NMDA receptor-mediated excitotoxicity depends on the coactivation of synaptic and extrasynaptic receptors

Cell Death and Disease

Volumn 4, Issue 3, 2013, Pages

  Zhou, X ^a,b   Hollern, D ^a   Liao, J ^c   Andrechek, E ^a   Wang, H ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b NANJING MEDICAL UNIVERSITY   (China)

^c University of California Riverside   (United States)

Author keywords

Intracellular signaling; Microarray; NMDA receptor

Indexed keywords

BICUCULLINE; CASPASE 3; CYCLIC AMP; LACTATE DEHYDROGENASE; MEMANTINE; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTROPHIC FACTOR; SYNAPSE RECEPTOR; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; N METHYLASPARTIC ACID; NIFEDIPINE;

ANIMAL CELL; ARTICLE; BRAIN ISCHEMIA; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL DEATH; CELL FATE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; EXCITOTOXICITY; INTRACELLULAR SIGNALING; NERVE CELL NECROSIS; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; SHORT COURSE THERAPY; SYNAPTIC INHIBITION; SYNAPTOSOME; ANIMAL; BRAIN CORTEX; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; NERVE CELL; NEWBORN; PRIMARY CELL CULTURE; SPRAGUE DAWLEY RAT; SYNAPSE; SYNAPTIC TRANSMISSION;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; ANIMALS, NEWBORN; BICUCULLINE; CELL DEATH; CELL SURVIVAL; CEREBRAL CORTEX; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; MEMANTINE; N-METHYLASPARTATE; NEURONS; NIFEDIPINE; PRIMARY CELL CULTURE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC TRANSMISSION; TRANSCRIPTION, GENETIC;

EID: 84875889310     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.82     Document Type: Article

References (39)

1. Choi DW, Koh JY, Peters S. Pharmacology of glutamate neurotoxicity in cortical cell culture: attenuation by NMDA antagonists. J Neurosci 1988; 8: 185-196.
2. Villmann C, Becker CM. On the hypes and falls in neuroprotection: targeting the NMDA receptor. Neuroscientist 2007; 13: 594-615.
3. Benarroch EE. NMDA receptors: recent insights and clinical correlations. Neurology 2011; 76: 1750-1757.
4. Szydlowska K, Tymianski M. Calcium, ischemia and excitotoxicity. Cell Calcium 2010; 47: 122-129.
5. Harris AZ, Pettit DL. Extrasynaptic and synaptic NMDA receptors form stable and uniform pools in rat hippocampal slices. J Physiol 2007; 584: 509-519.
6. Thomas CG, Miller AJ, Westbrook GL. Synaptic and extrasynaptic NMDA receptor NR2 subunits in cultured hippocampal neurons. J Neurophysiol 2006; 95: 1727-1734.
7. Hardingham GE, Bading H. Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci 2010; 11: 682-696.
8. Hardingham GE, Fukunaga Y, Bading H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 2002; 5: 405-414.
9. Milnerwood AJ, Gladding CM, Pouladi MA, Kaufman AM, Hines RM, Boyd JD et al. Early increase in extrasynaptic NMDA receptor signaling and expression contributes to phenotype onset in Huntington's disease mice. Neuron 2010; 65: 178-190.
10. Harris AZ, Pettit DL. Recruiting extrasynaptic NMDA receptors augments synaptic signaling. J Neurophysiol 2008; 99: 524-533.
11. Fellin T, Pascual O, Gobbo S, Pozzan T, Haydon PG, Carmignoto G. Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 2004; 43: 729-743.
12. Li B, Chen N, Luo T, Otsu Y, Murphy TH, Raymond LA. Differential regulation of synaptic and extra-synaptic NMDA receptors. Nat Neurosci 2002; 5: 833-834.
13. Choi DW, Maulucci-Gedde M, Kriegstein AR. Glutamate neurotoxicity in cortical cell culture. J Neurosci 1987; 7: 357-368.
14. Friedman LK, Segal M. Early exposure of cultured hippocampal neurons to excitatory amino acids protects from later excitotoxicity. Int J Dev Neurosci 2010; 28: 195-205.
15. Ullian EM, Barkis WB, Chen S, Diamond JS, Barres BA. Invulnerability of retinal ganglion cells to NMDA excitotoxicity. Mol Cell Neurosci 2004; 26: 544-557.
16. Chen S, Diamond JS. Synaptically released glutamate activates extrasynaptic NMDA receptors on cells in the ganglion cell layer of rat retina. J Neurosci 2002; 22: 2165-2173.
17. Zhang J, Diamond JS. Distinct perisynaptic and synaptic localization of NMDA and AMPA receptors on ganglion cells in rat retina. J Comp Neurol 2006; 498: 810-820.
18. Chandler LJ, Sutton G, Dorairaj NR, Norwood D. N-methyl D-aspartate receptor-mediated bidirectional control of extracellular signal-regulated kinase activity in cortical neuronal cultures. J Biol Chem 2001; 276: 2627-2636.
19. Soriano FX, Papadia S, Hofmann F, Hardingham NR, Bading H, Hardingham GE. Preconditioning doses of NMDA promote neuroprotection by enhancing neuronal excitability. J Neurosci 2006; 26: 4509-4518.
20. Xiong ZG, Zhu XM, Chu XP, Minami M, Hey J, Wei WL et al. Neuroprotection in ischemia: blocking calcium-permeable acid-sensing ion channels. Cell 2004; 118: 687-698.
21. Sattler R, Tymianski M. Molecular mechanisms of glutamate receptor-mediated excitotoxic neuronal cell death. Mol Neurobiol 2001; 24: 107-129.
22. Avoli M, Hwa G, Louvel J, Kurcewicz I, Pumain R, Lacaille JC. Functional and pharmacological properties of GABA-mediated inhibition in the human neocortex. Can J Physiol Pharmacol 1997; 75: 526-534.
23. Bengtson CP, Dick O, Bading H. A quantitative method to assess extrasynaptic NMDA receptor function in the protective effect of synaptic activity against neurotoxicity. BMC Neurosci 2008; 9: 11.
24. Goldberg MP, Choi DW. Combined oxygen and glucose deprivation in cortical cell culture: calcium-dependent and calcium-independent mechanisms of neuronal injury. J Neurosci 1993; 13: 3510-3524.
25. McKeage K. Memantine: a review of its use in moderate to severe Alzheimer's disease. CNS Drugs 2009; 23: 881-897.
26. Xia P, Chen HS, Zhang D, Lipton SA. Memantine preferentially blocks extrasynaptic over synaptic NMDA receptor currents in hippocampal autapses. J Neurosci 2010; 30: 11246-11250.
27. Wroge CM, Hogins J, Eisenman L, Mennerick S. Synaptic NMDA receptors mediate hypoxic excitotoxic death. J Neurosci 2012; 32: 6732-6742.
28. Leveille F, El Gaamouch F, Gouix E, Lecocq M, Lobner D, Nicole O et al. Neuronal viability is controlled by a functional relation between synaptic and extrasynaptic NMDA receptors. FASEB J 2008; 22: 4258-4271.
29. Sattler R, Xiong Z, Lu WY, MacDonald JF, Tymianski M. Distinct roles of synaptic and extrasynaptic NMDA receptors in excitotoxicity. J Neurosci 2000; 20: 22-33.
30. Gao C, Gill MB, Tronson NC, Guedea AL, Guzman YF, Huh KH et al. Hippocampal NMDA receptor subunits differentially regulate fear memory formation and neuronal signal propagation. Hippocampus 2010; 20: 1072-1082.
31. Barry AE, Klyubin I, Mc Donald JM, Mably AJ, Farrell MA, Scott M et al. Alzheimer's disease brain-derived amyloid-beta-mediated inhibition of LTP in vivo is prevented by immunotargeting cellular prion protein. J Neurosci 2011; 31: 7259-7263.
32. Gouix E, Leveille F, Nicole O, Melon C, Had-Aissouni L, Buisson A. Reverse glial glutamate uptake triggers neuronal cell death through extrasynaptic NMDA receptor activation. Mol Cell Neurosci 2009; 40: 463-473.
33. Hong SJ, Li H, Becker KG, Dawson VL, Dawson TM. Identification and analysis of plasticity-induced late-response genes. Proc Natl Acad Sci USA 2004; 101: 2145-2150.
34. Zhang SJ, Steijaert MN, Lau D, Schutz G, Delucinge-Vivier C, Descombes P et al. Decoding NMDA receptor signaling: identification of genomic programs specifying neuronal survival and death. Neuron 2007; 53: 549-562.
35. Tovar KR, Westbrook GL. Mobile NMDA receptors at hippocampal synapses. Neuron 2002; 34: 255-264.
36. Groc L, Heine M, Cognet L, Brickley K, Stephenson FA, Lounis B et al. Differential activitydependent regulation of the lateral mobilities of AMPA and NMDA receptors. Nat Neurosci 2004; 7: 695-696.
37. Kohr G. NMDA receptor function: subunit composition versus spatial distribution. Cell Tissue Res 2006; 326: 439-446.
38. Gladding CM, Raymond LA. Mechanisms underlying NMDA receptor synaptic/extrasynaptic distribution and function. Mol Cell Neurosci 2011; 48: 308-320.
39. Zhou X, Moon C, Zheng F, Luo Y, Soellner D, Nunez JL et al. N-methyl-D-aspartatestimulated ERK1/2 signaling and the transcriptional up-regulation of plasticity-related genes are developmentally regulated following in vitro neuronal maturation. J Neurosci Res 2009; 87: 2632-2644.