Role of the N-methyl-d-aspartate receptors complex in amyotrophic lateral sclerosis

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 2, 2013, Pages 312-322

  Spalloni, Alida ^a   Nutini, Michele ^a   Longone, Patrizia ^a  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

Author keywords

Amyotrophic lateral sclerosis; Excitotoxicity; Glutamate; N methyl d aspartate receptor; Neurodegeneration

Indexed keywords

AMPA RECEPTOR; DEXTRO SERINE; GLUTAMIC ACID; GLYCINE; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POLYAMINE; SPERMIDINE; SPERMINE; ZINC;

AMYOTROPHIC LATERAL SCLEROSIS; CELL DEATH; COMPLEX FORMATION; EXCITOTOXICITY; MOTONEURON; NERVE CELL DEGENERATION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SPINAL CORD;

AMYOTROPHIC LATERAL SCLEROSIS; CELL DEATH; HUMANS; MOTOR NEURONS; RECEPTORS, N-METHYL-D-ASPARTATE; SPINAL CORD;

EID: 84871003645     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2012.11.013     Document Type: Review

References (173)

1. Traynelis S.F., Wollmuth L.P., McBain C.J., Menniti F.S., Vance K.M., Ogden K.K., Hansen K.B., Yuan H., Myers S.J., Dingledine R. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 2010, 62:405-496.
2. Choi D.W. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1988, 8:623-634.
3. Arundine M., Tymianski M. Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium 2003, 34:325-337.
4. Lodge D. The history of the pharmacology and cloning of ionotropic glutamate receptors and the development of idiosyncratic nomenclature. Neuropharmacology 2009, 56:6-21.
5. Niswender C.M., Conn P.J. Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu. Rev. Pharmacol. Toxicol. 2010, 50:295-322.
6. Danbolt N.C. Glutamate uptake. Prog. Neurobiol. 2001, 65:1-105.
7. El Mestikawy S., Wallén-Mackenzie A., Fortin G.M., Descarries L., Trudeau L.E. From glutamate co-release to vesicular synergy: vesicular glutamate transporters. Nat. Rev. Neurosci. 2011, 12:204-216.
8. Meldrum B.S. Glutamate as a neurotransmitter in the brain: review of physiology and pathology. J. Nutr. 2000, 130(Suppl. 4S):1007S-1015S.
9. Ozawa S., Kamiya H., Tsuzuki K. Glutamate receptors in the mammalian central nervous system. Prog. Neurobiol. 1998, 54:581-618.
10. Madden D.R. The structure and function of glutamate receptor ion channels. Nat. Rev. Neurosci. 2002, 3:91-101.
11. Olney J.W. Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate. Science 1969, 164:719-721.
12. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., Lipton S.A. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-d-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:7162-7166.
13. Choi D.W. Excitotoxic cell death. J. Neurobiol. 1992, 23:1261-1276.
14. Murphy T.H., Malouf A.T., Sastre A., Schnaar R.L., Coyle J.T. Calcium-dependent glutamate cytotoxicity in a neuronal cell line. Brain Res. 1988, 444:325-332.
15. Frandsen, Schousboe A. Excitatory amino acid-mediated cytotoxicity and calcium homeostasis in cultured neurons. J. Neurochem. 1993, 60:1201-1211.
16. Johnson J.W., Ascher P. Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 1987, 325:529-531.
17. Mayer M.L., Westbrook G.L., Guthrie P.B. Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurons. Nature 1984, 309:261-263.
18. Sattler R., Charlton M.P., Hafner M., Tymianski M. Distinct influx pathways, not calcium load, determine neuronal vulnerability to calcium neurotoxicity. J. Neurochem. 1998, 71:2349-2364.
19. Garthwaite G., Garthwaite J. Mechanisms of AMPA neurotoxicity in rat brain slices. Eur. J. Neurosci. 1991, 3:729-736.
20. Reynolds I.J. Intracellular calcium and magnesium: critical determinants of excitotoxicity?. Prog. Brain Res. 1998, 116:225-243.
21. Mody, MacDonald J.F. NMDA receptor-dependent excitotoxicity: the role of intracellular Ca2+ release. Trends Pharmacol. Sci. 1995, 16:356-359.
22. Nicholls D.G. Mitochondrial dysfunction and glutamate excitotoxicity studied in primary neuronal cultures. Curr. Mol. Med. 2004, 4:149-177.
23. Olney J.W., de Gubareff T., Labruyere J. alpha-Aminoadipate blocks the neurotoxic action of N-methyl aspartate. Life Sci. 1979, 25:537-540.
24. Ikonomidou C., Price M.T., Mosinger J.L., Frierdich G., Labruyere J., Salles K.S., Olney J.W. Hypobaric-ischemic conditions produce glutamate-like cytopathology in infant rat brain. J. Neurosci. 1989, 9:1693-1700.
25. Hasbani M.J., Schlief M.L., Fisher D.A., Goldberg M.P. Dendritic spines lost during glutamate receptor activation reemerge at original sites of synaptic contact. J. Neurosci. 2001, 21:2393-2403.
26. Ikegaya Y., Kim J.A., Baba M., Iwatsubo T., Nishiyama N., Matsuki N. Rapid and reversible changes in dendrite morphology and synaptic efficacy following NMDA receptor activation: implication for a cellular defense against excitotoxicity. J. Cell Sci. 2001, 114:4083-4093.
27. Heath P.R., Shaw P.J. Update on the glutamatergic neurotransmitter system and the role of excitotoxicity in amyotrophic lateral sclerosis. Muscle Nerve 2002, 26:438-458.
28. Hynd M.R., Scott H.L., Dodd P.R. Selective loss of NMDA receptor NR1 subunit isoforms in Alzheimer's disease. J. Neurochem. 2004, 89:240-247.
29. Wang X., Michaelis E.K. Selective neuronal vulnerability to oxidative stress in the brain. Front. Aging Neurosci. 2010, 2:12.
30. Paoletti P. Molecular basis of NMDA receptor functional diversity. Eur. J. Neurosci. 2011, 33:1351-1365.
31. Laurie D.J., Seeburg P.H. Ligand affinities at recombinant N-methyl-d-aspartate receptors depend on subunit composition. Eur. J. Pharmacol. 1994, 268:335-345.
32. Monyer H., Burnashev N., Laurie D.J., Sakmann B., Seeburg P.H. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 1994, 12:529-540.
33. Cull-Candy S.G., Brickley S., Farrant M. NMDA receptor subunits: diversity, development and disease. Curr. Opin. Neurobiol. 2001, 11:327-335.
34. Köhr G. NMDA receptor function: subunit composition versus spatial distribution. Cell Tissue Res. 2006, 326:439-446.
35. Harney S.C., Jane D.E., Anwyl R. Extrasynaptic NR2D-containing NMDARs are recruited to the synapse during LTP of NMDAR-EPSCs. J. Neurosci. 2008, 28:11685-11694.
36. Low C.M., Wee K.S. New insights into the not-so-new NR3 subunits of N-methyl-d-aspartate receptor: localization, structure, and function. Mol. Pharmacol. 2010, 78:1-11.
37. Wee K.S., Zhang Y., Khanna S., Low C.M. Immunolocalization of NMDA receptor subunit NR3B in selected structures in the rat forebrain, cerebellum, and lumbar spinal cord. J. Comp. Neurol. 2008, 509:118-135.
38. Thomas C.G., Miller A.J., Westbrook G.L. Synaptic and extrasynaptic NMDA receptor NR2 subunits in cultured hippocampal neurons. J. Neurophysiol. 2006, 95:1727-1734.
39. Petralia R.S., Wang Y.X., Hua F., Yi Z., Zhou A., Ge L., Stephenson F.A., Wenthold R.J. Organization of NMDA receptors at extrasynaptic locations. Neuroscience 2010, 167:68-87.
40. Ferreira I.L., Duarte C.B., Carvalho A.P. Ca2+ influx through glutamate receptor-associated channels in retina cells correlates with neuronal cell death. Eur. J. Pharmacol. 1996, 302:153-162.
41. Merrill M.A., Chen Y., Strack S., Hell J.W. Activity-driven postsynaptic translocation of CaMKII. Trends Pharmacol. Sci. 2005, 26:645-653.
42. Gardoni F., Marcello E., Di Luca M. Postsynaptic density-membrane associated guanylate kinase proteins (PSD-MAGUKs) and their role in CNS disorders. Neuroscience 2009, 158:324-333.
43. Yamauchi M., Omote K., Ninomiya T. Direct evidence for the role of nitric oxide on the glutamate-induced neuronal death in cultured cortical neurons. Brain Res. 1998, 780:253-259.
44. Centeno C., Repici M., Chatton J.Y., Riederer B.M., Bonny C., Nicod P., Price M., Clarke P.G., Papa S., Franzoso G., Borsello T. Role of the JNK pathway in NMDA-mediated excitotoxicity of cortical neurons. Cell Death Differ. 2007, 14:240-253.
45. Mandir A.S., Poitras M.F., Berliner A.R., Herring W.J., Guastella D.B., Feldman A., Poirier G.G., Wang Z.Q., Dawson T.M., Dawson V.L. NMDA but not non-NMDA excitotoxicity is mediated by Poly(ADP-ribose) polymerase. J. Neurosci. 2000, 20:8005-8011.
46. Rowland L.P., Shneider N.A. Amyotrophic lateral sclerosis. N. Engl. J. Med. 2001, 344:1688-1700.
47. Cudkowicz M.E., Katz J., Moore D.H., O'Neill G., Glass J.D., Mitsumoto H., Appel S., Ravina B., Kieburtz K., Shoulson I., Kaufmann P., Khan J., Simpson E., Shefner J., Levin B., Cwik V., Schoenfeld D., Aggarwal S., McDermott M.P., Miller R.G. Toward more efficient clinical trials for amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 2010, 11:259-265.
48. Bensimon G., Lacomblez L., Meininger V. A controlled trial of riluzole in amyotrophic lateral sclerosis. ALS/Riluzole Study Group. N. Engl. J. Med. 1994, 30:585-591.
49. Zona C., Siniscalchi A., Mercuri N.B., Bernardi G. Riluzole interacts with voltage-activated sodium and potassium currents in cultured rat cortical neurons. Neuroscience 1998, 85:931-938.
50. Urbani, Belluzzi O. Riluzole inhibits the persistent sodium current in mammalian CNS neurons. Eur. J. Neurosci. 2000, 12:3567-3574.
51. Chéramy, Barbeito L., Godeheu G., Glowinski J. Riluzole inhibits the release of glutamate in the caudate nucleus of the cat in vivo. Neurosci. Lett. 1992, 147:209-212.
52. Cifra, Mazzone G.L., Nistri A. Riluzole: what it does to spinal and brainstem neurons and how it does it. Neuroscientist May 16 2012, http://dx.doi.org/10.1177/1073858412444932 ([Epub ahead of print] PubMed PMID: 22596264).
53. Al-Chalabi A., Jones A., Troakes C., King A., Al-Sarraj S., van den Berg L.H. The genetics and neuropathology of amyotrophic lateral sclerosis. Acta Neuropathol. 2012, 124:339-352.
54. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J.P., Deng H.X., Rahmani Z., Krizus A., McKenna-Yasek D., Cayabyab A., Gaston S.M., Berger R., Tanzi R.E., Halperin J.J., Herzfeldt B., Van Den Bergh R., Hung W.Y., Bird T., Deng G., Mulder D.W., Smyth C., Laing N.G., Soriano E., Pericak-Vance M.A., Haines J., Rouleau G.A., Gusella J.S., Horvitz H.R., Brown R.H. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62.
55. van Es M.A., Dahlberg C., Birve A., Veldink J.H., van den Berg L.H., Andersen P.M. Large-scale SOD1 mutation screening provides evidence for genetic heterogeneity in amyotrophic lateral sclerosis. J. Neurol. Neurosurg. Psychiatry 2010, 81:562-566.
56. Yang Y., Hentati A., Deng H.X., Dabbagh O., Sasaki T., Hirano M., Hung W.Y., Ouahchi K., Yan J., Azim A.C., Cole N., Gascon G., Yagmour A., Ben-Hamida M., Pericak-Vance M., Hentati F., Siddique T. The gene encoding alsin, a protein with three guanine-nucleotide exchange factor domains, is mutated in a form of recessive amyotrophic lateral sclerosis. Nat. Genet. 2001, 29:160-165.
57. Chen Y.Z., Bennett C.L., Huynh H.M., Blair I.P., Puls I., Irobi J., Dierick I., Abel A., Kennerson M.L., Rabin B.A., Nicholson G.A., Auer-Grumbach M., Wagner K., De Jonghe P., Griffin J.W., Fischbeck K.H., Timmerman V., Cornblath D.R., Chance P.F. DNA/RNA helicase gene mutations in a form of juvenile amyotrophic lateral sclerosis (ALS4). Am. J. Hum. Genet. 2004, 74:1128-1135.
58. Nishimura A.L., Mitne-Neto M., Silva H.C., Richieri-Costa A., Middleton S., Cascio D., Kok F., Oliveira J.R., Gillingwater T., Webb J., Skehel P., Zatz M. A mutation in the vesicle-trafficking protein VAPB causes late-onset spinal muscular atrophy and amyotrophic lateral sclerosis. Am. J. Hum. Genet. 2004, 75:822-831.
59. Greenway M.J., Andersen P.M., Russ C., Ennis S., Cashman S., Donaghy C., Patterson V., Swingler R., Kieran D., Prehn J., Morrison K.E., Green A., Acharya K.R., Brown R.H., Hardiman O. ANG mutations segregate with familial and 'sporadic' amyotrophic lateral sclerosis. Nat. Genet. 2006, 38:411-413.
60. Münch, Sedlmeier R., Meyer T., Homberg V., Sperfeld A.D., Kurt A., Prudlo J., Peraus G., Hanemann C.O., Stumm G., Ludolph A.C. Point mutations of the p150 subunit of dynactin (DCTN1) gene in ALS. Neurology 2004, 63:724-726.
61. Lambrechts, Storkebaum E., Morimoto M., Del-Favero J., Desmet F., Marklund S.L., Wyns S., Thijs V., Andersson J., van Marion I., Al-Chalabi A., Bornes S., Musson R., Hansen V., Beckman L., Adolfsson R., Pall H.S., Prats H., Vermeire S., Rutgeerts P., Katayama S., Awata T., Leigh N., Lang-Lazdunski L., Dewerchin M., Shaw C., Moons L., Vlietinck R., Morrison K.E., Robberecht W., Van Broeckhoven C., Collen D., Andersen P.M., Carmeliet P. VEGF is a modifier of amyotrophic lateral sclerosis in mice and humans and protects motoneurons against ischemic death. Nat. Genet. 2003, 34:383-394.
62. Strong M.J. The evidence for altered RNA metabolism in amyotrophic lateral sclerosis (ALS). J. Neurol. Sci. 2010, 2010(288):1-12.
63. Joyce P.I., Fratta P., Fisher E.M., Acevedo-Arozena A. SOD1 and TDP-43 animal models of amyotrophic lateral sclerosis: recent advances in understanding disease toward the development of clinical treatments. Mamm. Genome. 2011, 22:420-448.
64. Plaitakis, Caroscio J.T. Abnormal glutamate metabolism in amyotrophic lateral sclerosis. Ann. Neurol. 1987, 22:575-579.
65. Rothstein J.D., Tsai G., Kuncl R.W., Clawson L., Cornblath D.R., Drachman D.B., Pestronk A., Stauch B.L., Coyle J.T. Abnormal excitatory amino acid metabolism in amyotrophic lateral sclerosis. Ann. Neurol. 1990, 28:18-25.
66. Rothstein J.D., Martin L.J., Kuncl R.W. Decreased glutamate transport by the brain and spinal cord in amyotrophic lateral sclerosis. N. Engl. J. Med. 1992, 326:1464-1468.
67. Couratier P., Hugon J., Sindou P., Vallat J.M., Dumas M. Cell culture evidence for neuronal degeneration in amyotrophic lateral sclerosis being linked to glutamate AMPA/kainate receptors. Lancet 1993, 341:265-268.
68. Foran, Trotti D. Glutamate transporters and the excitotoxic path to motor neuron degeneration in amyotrophic lateral sclerosis. Antioxid. Redox Signal. 2009, 11:1587-1602.
69. Carriedo S.G., Sensi S.L., Yin H.Z., Weiss J.H. AMPA exposures induce mitochondrial Ca(2+) overload and ROS generation in spinal motor neurons in vitro. J. Neurosci. 2000, 20:240-250.
70. Van Den Bosch L., Vandenberghe W., Klaassen H., Van Houtte E., Robberecht W. Ca(2+)-permeable AMPA receptors and selective vulnerability of motor neurons. J. Neurol. Sci. 2000, 180:29-34.
71. Spalloni, Albo F., Ferrari F., Mercuri N., Bernardi G., Zona C., Longone P. Cu/Zn-superoxide dismutase (GLY93->ALA) mutation alters AMPA receptor subunit expression and function and potentiates kainate-mediated toxicity in motor neurons in culture. Neurobiol. Dis. 2004, 15:340-350.
72. Estevez A.G., Stutzmann J.M., Barbeito L. Protective effect of riluzole on excitatory amino acid-mediated neurotoxicity in motoneuron-enriched cultures. Eur. J. Pharmacol. 1995, 280:47-53.
73. Kalb R.G., Lidow M.S., Halsted M.J., Hockfield S. N-methyl-d-aspartate receptors are transiently expressed in the developing spinal cord ventral horn. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:8502-8506.
74. Hori N., Tan Y., King M., Strominger N.L., Carpenter D.O. Differential actions and excitotoxicity of glutamate agonists on motoneurons in adult mouse cervical spinal cord slices. Brain Res. 2002, 958:434-438.
75. Nagy G.G., Watanabe M., Fukaya M., Todd A.J. Synaptic distribution of the NR1, NR2A and NR2B subunits of the N-methyl-d-aspartate receptor in the rat lumbar spinal cord revealed with an antigen-unmasking technique. Eur. J. Neurosci. 2004, 20:3301-3312.
76. Stegenga S.L., Kalb R.G. Developmental regulation of N-methyl-d-aspartate- and kainate-type glutamate receptor expression in the rat spinal cord. Neuroscience 2001, 105:499-507.
77. Tölle T.R., Berthele A., Zieglgänsberger W., Seeburg P.H., Wisden W. The differential expression of 16 NMDA and non-NMDA receptor subunits in the rat spinal cord and in periaqueductal gray. J. Neurosci. 1993, 13:5009-5028.
78. Fukaya M., Hayashi Y., Watanabe M. NR2 to NR3B subunit switchover of NMDA receptors in early postnatal motoneurons. Eur. J. Neurosci. 2005, 21:1432-1436.
79. Nishi M., Hinds H., Lu H.P., Kawata M., Hayashi Y. Motoneuron-specific expression of NR3B, a novel NMDA-type glutamate receptor subunit that works in a dominant-negative manner. J. Neurosci. 2001, 21:RC185.
80. Roberts A.C., Díez-García J., Rodriguiz R.M., López I.P., Luján R., Martínez-Turrillas R., Picó E., Henson M.A., Bernardo D.R., Jarrett T.M., Clendeninn D.J., López-Mascaraque L., Feng G., Lo D.C., Wesseling J.F., Wetsel W.C., Philpot B.D., Pérez-Otaño I. Downregulation of NR3A-containing NMDARs is required for synapse maturation and memory consolidation. Neuron 2009, 2009(63):342-356.
81. Ziskind-Conhaim L. NMDA receptors mediate poly- and monosynaptic potentials in motoneurons of rat embryos. J. Neurosci. 1990, 10:125-135.
82. Kalb R.G., Hockfield S. Activity-dependent development of spinal cord motor neurons. Brain Res. Brain Res. Rev. 1992, 283-289.
83. Arvanian V.L., Bowers W.J., Petruska J.C., Motin V., Manuzon H., Narrow W.C., Federoff H.J., Mendell L.M. Viral delivery of NR2D subunits reduces Mg2+ block of NMDA receptor and restores NT-3-induced potentiation of AMPA-kainate responses in maturing rat motoneurons. J. Neurophysiol. 2004, 92:2394-2404.
84. Bonnot, Whelan P.J., Mentis G.Z., O'Donovan M.J. Locomotor-like activity generated by the neonatal mouse spinal cord. Brain Res. Brain Res. Rev. 2002, 40:141-151.
85. Konnerth, Keller B.U., Lev-Tov A. Patch clamp analysis of excitatory synapses in mammalian spinal cord slices. Pflugers Arch. 1990, 417:285-290.
86. Palecek J.I., Abdrachmanova G., Vlachová V., Vyklick L. Properties of NMDA receptors in rat spinal cord motoneurons. Eur. J. Neurosci. 1999, 11:827-836.
87. Sucher N.J., Akbarian S., Chi C.L., Leclerc C.L., Awobuluyi M., Deitcher D.L., Wu M.K., Yuan J.P., Jones E.G., Lipton S.A. Developmental and regional expression pattern of a novel NMDA receptor-like subunit (NMDAR-L) in the rodent brain. J. Neurosci. 1995, 15:6509-6520.
88. Manuel M., Li Y., Elbasiouny S.M., Murray K., Griener A., Heckman C.J., Bennett D.J. NMDA induces persistent inward and outward currents that cause rhythmic bursting in adult rodent motoneurons. J. Neurophysiol. 2012, 108(11):2991-2998. http://dx.doi.org/10.1152/jn.00518.2012(Epub 2012 Sep 12).
89. Enríquez Denton M., Wienecke J., Zhang M., Hultborn H., Kirkwood P.A. Voltage-dependent amplification of synaptic inputs in respiratory motoneurones. J. Physiol. 2012, 590:3067-3090.
90. Jiang M., Schuster J.E., Fu R., Siddique T., Heckman C.J. Progressive changes in synaptic inputs to motoneurons in adult sacral spinal cord of a mouse model of amyotrophic lateral sclerosis. J. Neurosci. 2009, 29:15031-15038.
91. Quinlan K.A., Schuster J.E., Fu R., Siddique T., Heckman C.J. Altered postnatal maturation of electrical properties in spinal motoneurons in a mouse model of amyotrophic lateral sclerosis. J. Physiol. 2011, 589:2245-2260.
92. Urushitani M., Nakamizo T., Inoue R., Sawada H., Kihara T., Honda K., Akaike A., Shimohama S. N-methyl-d-aspartate receptor-mediated mitochondrial Ca(2+) overload in acute excitotoxic motor neuron death: a mechanism distinct from chronic neurotoxicity after Ca(2+) influx. J. Neurosci. Res. 2001, 63:377-387.
93. Brunet N., Tarabal O., Esquerda J.E., Calderó J. Excitotoxic motoneuron degeneration induced by glutamate receptor agonists and mitochondrial toxins in organotypic cultures of chick embryo spinal cord. J. Comp. Neurol. 2009, 516:277-290.
94. Sanelli T., Ge W., Leystra-Lantz C., Strong M.J. Calcium mediated excitotoxicity in neurofilament aggregate-bearing neurons in vitro is NMDA receptor dependant. J. Neurol. Sci. 2007, 256:39-51.
95. Sanelli T.R., Sopper M.M., Strong M.J. Sequestration of nNOS in neurofilamentous aggregate bearing neurons in vitro leads to enhanced NMDA-mediated calcium influx. Brain Res. 2004, 1004:8-17.
96. White R.J., Reynolds I.J. Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure. J. Neurosci. 1996, 16:5688-5697.
97. Ashpole N.M., Song W., Brustovetsky T., Engleman E.A., Brustovetsky N., Cummins T.R., Hudmon A. Calcium/calmodulin-dependent protein kinase II (CaMKII) inhibition induces neurotoxicity via dysregulation of glutamate/calcium signaling and hyperexcitability. J. Biol. Chem. 2012, 287:8495-8506.
98. Budd S.L., Nicholls D.G. Mitochondria, calcium regulation, and acute glutamate excitotoxicity in cultured cerebellar granule cells. J. Neurochem. 1996, 67:2282-2291.
99. Nicholls D.G., Johnson-Cadwell L., Vesce S., Jekabsons M., Yadava N. Bioenergetics of mitochondria in cultured neurons and their role in glutamate excitotoxicity. J. Neurosci. Res. 2007, 85:3206-3212.
100. Kambe Y., Nakamichi N., Takarada T., Fukumori R., Nakazato R., Hinoi E., Yoneda Y. A possible pivotal role of mitochondrial free calcium in neurotoxicity mediated by N-methyl-d-aspartate receptors in cultured rat hippocampal neurons. Neurochem. Int. 2011, 59:10-20.
101. Peng T.I., Greenamyre J.T. Privileged access to mitochondria of calcium influx through N-methyl-d-aspartate receptors. Mol. Pharmacol. 1998, 53:974-980.
102. Nguyen, Alavi M.V., Kim K.Y., Kang T., Scott R.T., Noh Y.H., Lindsey J.D., Wissinger B., Ellisman M.H., Weinreb R.N., Perkins G.A., Ju W.K. A new vicious cycle involving glutamate excitotoxicity, oxidative stress and mitochondrial dynamics. Cell Death Dis Dec 8 2011, 2:e240. 10.1038/cddis.2011.117.
103. Cassina P., Cassina A., Pehar M., Castellanos R., Gandelman M., de León A., Robinson K.M., Mason R.P., Beckman J.S., Barbeito L., Radi R. Mitochondrial dysfunction in SOD1G93A-bearing astrocytes promotes motor neuron degeneration: prevention by mitochondrial-targeted antioxidants. J. Neurosci. 2008, 28:4115-4122.
104. Shrivastava M., Vivekanandhan S., Pati U., Behari M., Das T.K. Mitochondrial perturbance and execution of apoptosis in platelet mitochondria of patients with amyotrophic lateral sclerosis. Int. J. Neurosci. 2011, 121:149-158.
105. Martin L.J., Gertz B., Pan Y., Price A.C., Molkentin J.D., Chang Q. The mitochondrial permeability transition pore in motor neurons: involvement in the pathobiology of ALS mice. Exp. Neurol. 2009, 218:333-346.
106. Martin L.J. An approach to experimental synaptic pathology using green fluorescent protein-transgenic mice and gene knockout mice to show mitochondrial permeability transition pore-driven excitotoxicity in interneurons and motoneurons. Toxicol. Pathol. 2011, 39:220-233.
107. Li M., Ona V.O., Guégan C., Chen M., Jackson-Lewis V., Andrews L.J., Olszewski A.J., Stieg P.E., Lee J.P., Przedborski S., Friedlander R.M. Functional role of caspase-1 and caspase-3 in an ALS transgenic mouse model. Science 2000, 288:335-339.
108. Verkhratsky A.J., Petersen O.H. Neuronal calcium stores. Cell Calcium 1998, 333-343.
109. Berridge M.J. The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 2002, 32:235-249.
110. Ruiz A., Matute C., Alberdi E. Endoplasmic reticulum Ca(2+) release through ryanodine and IP(3) receptors contributes to neuronal excitotoxicity. Cell Calcium 2009, 46:273-281.
111. Arnaudeau S., Kelley W.L., Walsh J.V., Demaurex N. Mitochondria recycle Ca(2+) to the endoplasmic reticulum and prevent the depletion of neighboring endoplasmic reticulum regions. J. Biol. Chem. 2001, 276:29430-29439.
112. Malhotra J.D., Kaufman R.J. ER stress and its functional link to mitochondria: role in cell survival and death. Cold Spring Harb. Perspect. Biol. 2011, 3:a004424. 10.1101/cshperspect.a004424.
113. Hetz The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol. 2012, 13:89-102. 10.1038/nrm3270.
114. Kikuchi H., Almer G., Yamashita S., Guégan C., Nagai M., Xu Z., Sosunov A.A., McKhann G.M., Przedborski S. Spinal cord endoplasmic reticulum stress associated with a microsomal accumulation of mutant superoxide dismutase-1 in an ALS model. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:6025-6030.
115. Wootz H., Hansson I., Korhonen L., Näpänkangas U., Lindholm D. Caspase-12 cleavage and increased oxidative stress during motoneuron degeneration in transgenic mouse model of ALS. Biochem. Biophys. Res. Commun. 2004, 322:281-286.
116. Kanekura, Nishimoto I., Aiso S., Matsuoka M. Characterization of amyotrophic lateral sclerosis-linked P56S mutation of vesicle-associated membrane protein-associated protein B (VAPB/ALS8). J. Biol. Chem. 2006, 281:30223-30233.
117. Prell T., Lautenschläger J., Witte O.W., Carri M.T., Grosskreutz J. The unfolded protein response in models of human mutant G93A amyotrophic lateral sclerosis. Eur. J. Neurosci. 2012, 35:652-660.
118. Tarabal O., Calderó J., Casas C., Oppenheim R.W., Esquerda J.E. Protein retention in the endoplasmic reticulum, blockade of programmed cell death and autophagy selectively occur in spinal cord motoneurons after glutamate receptor-mediated injury. Mol. Cell. Neurosci. 2005, 29:283-298.
119. McBain C.J., Kleckner N.W., Wyrick S., Dingledine R. Structural requirements for activation of the glycine coagonist site of N-methyl-d-aspartate receptors expressed in Xenopus oocytes. Mol. Pharmacol. 1989, 36:556-565.
120. Fadda, Danysz W., Wroblewski J.T., Costa E. Glycine and d-serine increase the affinity of N-methyl-d-aspartate sensitive glutamate binding sites in rat brain synaptic membranes. Neuropharmacology 1988, 27:1183-1185.
121. Lerma, Zukin R.S., Bennett M.V. Glycine decreases desensitization of N-methyl-d-aspartate (NMDA) receptors expressed in Xenopus oocytes and is required for NMDA responses. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:2354-2358.
122. Nong Y., Huang Y.Q., Ju W., Kalia L.V., Ahmadian G., Wang Y.T., Salter M.W. Glycine binding primes NMDA receptor internalization. Nature 2003, 422:302-307.
123. Compton R.P., Hood W.F., Monahan J.B. Evidence for a functional coupling of the NMDA and glycine recognition sites in synaptic plasma membranes. Eur. J. Pharmacol. 1990, 188:63-70.
124. Panatier, Theodosis D.T., Mothet J.P., Touquet B., Pollegioni L., Poulain D.A., Oliet S.H. Glia-derived d-serine controls NMDA receptor activity and synaptic memory. Cell 2006, 775-784.
125. Shleper, Kartvelishvily E., Wolosker H. d-serine is the dominant endogenous coagonist for NMDA receptor neurotoxicity in organotypic hippocampal slices. J. Neurosci. 2005, 9413-9417.
126. Miya K., Inoue R., Takata Y., Abe M., Natsume R., Sakimura K., Hongou K., Miyawaki T., Mori H. Serine racemase is predominantly localized in neurons in mouse brain. J. Comp. Neurol. 2008, 510:641-654.
127. Wolosker Serine racemase and the serine shuttle between neurons and astrocytes. Biochim. Biophys. Acta 2011, 1814:1558-1566.
128. Henneberger, Bard L., Rusakov D.A. d-Serine: a key to synaptic plasticity?. Int. J. Biochem. Cell Biol. 2012, 44:587-590.
129. Kinney G.G., Sur C., Burno M., Mallorga P.J., Williams J.B., Figueroa D.J., Wittmann M., Lemaire W., Conn P.J. The glycine transporter type 1 inhibitor N-[3-(4'-fluorophenyl)-3-(4'-phenylphenoxy)propyl]sarcosine potentiates NMDA receptor-mediated responses in vivo and produces an antipsychotic profile in rodent behavior. J. Neurosci. 2003, 586-7591.
130. Cubelos, Giménez C., Zafra F. Localization of the GLYT1 glycine transporter at glutamatergic synapses in the rat brain. Cereb. Cortex 2005, 448-459.
131. Martina, Gorfinkel Y., Halman S., Lowe J.A., Periyalwar P., Schmidt C.J., Bergeron R. Glycine transporter type 1 blockade changes NMDA receptor-mediated responses and LTP in hippocampal CA1 pyramidal cells by altering extracellular glycine levels. J. Physiol. 2004, 489-500.
132. Berger A.J., Dieudonné S., Ascher P. Glycine uptake governs glycine site occupancy at NMDA receptors of excitatory synapses. J. Neurophysiol. 1998, 3336-3340.
133. Stevens E.R., Gustafson E.C., Miller R.F. Glycine transport accounts for the differential role of glycine vs. d-serine at NMDA receptor coagonist sites in the salamander retina. Eur. J. Neurosci. 2010, 808-816.
134. Raiteri L., Paolucci E., Prisco S., Raiteri M., Bonanno G. Activation of a glycine transporter on spinal cord neurons causes enhanced glutamate release in a mouse model of amyotrophic lateral sclerosis. Br. J. Pharmacol. 2003, 1021-1025.
135. Rodríguez-Ithurralde, Olivera S., Vincent O., Maruri A. In vivo and in vitro studies of glycine- and glutamate-evoked acetylcholinesterase release from spinal motor neurones: implications for amyotrophic lateral sclerosis/motor neurone disease pathogenesis. J. Neurol. Sci. 1997, 54-61.
136. Chatterton J.E., Awobuluyi M., Premkumar L.S., Takahashi H., Talantova M., Shin Y., Cui J., Tu S., Sevarino K.A., Nakanishi N., Tong G., Lipton S.A., Zhang D. Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 2002, 415:793-798.
137. Awobuluyi M., Yang J., Ye Y., Chatterton J.E., Godzik A., Lipton S.A., Zhang D. Subunit-specific roles of glycine-binding domains in activation of NR1/NR3 N-methyl-d-aspartate receptors. Mol. Pharmacol. 2007, 71:112-122.
138. Sasabe J., Chiba T., Yamada M., Okamoto K., Nishimoto I., Matsuoka M., Aiso S. d-serine is a key determinant of glutamate toxicity in amyotrophic lateral sclerosis. EMBO J. 2007, 4149-4159.
139. Sasabe J., Miyoshi Y., Suzuki M., Mita M., Konno R., Matsuoka M., Hamase K., Aiso S. d-amino acid oxidase controls motoneuron degeneration through d-serine. Proc. Natl. Acad. Sci. U. S. A. 2012, 2012(109):627-632.
140. Mitchell J., Paul P., Chen H.J., Morris A., Payling M., Falchi M., Habgood J., Panoutsou S., Winkler S., Tisato V., Hajitou A., Smith B., Vance C., Shaw C., Mazarakis N.D., de Belleroche J. Familial amyotrophic lateral sclerosis is associated with a mutation in d-amino acid oxidase. Proc. Natl. Acad. Sci. U. S. A. 2010, 7556-7561.
141. Thompson, Marecki J.C., Marinesco S., Labrie V., Roder J.C., Barger S.W., Crow J.P. Paradoxical roles of serine racemase and d-serine in the G93A mSOD1 mouse model of amyotrophic lateral sclerosis. J. Neurochem. 2012, 598-610.
142. Crow J.P., Sampson J.B., Zhuang Y., Thompson J.A., Beckman J.S. Decreased zinc affinity of amyotrophic lateral sclerosis-associated superoxide dismutase mutants leads to enhanced catalysis of tyrosine nitration by peroxynitrite. J. Neurochem. 1997, 1936-1944.
143. Estévez A.G., Crow J.P., Sampson J.B., Reiter C., Zhuang Y., Richardson G.J., Tarpey M.M., Barbeito L., Beckman J.S. Induction of nitric oxide-dependent apoptosis in motor neurons by zinc-deficient superoxide dismutase. Science 1999, 2498-2500.
144. Westbrook G.L., Mayer M.L. Micromolar concentrations of Zn2+ antagonize NMDA and GABA responses of hippocampal neurons. Nature 1987, 640-643.
145. Vogt K., Mellor J., Tong G., Nicoll R. The actions of synaptically released zinc at hippocampal mossy fiber synapses. Neuron 2000, 187-196.
146. Sensi S.L., Paoletti P., Bush A.I., Sekler I. Zinc in the physiology and pathology of the CNS. Nat. Rev. Neurosci. 2009, 780-791.
147. Peters S., Koh J., Choi D.W. Zinc selectively blocks the action of N-methyl-d-aspartate on cortical neurons. Science 1987, 589-593.
148. Low C.M., Zheng F., Lyuboslavsky P., Traynelis S.F. Molecular determinants of coordinated proton and zinc inhibition of N-methyl-d-aspartate NR1/NR2A receptors. Proc. Natl. Acad. Sci. U. S. A. 2000, 11062-11067.
149. Coughenour L.L., Barr B.M. Use of trifluoroperazine isolates a [(3)H]Ifenprodil binding site in rat brain membranes with the pharmacology of the voltage-independent ifenprodil site on N-methyl-d-aspartate receptors containing NR2B subunits. J. Pharmacol. Exp. Ther. 2001, 150-159.
150. Mony L., Kew J.N., Gunthorpe M.J., Paoletti P. Allosteric modulators of NR2B-containing NMDA receptors: molecular mechanisms and therapeutic potential. Br. J. Pharmacol. 2009, 1301-1317.
151. Manzerra, Behrens M.M., Canzoniero L.M., Wang X.Q., Heidinger V., Ichinose T., Yu S.P., Choi D.W. Zinc induces a Src family kinase-mediated up-regulation of NMDA receptor activity and excitotoxicity. Proc. Natl. Acad. Sci. U. S. A. 2001, 11055-11061.
152. Choi D.W., Yokoyama M., Koh J. Zinc neurotoxicity in cortical cell culture. Neuroscience 1988, 67-79.
153. Dineley K.E., Scanlon J.M., Kress G.J., Stout A.K., Reynolds I.J. Astrocytes are more resistant than neurons to the cytotoxic effects of increased [Zn(2+)](i). Neurobiol. Dis. 2000, 310-320.
154. Sensi S.L., Canzoniero L.M., Yu S.P., Ying H.S., Koh J.Y., Kerchner G.A., Choi D.W. Measurement of intracellular free zinc in living cortical neurons: routes of entry. J. Neurosci. 1997, 9554-9564.
155. Yao X. Effect of zinc exposure on HNE and GLT-1 in spinal cord culture. Neurotoxicology 2009, 121-126.
156. Nutini M., Frazzini V., Marini C., Spalloni A., Sensi S.L., Longone P. Zinc pre-treatment enhances NMDAR-mediated excitotoxicity in cultured cortical neurons from SOD1(G93A) mouse, a model of amyotrophic lateral sclerosis. Neuropharmacology 2011, 1200-1208.
157. Jaarsma, Rognoni F., van Duijn W., Verspaget H.W., Haasdijk E.D., Holstege J.C. Cu Zn superoxide dismutase (SOD1) accumulates in vacuolated mitochondria in transgenic mice expressing amyotrophic lateral sclerosis-linked SOD1 mutations. Acta Neuropathol. 2001, 293-305.
158. Pasinelli, Belford M.E., Lennon N., Bacskai B.J., Hyman B.T., Trotti D., Brown R.H. Amyotrophic lateral sclerosis-associated SOD1 mutant proteins bind and aggregate with Bcl-2 in spinal cord mitochondria. Neuron 2004, 19-30.
159. Igarashi K., Kashiwagi K. Characteristics of cellular polyamine transport in prokaryotes and eukaryotes. Plant Physiol. Biochem. 2010, 506-512.
160. Rock D.M., Macdonald R.L. Polyamine regulation of N-methyl-d-aspartate receptor channels. Annu. Rev. Pharmacol. Toxicol. 1995, 463-482.
161. Williams K., Dawson V.L., Romano C., Dichter M.A., Molinoff P.B. Characterization of polyamines having agonist, antagonist, and inverse agonist effects at the polyamine recognition site of the NMDA receptor. Neuron 1990, 199-208.
162. Benveniste M., Mayer M.L. Multiple effects of spermine on N-methyl-d-aspartic acid receptor responses of rat cultured hippocampal neurones. J. Physiol. 1993, 131-163.
163. Williams K., Zappia A.M., Pritchett D.B., Shen Y.M., Molinoff P.B. Sensitivity of the N-methyl-d-aspartate receptor to polyamines is controlled by NR2 subunits. Mol. Pharmacol. 1994, 803-809.
164. Traynelis S.F., Hartley M., Heinemann S.F. Control of proton sensitivity of the NMDA receptor by RNA splicing and polyamines. Science 1995, 873-876.
165. Mott D.D., Doherty J.J., Zhang S., Washburn M.S., Fendley M.J., Lyuboslavsky P., Traynelis S.F., Dingledine R. Phenylethanolamines inhibit NMDA receptors by enhancing proton inhibition. Nat. Neurosci. 1998, 659-667.
166. de Vera N., Martínez E., Sanfeliu C. Spermine induces cell death in cultured human embryonic cerebral cortical neurons through N-methyl-d-aspartate receptor activation. J. Neurosci. Res. 2008, 861-872.
167. Gomes-Trolin, Nygren I., Aquilonius S.M., Askmark H. Increased red blood cell polyamines in ALS and Parkinson's disease. Exp. Neurol. 2002, 515-520.
168. Ekegren T., Gomes-Trolin C., Nygren I., Askmark H. Maintained regulation of polyamines in spinal cord from patients with amyotrophic lateral sclerosis. J. Neurol. Sci. 2004, 49-53.
169. Virgili M., Crochemore C., Peña-Altamira E., Contestabile A. Regional and temporal alterations of ODC/polyamine system during ALS-like neurodegenerative motor syndrome in G93A transgenic mice. Neurochem. Int. 2006, 201-207.
170. Wang, Zhang D. Memantine prolongs survival in an amyotrophic lateral sclerosis mouse model. Eur. J. Neurosci. 2005, 2376-2380.
171. Joo I.S., Hwang D.H., Seok J.I., Shin S.K., Kim S.U. Oral administration of memantine prolongs survival in a transgenic mouse model of amyotrophic lateral sclerosis. J. Clin. Neurol. 2007, 181-186.
172. de Carvalho M., Pinto S., Costa J., Evangelista T., Ohana B., Pinto A. A randomized, placebo-controlled trial of memantine for functional disability in amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 2010, 456-460.
173. Levine T.D., Bowser R., Hank N., Saperstein D. A pilot trial of memantine and riluzole in ALS: correlation to CSF biomarkers. Amyotroph. Lateral Scler. 2010, 514-519.