This Article Abstract Free Full Text (Free PDF) Free Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Add to Saved Citations Download to citation manager Request Permissions Request Reprints Add to My Marked Citations Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (17) Citing Articles via Google Scholar Citing Articles via Scopus Google Scholar Articles by Papadia, S. Articles by Hardingham, G. E. Search for Related Content PubMed PubMed Citation Articles by Papadia, S. Articles by Hardingham, G. E. Social Bookmarking                         What's this?

The Dichotomy of NMDA Receptor Signaling

Centre for Neuroscience Research, University of Edinburgh, Edinburgh, United Kingdom

Giles E. Hardingham

Centre for Neuroscience Research, University of Edinburgh, Edinburgh, United Kingdom, Giles.Hardingham{at}ed.ac.uk

The N-methyl-D-aspartate (NMDA) subtype of ionotropic glutamate receptors plays a Jekyll and Hyde role in the mammalian central nervous system. In pathological scenarios such as ischemia, Ca²⁺ influx through the NMDA receptor is a key mediator of cell death. However, physiological levels of NMDA-receptor activity can promote neuronal survival and resistance to trauma and play important roles in synaptic plasticity and transmission. This dichotomy may explain the poor tolerance and efficacy of NMDA-receptor antagonists in clinical trials for excitotoxic trauma. There is a growing understanding of the signaling events that mediate the opposing effects of NMDA-receptor activity and the factors that determine whether an episode of NMDA-receptor activity will promote survival or death. This knowledge may lead to therapeutic strategies that enable the selective blockade of prodeath signaling cassettes while sparing physiological signaling to survival and plasticity. NEUROSCIENTIST 13(6):572—579, 2007. DOI: 10.1177/1073858407305833

Key Words: Apoptosis • Necrosis • Neuroprotection • Stroke • NMDA receptor • Extrasynaptic • Synaptic activity • CREB • Akt • Calcium

References

• Aamodt SM, Constantine-Paton M. 1999. The role of neural activity in synaptic development and its implications for adult brain function. Adv Neurol 79:133-44.[Medline] [Order article via Infotrieve]
• Aarts M., Iihara K., Wei WL, Xiong ZG, Arundine M., Cerwinski W., and others. 2003. A key role for TRPM7 channels in anoxic neuronal death. Cell 115(7):863-77.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Aarts M., Liu Y., Liu L., Besshoh S., Arundine M., Gurd JW, and others. 2002. Treatment of ischemic brain damage by perturbing NMDA receptor- PSD-95 protein interactions. Science 298(5594):846-50.[Abstract/Free Full Text]
• Adams SM, de Rivero Vaccari JC, Corriveau RA 2004. Pronounced cell death in the absence of NMDA receptors in the developing somatosensory thalamus. J Neurosci 24(42):9441-50.[Abstract/Free Full Text]
• Albers GW, Goldstein LB, Hall D., Lesko LM 2001. Aptiganel hydrochloride in acute ischemic stroke: a randomized controlled trial. JAMA 286(21):2673-82.[Abstract/Free Full Text]
• Alessi DR, James SR, Downes CP, Holmes AB, Gaffney PR, Reese CB, and others. 1997. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr Biol 7(4):261-9.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Arundine M., Tymianski M. 2004. Molecular mechanisms of glutamate-dependent neurodegeneration in ischemia and traumatic brain injury. Cell Mol Life Sci 61(6):657-68.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Bano D., Young KW, Guerin CJ, Lefeuvre R., Rothwell NJ, Naldini L., and others. 2005. Cleavage of the plasma membrane Na+/Ca2+ exchanger in excitotoxicity. Cell 120(2):275-85.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Bliss TV, Collingridge GL 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361(6407):31-9.[CrossRef][Medline] [Order article via Infotrieve]
• Bonni A., Brunet A., West AE, Datta SR, Takasu MA, Greenberg ME 1999. Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286(5443):1358-62.[Abstract/Free Full Text]
• Borsello T., Clarke PG, Hirt L., Vercelli A., Repici M., Schorderet DF, and others. 2003. A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischemia. Nat Med 9(9):1180-6.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Brunet A., Bonni A., Zigmond MJ, Lin MZ, Juo P., Hu LS and others. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96(6):857-68.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Camacho A., Massieu L. 2006. Role of glutamate transporters in the clearance and release of glutamate during ischemia and its relation to neuronal death. Arch Med Res 37(1):11-8.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Cao J., Semenova MM, Solovyan VT, Han J., Coffey ET, Courtney MJ 2004. Distinct requirements for p38alpha and c-Jun N-terminal kinase stress-activated protein kinases in different forms of apoptotic neuronal death. J Biol Chem 279(34):35903-13.[Abstract/Free Full Text]
• Choi DW 1988. Calcium-mediated neurotoxicity: relationship to specific channel types and role in ischemic damage. Trends Neurosci 11(10):465-9.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Collins MO, Husi H., Yu L., Brandon JM, Anderson CN, Blackstock WP, and others. 2006. Molecular characterization and comparison of the components and multiprotein complexes in the postsynaptic proteome. J Neurochem 97 Suppl 1:16-23.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Cross DA, Alessi DR, Cohen P., Andjelkovich M., Hemmings BA 1995. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378(6559):785-9.[CrossRef][Medline] [Order article via Infotrieve]
• Deisseroth K., Heist EK, Tsien RW 1998. Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons. Nature 392(6672):198-202.[CrossRef][Medline] [Order article via Infotrieve]
• Dirnagl U., Iadecola C., Moskowitz MA 1999. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22(9):391-7.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Downward J. 1999. How BAD phosphorylation is good for survival. Nat Cell Biol 1(2):E33-5.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Dyker AG, Edwards KR, Fayad PB, Hormes JT, Lees KR 1999. Safety and tolerability study of aptiganel hydrochloride in patients with an acute ischemic stroke. Stroke 30(10):2038-42.[Abstract/Free Full Text]
• Frizelle PA, Chen PE, Wyllie Dja. 2006. Equilibrium constants for NVP-AAM077 acting at recombinant NR1/NR2A and NR1/NR2B NMDA receptors: implications for studies of synaptic transmission. Mol Pharmacol 70(3):1022-32.[Abstract/Free Full Text]
• Gilley J., Coffer PJ, Ham J. 2003. FOXO transcription factors directly activate bim gene expression and promote apoptosis in sympathetic neurons. J Cell Biol 162(4):613-22.[Abstract/Free Full Text]
• Gould E., Cameron HA, McEwen BS 1994. Blockade of NMDA receptors increases cell death and birth in the developing rat dentate gyrus. J Comp Neurol 340:551-65.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Grabb MC, Choi DW 1999. Ischemic tolerance in murine cortical cell culture: critical role for NMDA receptors. J Neurosci 19:1657-62.[Abstract/Free Full Text]
• Hansen HH, Briem T., Dzietko M., Sifringer M., Voss A., Rzeski W., and others. 2004. Mechanisms leading to disseminated apoptosis following NMDA receptor blockade in the developing rat brain. Neurobiol Dis 16(2):440-53.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Hardingham GE, Arnold FJ, Bading H. 2001a. A calcium microdomain near NMDA receptors: on switch for ERK-dependent synapse-to-nucleus communication. Nat Neurosci 4(6):565-6.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Hardingham GE, Arnold FJ, Bading H. 2001b. Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nat Neurosci 4(3):261-7.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Hardingham GE, Bading H. 2002. Coupling of extrasynaptic NMDA receptors to a CREB shut-off pathway is developmentally regulated. Biochim Biophys Acta 1600(1-2):148-53.[Medline] [Order article via Infotrieve]
• Hardingham GE, Bading H. 2003. The Yin and Yang of NMDA receptor signaling. Trends Neurosci 26(2):81-9.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Hardingham GE, Chawla S., Cruzalegui FH, Bading H. 1999. Control of recruitment and transcription-activating function of CBP determines gene regulation by NMDA receptors and L-type calcium channels. Neuron 22(4):789-98.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Hardingham GE, Chawla S., Johnson CM, Bading H. 1997. Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature 385(6613):260-5.[CrossRef][Medline] [Order article via Infotrieve]
• Hardingham GE, Fukunaga Y., Bading H. 2002. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 5(5):405-14.[Web of Science][Medline] [Order article via Infotrieve]
• Hartley DM, Kurth MC, Bjerkness L., Weiss JH, Choi DW 1993. Glutamate receptor-induced 45Ca2+ accumulation in cortical cell culture correlates with subsequent neuronal degeneration. J Neurosci 13(5):1993 -2000.
• Hetman M., Kharebava G. 2006. Survival signaling pathways activated by NMDA receptors. Curr Top Med Chem 6(8):787-99.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Hossmann K-A. 1994. Viability thresholds and the penumbra of focal ischemia. Ann Neurol 36:557-65.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Ikonomidou C., Bosch F., Miksa M., Bittigau P., Vockler J., Dikranian K., and others. 1999. Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 283:70-4.[Abstract/Free Full Text]
• Ikonomidou C., Stefovska V., Turski L. 2000. Neuronal death enhanced by N-methyl-D-aspartate antagonists. Proc Natl Acad Sci U S A 97(23):12885-90.[Abstract/Free Full Text]
• Ikonomidou C., Turski L. 2002. Why did NMDA receptor antagonists fail clinical trials for stroke and traumatic brain injury? Lancet Neurol 1:383-6.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Impey S., Fong AL, Wang Y., Cardinaux JR, Fass DM, Obrietan K., and others. 2002. Phosphorylation of CBP mediates transcriptional activation by neural activity and CaM kinase IV. Neuron 34(2): 235-44.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Impey S., McCorkle SR, Cha-Molstad H., Dwyer JM, Yochum GS, Boss JM, and others. 2004. Defining the CREB regulon: a genome-wide analysis of transcription factor regulatory regions. Cell 119(7):1041-54.[Web of Science][Medline] [Order article via Infotrieve]
• Ivanov A., Pellegrino C., Rama S., Dumalska I., Salyha Y., Ben-Ari Y., and others. 2006. Opposing role of synaptic and extrasynaptic NMDA receptors in regulation of the ERK activity in cultured rat hippocampal neurons. J Physiol 572(3):789-98.[Abstract/Free Full Text]
• Jaworski J., Mioduszewska B., Sanchez-Capelo A., Figiel I., Habas A., Gozdz A., and others. 2003. Inducible cAMP early repressor, an endogenous antagonist of cAMP responsive element-binding protein, evokes neuronal apoptosis in vitro. J Neurosci 23(11):4519-26.[Abstract/Free Full Text]
• Joyal JL, Burks DJ, Pons S., Matter WF, Vlahos CJ, White MF, and others. 1997. Calmodulin activates phosphatidylinositol 3-kinase. J Biol Chem 272(45):28183-6.[Abstract/Free Full Text]
• Karadottir R., Cavelier P., Bergersen LH, Attwell D. 2005. NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438(7071):1162-6.[CrossRef][Medline] [Order article via Infotrieve]
• Kim AH, Khursigara G., Sun X., Franke TF, Chao MV 2001. Akt phosphorylates and negatively regulates apoptosis signal-regulating kinase 1. Mol Cell Biol 21(3):893-901.[Abstract/Free Full Text]
• Kohr G. 2006. NMDA receptor function: subunit composition versus spatial distribution. Cell Tissue Res 326(2):439-46.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Kovacs KA, Steullet P., Steinmann M., Do KQ, Magistretti PJ, Halfon O., and others. 2007. TORC1 is a calcium- and cAMP-sensitive coincidence detector involved in hippocampal long-term synaptic plasticity. Proc Natl Acad Sci U S A 104(11):4700-5.[Abstract/Free Full Text]
• Lafon-Cazal M., Perez V., Bockaert J., Marin P. 2002. Akt mediates the anti-apoptotic effect of NMDA but not that induced by potassium depolarization in cultured cerebellar granule cells. Eur J Neurosci 16(4):575-83.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Lee B., Butcher GQ, Hoyt KR, Impey S., Obrietan K. 2005. Activity-dependent neuroprotection and cAMP response element-binding protein (CREB): kinase coupling, stimulus intensity, and temporal regulation of CREB phosphorylation at serine 133. J Neurosci 25: 1137-48.[Abstract/Free Full Text]
• Lee J-M., Zipfel GJ, Choi DW 1999. The changing landscape of ischaemic brain injury mechanisms. Nature 399:A7-14.[Medline] [Order article via Infotrieve]
• Limback-Stokin K., Korzus E., Nagaoka-Yasuda R., Mayford M. 2004. Nuclear calcium/calmodulin regulates memory consolidation. J Neurosci 24(48):10858-67.[Abstract/Free Full Text]
• Lipton SA 2006. Paradigm shift in neuroprotection by NMDA receptor blockade: memantine and beyond. Nat Rev Drug Discov 5(2): 160-70.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Lipton SA, Nakanishi N. 1999. Shakespeare in love—with NMDA receptors? Nat Med 5(3):270-1.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Lipton SA, Rosenberg PA 1994. Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med 330(9):613-22.[Free Full Text]
• Liu Y., Wong TP, Aarts M., Rooyakkers A., Liu L., Lai TW, and others. 2007. NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo. J Neurosci 27(11):2846-57.[Abstract/Free Full Text]
• Lonze BE, Ginty DD 2002. Function and regulation of CREB family transcription factors in the nervous system. Neuron 35(4):605-23.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Lonze BE, Riccio A., Cohen S., Ginty DD 2002. Apoptosis, axonal growth defects, and degeneration of peripheral neurons in mice lacking CREB. Neuron 34:371-85.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Mabuchi T., Kitagawa K., Kuwabara K., Takasawa K., Ohtsuki T., Xia Z., and others. 2001. Phosphorylation of cAMP response element-binding protein in hippocampal neurons as a protective response after exposure to glutamate in vitro and ischemia in vivo. J Neurosci 21:9204-13.[Abstract/Free Full Text]
• Mantamadiotis T., Lemberger T., Bleckmann SC, Kern H., Kretz O., Villalba AM, and others. 2002. Disruption of CREB function in brain leads to neurodegeneration. Nat Genet 31:47-54.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Mayr B., Montminy M. 2001. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat Rev Mol Cell Biol 2(8):599-609.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Monti B., Contestabile A. 2000. Blockade of the NMDA receptor increases developmental apoptotic elimination of granule neurons and activates caspases in the rat cerebellum. Eur J Neurosci 12(9):3117-23.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Muir KW 2006. Glutamate-based therapeutic approaches: clinical trials with NMDA antagonists. Curr Opin Pharmacol 6(1):53-60.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Neyton J., Paoletti P. 2006. Relating NMDA receptor function to receptor subunit composition: limitations of the pharmacological approach. J Neurosci 26(5):1331-3.[Free Full Text]
• Nicholls DG 2004. Mitochondrial dysfunction and glutamate excitotoxicity studied in primary neuronal cultures. Curr Mol Med 4(2):149-77.[CrossRef]
• Olney JW, Wozniak DF, Jevtovic-Todorovic V., Farber NB, Bittigau P., Ikonomidou C. 2002. Drug-induced apoptotic neurodegeneration in the developing brain. Brain Pathol 12(4):488-98.[Web of Science][Medline] [Order article via Infotrieve]
• Papadia S., Stevenson P., Hardingham NR, Bading H., Hardingham GE 2005. Nuclear Ca2+ and the cAMP response element-binding protein family mediate a late phase of activity-dependent neuroprotection. J Neurosci 25(17):4279-87.[Abstract/Free Full Text]
• Pohl D., Ishmaru MJ, Bittigau P., Stadhaus D., Hubner C., Olney JW, and others. 1999. NMDA antagonists and apoptotic cell death triggered by head trauma in developing rat brain. Proc Natl Acad Sci U S A 96:2508-13.[Abstract/Free Full Text]
• Pottorf WJ 2nd, Johanns TM, Derrington SM, Strehler EE, Enyedi A., Thayer SA 2006. Glutamate-induced protease-mediated loss of plasma membrane Ca2+ pump activity in rat hippocampal neurons. J Neurochem 98(5):1646-56.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Rameau GA, Tukey DS, Garcin-Hosfield ED, Titcombe RF, Misra C., Khatri L., and others. 2007. Biphasic coupling of neuronal nitric oxide synthase phosphorylation to the NMDA receptor regulates AMPA receptor trafficking and neuronal cell death. J Neurosci 27(13):3445-55.[Abstract/Free Full Text]
• Riccio A., Ahn S., Davenport CM, Blendy JA, Ginty DD 1999. Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons. Science 286(5448):2358-61.[Abstract/Free Full Text]
• Rossi DJ, Oshima T., Attwell D. 2000. Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 403:316-21.[CrossRef][Medline] [Order article via Infotrieve]
• Sala C., Rudolph-Correia S., Sheng M. 2000. Developmentally regulated NMDA receptor-dependent dephosphorylation of cAMP response element-binding protein (CREB) in hippocampal neurons. J Neurosci 20:3529-36.[Abstract/Free Full Text]
• Sarbassov DD, Guertin DA, Ali SM, Sabatini DM 2005. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307(5712):1098-101.[Abstract/Free Full Text]
• Schwab BL, Guerini D., Didszun C., Bano D., Ferrando-May E., Fava E., and others. 2002. Cleavage of plasma membrane calcium pumps by caspases: a link between apoptosis and necrosis. Cell Death Differ 9(8):818-31.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Screaton RA, Conkright MD, Katoh Y., Best JL, Canettieri G., Jeffries S., and others. 2004. The CREB coactivator TORC2 functions as a calcium-and cAMP-sensitive coincidence detector. Cell 119(1):61-74.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Semenova MM, Maki-Hokkonen AM, Cao J., Komarovski V., Forsberg KM, Koistinaho M., and others. 2007. Rho mediates calcium-dependent activation of p38alpha and subsequent excitotoxic cell death. Nat Neurosci 10(4):436-43.[Web of Science][Medline] [Order article via Infotrieve]
• Shieh PB, Hu SC, Bobb K., Timmusk T., Ghosh A. 1998. Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron 20(4):727-40.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Soriano FX, Papadia S., Hofmann F., Hardingham NR, Bading H., Hardingham GE 2006. Preconditioning doses of NMDA promote neuroprotection by enhancing neuronal excitability. J Neurosci 26(17):4509-18.[Abstract/Free Full Text]
• Stout AK, Raphael HM, Kanterewicz BI, Klann E., Reynolds IJ 1998. Glutamate-induced neuron death requires mitochondrial calcium uptake. Nat Neurosci 1(5):366-73.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Szczesniak AM, Gilbert RW, Mukhida M., Anderson GI 2005. Mechanical loading modulates glutamate receptor subunit expression in bone. Bone 37(1):63-73.[Medline] [Order article via Infotrieve]
• Tanaka K., Nagata E., Suzuki S., Dembo T., Nogawa S., Fukuuchi Y. 1999. Immunohistochemical analysis of cyclic AMP response element binding protein phosphorylation in focal cerebral ischemia in rats. Brain Res 818:520-6.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Tao X., Finkbeiner S., Arnold DB, Shaywitz AJ, Greenberg ME 1998. Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20(4):709-26.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Tashiro A., Sandler VM, Toni N., Zhao C., Gage FH 2006. NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 442(7105):929-33.[CrossRef][Medline] [Order article via Infotrieve]
• Tompa P., Baki A., Schad E., Friedrich P. 1996. The calpain cascade. Mu-calpain activates m-calpain. J Biol Chem 271(52):33161-4.[Abstract/Free Full Text]
• Tuneva EO, Bychkova ON, Boldyrev AA 2003. Effect of NMDA on production of reactive oxygen species by human lymphocytes. Bull Exp Biol Med 136(2):159-61.[Web of Science][Medline] [Order article via Infotrieve]
• Walton MR, Dragunow M. 2000. Is CREB a key to neuronal survival? Trends Neurosci 23(2):48-53.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Walton M., Woodgate AM, Muravlev A., Xu R., During MJ, Dragunow M. 1999. CREB phosphorylation promotes nerve cell survival. J Neurochem 73(5):1836-42.[Web of Science][Medline] [Order article via Infotrieve]
• Waxman EA, Lynch DR 2005. N-methyl-D-aspartate receptor subtypes: multiple roles in excitotoxicity and neurological disease. Neuroscientist 11(1):37-49.[Abstract/Free Full Text]
• Wu GY, Deisseroth K., Tsien RW 2001. Activity-dependent CREB phosphorylation: convergence of a fast, sensitive calmodulin kinase pathway and a slow, less sensitive mitogen-activated protein kinase pathway. Proc Natl Acad Sci U S A 98(5):2808-13.[Abstract/Free Full Text]
• Yamaguchi A., Tamatani M., Matsuzaki H., Namikawa K., Kiyama H., Vitek MP, and others. 2001. Akt activation protects hippocampal neurons from apoptosis by inhibiting transcriptional activity of p53. J Biol Chem 276(7):5256-64.[Abstract/Free Full Text]
• Zhang SJ, Steijaert MN, Lau D., Schutz G., Delucinge-Vivier C., Descombes P., and others. 2007. Decoding NMDA receptor signaling: identification of genomic programs specifying neuronal survival and death. Neuron 53(4):549-62.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Zhang X., Odom DT, Koo SH, Conkright MD, Canettieri G., Best J., and others. 2005. Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc Natl Acad Sci U S A 102(12):4459-64.[Abstract/Free Full Text]

The Neuroscientist, Vol. 13, No. 6, 572-579 (2007)
DOI: 10.1177/10738584070130060401


CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				A. Deng and S. C. Thomson Renal NMDA receptors independently stimulate proximal reabsorption and glomerular filtration Am J Physiol Renal Physiol, May 1, 2009; 296(5): F976 - F982. [Abstract] [Full Text] [PDF]

				M. Y. Heng, P. J. Detloff, P. L. Wang, J. Z. Tsien, and R. L. Albin In Vivo Evidence for NMDA Receptor-Mediated Excitotoxicity in a Murine Genetic Model of Huntington Disease J. Neurosci., March 11, 2009; 29(10): 3200 - 3205. [Abstract] [Full Text] [PDF]

				F. T. Crews and K. Nixon Mechanisms of Neurodegeneration and Regeneration in Alcoholism Alcohol Alcohol., March 1, 2009; 44(2): 115 - 127. [Abstract] [Full Text] [PDF]

				P. R. Joshi, N.-P. Wu, V. M. Andre, D. M. Cummings, C. Cepeda, J. A. Joyce, J. B. Carroll, B. R. Leavitt, M. R. Hayden, M. S. Levine, et al. Age-Dependent Alterations of Corticostriatal Activity in the YAC128 Mouse Model of Huntington Disease J. Neurosci., February 25, 2009; 29(8): 2414 - 2427. [Abstract] [Full Text] [PDF]

				C. M. Cowan, M. M. Y. Fan, J. Fan, J. Shehadeh, L. Y. J. Zhang, R. K. Graham, M. R. Hayden, and L. A. Raymond Polyglutamine-Modulated Striatal Calpain Activity in YAC Transgenic Huntington Disease Mouse Model: Impact on NMDA Receptor Function and Toxicity J. Neurosci., November 26, 2008; 28(48): 12725 - 12735. [Abstract] [Full Text] [PDF]

				F. X. Soriano, M.-A. Martel, S. Papadia, A. Vaslin, P. Baxter, C. Rickman, J. Forder, M. Tymianski, R. Duncan, M. Aarts, et al. Specific Targeting of Pro-Death NMDA Receptor Signals with Differing Reliance on the NR2B PDZ Ligand J. Neurosci., October 15, 2008; 28(42): 10696 - 10710. [Abstract] [Full Text] [PDF]

This Article Abstract Free Full Text (Free PDF) Free Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Add to Saved Citations Download to citation manager Request Permissions Request Reprints Add to My Marked Citations Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (17) Citing Articles via Google Scholar Citing Articles via Scopus Google Scholar Articles by Papadia, S. Articles by Hardingham, G. E. Search for Related Content PubMed PubMed Citation Articles by Papadia, S. Articles by Hardingham, G. E. Social Bookmarking                         What's this?