The Yin and Yang of NMDA receptor signalling

Trends in Neurosciences

Volumn 26, Issue 2, 2003, Pages 81-89

  Hardingham, Giles E ^a   Bading, Hilmar ^b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE 1; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NERVE GROWTH FACTOR; PROTEIN BAD; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA;

ACTIN POLYMERIZATION; APOPTOSIS; CALCIUM TRANSPORT; CELL SURVIVAL; CYTOKINE PRODUCTION; GENE EXPRESSION; GRANULE CELL; MITOCHONDRION; NERVE CELL LESION; NERVE CELL NECROSIS; NERVE CELL PLASTICITY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; TOXICITY;

ANIMALS; APOPTOSIS; BRAIN; CALCIUM; CALCIUM CHANNELS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; HUMANS; MICE; MODELS, BIOLOGICAL; NEURONS; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION;

EID: 0037301661     PISSN: 01662236     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-2236(02)00040-1     Document Type: Review

References (92)

1. Forrest D., et al. Targeted disruption of NMDA receptor 1 gene abolishes NMDA response and results in neonatal death. Neuron. 13:1994;325-338.
2. Bliss T.V.P., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 361:1993;31-38.
3. Lipton S.A., Rosenberg P.A. Excitatory amino acids as a final common pathway for neurologic disorders. N. Engl. J. Med. 330:1994;613-621.
4. Lee J.-M., et al. The changing landscape of ischaemic brain injury mechanisms. Nature. 399:1999;A7-A14.
5. Dirnagl U., et al. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 22:1999;391-397.
6. Olney J.W., et al. Excitotoxic mechanisms of epileptic brain damage. Adv. Neurol. 44:1986;857-877.
7. Kaul M., et al. Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature. 410:2001;988-994.
8. Lancelot E., Beal M.F. Glutamate toxicity in chronic neurodegenerative disease. Prog. Brain Res. 116:1998;331-347.
9. Olney J.W., et al. Glutamate signaling and the fetal alcohol syndrome. Mental Retardation And Developmental Disabilities Research Reviews. 7:2001;267-275.
10. Sherrard R.M., Bower A.J. Role of afferents in the development and cell survival of the vertebrate nervous system. Clin. Exp. Pharmacol. Physiol. 25:1998;487-495.
11. Catsicas M., et al. Rapid onset of neuronal death induced by blockade of either axoplasmic-transport or action-potentials in afferent-fibers during brain-development. J. Neurosci. 12:1992;4642-4650.
12. Huang E.J., Reichardt L.F. Neurotrophins: Roles in neuronal development and function. Annu. Rev. Neurosci. 24:2001;677-736.
13. Kohara K., et al. Activity-dependent transfer of brain-derived neurotrophic factor to postsynaptic neurons. Science. 291:2001;2419-2423.
14. Linden R. The survival of developing neurons: a review of afferent control. Neuroscience. 58:1994;671-682.
15. Ikonomidou C., et al. Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science. 283:1999;70-74.
16. Sloviter R.S. Apoptosis: a guide for the perplexed. Trends Pharmacol. Sci. 23:2002;19-24.
17. Gould E., et al. Blockade of NMDA receptors increases cell death and birth in the developing rat dentate gyrus. J. Comp. Neurol. 340:1994;551-565.
18. Monti B., Contestabile A. Blockade of the NMDA receptor increases developmental apoptotic elimination of granule neurons and activates caspases in the rat cerebellum. Eur. J. Neurosci. 12:2000;3117-3123.
19. Pohl D., et al. NMDA antagonists and apoptotic cell death triggered by head trauma in developing rat brain. Proc. Natl. Acad. Sci. U. S. A. 96:1999;2508-2513.
20. Ikonomidou C., et al. Neuronal death enhanced by N-methyl-D-aspartate antagonists. Proc. Natl. Acad. Sci. U. S. A. 97:2000;12885-12890.
21. Ciani E., et al. Chronic pre-explant blockade of the NMDA receptor affects survival of cerebellar granule cells explanted in vitro. Brain Res. Dev. Brain Res. 99:1997;112-117.
22. Brenneman D.E., et al. N-methyl-D-aspartate receptors influence neuronal survival in developing spinal cord cultures. Brain Res. 51:1990;63-68.
23. Hardingham G.E., et al. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat. Neurosci. 5:2002;405-414.
24. Ikonomidou C., Turski L. Why did NMDA receptor antagonists fail clinical trials for stroke and traumatic brain injury? Lancet. 1:2002;383-386.
25. Yano S., et al. Calcium promotes cell survival through CaM-K kinase activation of the protein-kinase-B pathway. Nature. 396:1998;584-587.
26. Brunet A., et al. Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr. Opin. Neurobiol. 11:2001;297-305.
27. Bonni A., et al. Cell survival promoted by the ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science. 286:1999;1358-1362.
28. Cole A.J., et al. Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature. 340:1989;474-476.
29. Wisden W., et al. Differential expression of immediate early genes in the hippocampus and spinal cord. Neuron. 4:1990;603-614.
30. Schulz S., et al. Direct evidence for biphasic cAMP responsive element-binding protein phosphorylation during long-term potentiation in the rat dentate gyrus in vivo. J. Neurosci. 19:1999;5683-5692.
31. Cammarota M., et al. Learning-associated activation of nuclear MAPK, CREB and Elk-1, along with Fos production, in the rat hippocampus after a one-trial avoidance learning: abolition by NMDA receptor blockade. Mol. Brain Res. 76:2000;36-46.
32. Meberg P.J., et al. Gene expression of the transcription factor NF-κ B in hippocampus: regulation by synaptic activity. Mol. Brain Res. 38:1996;179-190.
33. Lipsky R.H., et al. Nuclear factor κB is a critical determinant in N-methyl-D-aspartate receptor-mediated neuroprotection. J. Neurochem. 78:2001;254-264.
34. Silva A.J., et al. CREB and memory. Annu. Rev. Neurosci. 21:1998;127-148.
35. Barco A., et al. Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell. 108:2002;689-703.
36. Walton M.R., Dragunow M. Is CREB a key to neuronal survival? Trends Neurosci. 23:2000;48-53.
37. Mattson M.P., et al. Roles of nuclear factor κB in neuronal survival and plasticity. J. Neurochem. 74:2000;443-456.
38. Mantamadiotis T., et al. Disruption of CREB function in brain leads to neurodegeneration. Nat. Genet. 31:2002;47-54.
39. Lonze B.E., et al. Apoptosis, axonal growth defects, and degeneration of peripheral neurons in mice lacking CREB. Neuron. 34:2002;371-385.
40. Mabuchi T., et al. 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. 21:2001;9204-9213.
41. Riccio A., et al. Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons. Science. 286:1999;2358-2361.
42. Tao X., et al. Calcium influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron. 20:1988;709-726.
43. Shieh P.B., et al. Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron. 20:1998;727-740.
44. Lonze B.E., Ginty D.D. Function and regulation of CREB family transcription factors in the nervous system. Neuron. 35:2002;605-623.
45. Yu Z., et al. Lack of the p50 subunit of nuclear factor-κB increases the vulnerability of hippocampal neurons to excitotoxic injury. J. Neurosci. 19:1999;8856-8865.
46. Bhakar A.L., et al. Constitutive Nuclear Factor-κB activity is required for central neuron survival. J. Neurosci. 22:2002;8466-8475.
47. Maggirwar S.B., et al. Nerve growth factor-dependent activation of NF-κ B contributes to survival of sympathetic neurons. J. Neurosci. 18:1998;10356-10365.
48. Middleton G., et al. Cytokine-induced nuclear factor κ B activation promotes the survival of developing neurons. J. Cell Biol. 148:2000;325-332.
49. Wellmann H., et al. Retrograde transport of transcription factor NF-κ B in living neurons. J. Biol. Chem. 276:2001;11821-11829.
50. Mattson M.P., Camandola S. NF-κB in neuronal plasticity and neurodegenerative disorders. J. Clin. Invest. 107:2001;247-254.
51. Young D., et al. Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective. Nat. Med. 5:1999;448-453.
52. Bading H., et al. Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science. 260:1993;181-186.
53. Hardingham G.E., et al. Control of recruitment and transcription-activating function of CBP determines gene regulation by NMDA receptors and L-type calcium channels. Neuron. 22:1999;789-798.
54. Tovar K.R., Westbrook G.L. The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocAMPal synapses in vitro. J. Neurosci. 19:1999;4180-4188.
55. Hardingham, G.E. and Bading, H. Coupling of extrasynaptic NMDA receptors to CREB shut-off pathway is developmentally regulated. Biochim. Biophys. Acta Mol. Cell Res. (in press).
56. Sala C., et al. Developmentally regulated NMDA receptor-dependent dephosphorylation of cAMP response element-binding protein (CREB) in hippocampal neurons. J. Neurosci. 20:2000;3529-3536.
57. Rossi D.J., et al. Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature. 403:2000;316-321.
58. Tanaka K., et al. Immunohistochemical analysis of cyclic AMP response element binding protein phosphorylation in focal cerebral ischemia in rats. Brain Res. 818:1999;520-526.
59. Hossmann K.-A. Viability thresholds and the penumbra of focal ischemia. Ann. Neurol. 36:1994;557-565.
60. 2+ accumulation in cortical cell culture correlates with subsequent neuronal degeneration. J. Neurosci. 13:1993;1993-2000.
61. Nicholls D.G., Budd S.L. Mitochondria and neuronal survival. Physiol. Rev. 80:2000;315-360.
62. Ankarcrona M., et al. Glutamate-induced neuronal death: A succession of necrosis or apoptosis depending on mitochondrial function. Neuron. 15:1995;961-973.
63. Cheung N.S., et al. Micromolar L-glutamate induces extensive apoptosis in an apoptotic- necrotic continuum of insult-dependent, excitotoxic injury in cultured cortical neurones. Neuropharmacology. 37:1998;1419-1429.
64. Budd S.L., Nicholls D.G. Mitochondrial calcium regulation, and acute glutamate excitotoxicity in cultured cerebellar granule cells. J. Neurochem. 67:1996;2282-2291.
65. 2+ following intense glutamate stimulation of cultured rat forebrain neurones. J. Physiol. 498:1997;31-47.
66. Keelan J., et al. Excitotoxic mitochondrial depolarisation requires both calcium and nitric oxide in rat hippocampal neurons. J. Physiol. 520:1999;797-813.
67. Stout A.K., et al. Glutamate-induced neuron death requires mitochondrial calcium uptake. Nat. Neurosci. 1:1998;366-373.
68. Ward M.W., et al. Mitochondrial membrane potential and glutamate excitotoxicity in cultured cerebellar granule cells. J. Neurosci. 20:2000;7208-7219.
69. Andreyev A.Y., et al. Cytochrome c release from brain mitochondria is independent of the mitochondrial permeability transition. FEBS Lett. 439:1998;373-376.
70. Kawasaki H., et al. Activation and involvement of p38 mitogen-activated protein kinase in glutamate-induced apoptosis in rat cerebellar granule cells. J. Biol. Chem. 272:1997;18518-18521.
71. Schwarzschild M.A., et al. Glutamate, but not dopamine, stimulates stress-activated protein kinase and AP-1-mediated transcription in striatal neurons. J. Neurosci. 15:1997;3455-3466.
72. Yang D.D., et al. Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature. 389:1997;865-870.
73. 2+ influx underlies potent induction of injury. J. Neurosci. 16:1996;5457-5465.
74. Eimerl S., Schramm M. The quantity of calcium that appears to induce neuronal death. J. Neurochem. 62:1994;1223-1226.
75. Tymianski M., et al. Source specificity of early calcium neurotoxicity in cultures embryonic spinal neurons. J. Neurosci. 13:1993;2085-2104.
76. Sattler R., et al. Distinct influx pathways, not calcium load, determine neuronal vulnerability to calcium neurotoxicity. J. Neurochem. 71:1998;2346-2364.
77. Peng T.I., Greenamyre J.T. Privileged access to mitochondria of calcium influx through N-methyl-D-aspartate receptors. Mol. Pharmacol. 53:1998;974-980.
78. Stout A.K., Reynolds I.J. High-affinity calcium indicators underestimate increases in intracellular calcium concentrations associated with excitotoxic glutamate stimulations. Neuroscience. 89:1998;91-100.
79. Sheng M., Pak D.T. Ligand-gated ion channel interactions with cytoskeletal and signaling proteins. Annu. Rev. Physiol. 62:2000;755-778.
80. Husi H., et al. Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat. Neurosci. 3:2000;661-669.
81. Lacza Z., et al. Mitochondrial nitric oxide synthase is constitutively active and is functionally upregulated in hypoxia. Free Radic. Biol. Med. 31:2001;1609-1615.
82. Sattler R., et al. Specific coupling of NMDA receptor activation to nitric oxide neurotoxicity by PSD-95 protein. Science. 284:1999;1845-1848.
83. Aarts M., et al. Treatment of ischemic brain damage by perturbing NMDA receptor- PSD-95 protein interactions. Science. 298:2002;846-850.
84. Anegawa N.J., et al. N-methyl-D-aspartate receptor mediated toxicity in nonneuronal cell lines: characterization using fluorescent measures of cell viability and reactive oxygen species production. Mol. Brain Res. 77:2000;163-175.
85. Rameau G.A., et al. Role of NMDA receptor functional domains in excitatory cell death. Neuropharmacology. 39:2000;2255-2266.
86. Sattler R., et al. Distinct roles of synaptic and extrasynaptic NMDA receptors in excitotoxicity. J. Neurosci. 20:2000;22-33.
87. Wang Y., et al. Endoplasmic reticulum calcium release is modulated by actin polymerisation. J. Neurochem. 82:2002;945-952.
88. Mattson M.P. Presenilin-1 mutation increases neuronal vulnerability to focal ischemia in vivo and to hypoxia and glucose deprivation in cell culture: involvement of perturbed calcium homeostasis. J. Neurosci. 20:2000;1358-1364.
89. Lipton S.A., Nakanishi N. Shakespeare in Love - with NMDA receptors? Nat. Med. 5:1999;270-271.
90. Lipton S.A., Kater S.B. Neurotransmitter regulation of neuronal outgrowth, plasticity and survival. Trends Neurosci. 12:1989;265-270.
91. Parsons C.G., et al. Memantine is a clinically well tolerated N-methyl-D-aspartate (NMDA) receptor antagonist-a review of preclinical data. Neuropharmacology. 38:1999;735-767.
92. Birmingham K. Future of neuroprotective drugs in doubt. Nat. Med. 8:2002;5.