astrocytosis. J Neurosci Res 87:2890-2897
56. Thangavelu K, Pan CQ, Karlberg T et al (2012) Structural basis for the allosteric inhibitory mechanism of human kidney-type glutaminase (KGA) and its regulation by Raf-Mek-Erk signaling in cancer cell metabolism. Proc Natl Acad Sci U S A 109:7705-7710
57. Tischkau SA, Gallman EA, Buchanan GF, Gillette MU (2000) Differential cAMP gating of glutamatergic signaling regulates long-term state changes in the suprachiasmatic circadian clock. J Neurosci 20:7830-7837
58. Verheij M, Ruiter GA, Zerp SF et al (1998) The role of the stress-activated protein kinase (SAPK/JNK) signaling pathway in radiation-induced apoptosis. Radiother Oncol 47:225-232
59. Wang CX, Song JH, Song DK, Yong VW, Shuaib A, Hao C (2006) Cyclin-dependent kinase-5 prevents neuronal apoptosis through ERK-mediated upregulation of Bcl-2. Cell Death Differ 13:1203-1212
60. Wang X, Zhu G, Yang S et al (2011) Paeonol prevents excitotoxicity in rat pheochromocytoma PC12 cells via downregulation of ERK activation and inhibition of apoptosis. Planta Med 77:1695-1701
61. Wang Y, Qin ZH (2010) Molecular and cellular mechanisms of excitotoxic neuronal death. Apoptosis 15:1382-1402
62. 2+ influx via l-type calcium channels activates the Src/ERK/cyclic-AMP response element binding protein signal pathway and Bcl-2 expression in rat hippocampal neurons: a potential initiation mechanism for estrogen-induced neuroprotection. Neuroscience 135:59-72
63. Yoon CH, Kim MJ, Park MT et al (2009) Activation of p38 mitogen-activated protein kinase is required for death receptor-independent caspase-8 activation and cell death in response to sphingosine. Mol Cancer Res 7:361-370
64. Zachary I (2005) Neuroprotective role of vascular endothelial growth factor: signalling mechanisms, biological function, and therapeutic potential. Neurosignals 14:207-221
65. Zhang J, Zhang D, McQuade JS, Behbehani M, Tsien JZ, Xu M (2002) c-fos regulates neuronal excitability and survival. Nat Genet 30:416-420
66. Zhu X, Lee H-G, Raina AK, Perry G, Smith MA (2003) The role of mitogen-activated protein kinase pathways in Alzheimer's disease. Neurosignals 11:270-281