The role of AMPA receptor-mediated excitotoxicity in ALS: Is deficient RNA editing to blame?

Current Anaesthesia and Critical Care

Volumn 20, Issue 5-6, 2009, Pages 227-235

  Duncan, Kathryn ^a  

^a DURHAM UNIVERSITY   (United Kingdom)

Author keywords

ALS; Calcium; Excitotoxicity; MND; RNA editing

Indexed keywords

AMPA RECEPTOR; CALCIUM ION; COPPER ZINC SUPEROXIDE DISMUTASE; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR 2; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; KAINIC ACID RECEPTOR; MESSENGER RNA; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 2; METABOTROPIC RECEPTOR 3; METABOTROPIC RECEPTOR 4; METABOTROPIC RECEPTOR 5; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NUCLEAR RECEPTOR COACTIVATOR 2; REACTIVE OXYGEN METABOLITE; RILUZOLE; RNA; VASCULOTROPIN A;

AMYOTROPHIC LATERAL SCLEROSIS; CALCIUM CONDUCTANCE; CALCIUM TRANSPORT; DRUG EFFICACY; ENDOPLASMIC RETICULUM; EXCITOTOXICITY; GENE MUTATION; HUMAN; NERVE CELL NECROSIS; NERVE DEGENERATION; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; RNA EDITING; SPINAL CORD MOTONEURON;

EID: 69649104596     PISSN: 09537112     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cacc.2009.07.010     Document Type: Review

References (131)

1. Turner B.J., and Talbot K. Transgenics, toxicity and therapeutics in rodent models of mutant SOD1-mediated familial ALS. Prog Neurobiol 85 1 (2008) 94-134
2. Kunst C.B. Complex genetics of amyotrophic lateral sclerosis. Am J Hum Genet 75 6 (2004) 933-947
3. Hirtz D., Thurman D.J., Gwinn-Hardy K., Mohamed M., Chaudhuri A.R., and Zalutsky R. How common are the "common" neurologic disorders?. Neurology 68 5 (2007) 326-337
4. Przedborski S., Vila M., and Jackson-Lewis V. Neurodegeneration: what is it and where are we?. J Clin Invest 111 1 (2003) 3-10
5. Rosen D.R. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 364 6435 (1993) 362
6. Rowland L.P., and Shneider N.A. Amyotrophic lateral sclerosis. N Engl J Med 344 22 (2001) 1688-1700
7. Turner M.R., Kiernan M.C., Leigh P.N., and Talbot K. Biomarkers in amyotrophic lateral sclerosis. Lancet Neurol 8 1 (2009) 94-109
8. Shaw P.J. Molecular and cellular pathways of neurodegeneration in motor neurone disease. J Neurol Neurosurg Psychiatr 76 8 (2005) 1046-1057
9. Nishihira Y., Tan C.F., Toyoshima Y., Yonemochi Y., Kondo H., Nakajima T., et al. Sporadic amyotrophic lateral sclerosis: widespread multisystem degeneration with TDP-43 pathology in a patient after long-term survival on a respirator. Neuropathology (2009) doi: 10.1111/j.1440-1789.2008.00999.x
10. Brooks B.R. Managing amyotrophic lateral sclerosis: slowing disease progression and improving patient quality of life. Ann Neurol 65 Suppl. 1 (2009) S17-S23
11. Bensimon G., Lacomblez L., and Meininger V. A controlled trial of riluzole in amyotrophic lateral sclerosis. ALS/Riluzole Study Group. N Engl J Med 330 9 (1994) 585-591
12. Traynor B.J., Bruijn L., Conwit R., Beal F., O'Neill G., Fagan S.C., et al. Neuroprotective agents for clinical trials in ALS: a systematic assessment. Neurology 67 1 (2006) 20-27
13. Van Den Bosch L., Van Damme P., Bogaert E., and Robberecht W. The role of excitotoxicity in the pathogenesis of amyotrophic lateral sclerosis. Biochim Biophys Acta 1762 11-12 (2006) 1068-1082
14. Lipton S.A., and Rosenberg P.A. Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med 330 9 (1994) 613-622
15. Matute C., Alberdi E., Domercq M., Perez-Cerda F., Perez-Samartin A., and Sanchez-Gomez M.V. The link between excitotoxic oligodendroglial death and demyelinating diseases. Trends Neurosci 24 4 (2001) 224-230
16. Arundine M., and Tymianski M. Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium 34 4-5 (2003) 325-337
17. Choi D.W. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1 8 (1988) 623-634
18. MacDermott A.B., Mayer M.L., Westbrook G.L., Smith S.J., and Barker J.L. NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature 321 6069 (1986) 519-522
19. Kwak S., and Weiss J.H. Calcium-permeable AMPA channels in neurodegenerative disease and ischemia. Curr Opin Neurobiol 16 3 (2006) 281-287
20. Mattson M.P. Neuroprotective signal transduction: relevance to stroke. Neurosci Biobehav Rev 21 2 (1997) 193-206
21. Arundine M., and Tymianski M. Molecular mechanisms of glutamate-dependent neurodegeneration in ischemia and traumatic brain injury. Cell Mol Life Sci 61 6 (2004) 657-668
22. Liu Y., Wong T.P., Aarts M., Rooyakkers A., Liu L., Lai T.W., et al. NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo. J Neurosci 27 11 (2007) 2846-2857
23. Takuma H., Kwak S., Yoshizawa T., and Kanazawa I. Reduction of GluR2 RNA editing, a molecular change that increases calcium influx through AMPA receptors, selective in the spinal ventral gray of patients with amyotrophic lateral sclerosis. Ann Neurol 46 6 (1999) 806-815
24. Spencer P.S., Roy D.N., Ludolph A., Hugon J., Dwivedi M.P., and Schaumburg H.H. Lathyrism: evidence for role of the neuroexcitatory aminoacid BOAA. Lancet 2 8515 (1986) 1066-1067
25. Teitelbaum J.S., Zatorre R.J., Carpenter S., Gendron D., Evans A.C., Gjedde A., et al. Neurologic sequelae of domoic acid intoxication due to the ingestion of contaminated mussels. N Engl J Med 322 25 (1990) 1781-1787
26. Spencer P.S., Hugon J., Ludolph A., Nunn P.B., Ross S.M., Roy D.N., et al. Discovery and partial characterization of primate motor-system toxins. Ciba Found Symp 126 (1987) 221-238
27. Weiss J.H., Koh J.Y., and Choi D.W. Neurotoxicity of beta-N-methylamino-L-alanine (BMAA) and beta-N-oxalylamino-L-alanine (BOAA) on cultured cortical neurons. Brain Res 497 1 (1989) 64-71
28. Carriedo S.G., Yin H.Z., and Weiss J.H. Motor neurons are selectively vulnerable to AMPA/kainate receptor-mediated injury in vitro. J Neurosci 16 13 (1996) 4069-4079
29. Hirata A., Nakamura R., Kwak S., Nagata N., and Kamakura K. AMPA receptor-mediated slow neuronal death in the rat spinal cord induced by long-term blockade of glutamate transporters with THA. Brain Res 771 1 (1997) 37-44
30. Nakamura R., Kamakura K., and Kwak S. Late-onset selective neuronal damage in the rat spinal cord induced by continuous intrathecal administration of AMPA. Brain Res 654 2 (1994) 279-285
31. Sun H., Kawahara Y., Ito K., Kanazawa I., and Kwak S. Slow and selective death of spinal motor neurons in vivo by intrathecal infusion of kainic acid: implications for AMPA receptor-mediated excitotoxicity in ALS. J Neurochem 98 3 (2006) 782-791
32. Van Den Bosch L., Vandenberghe W., Klaassen H., Van Houtte E., and Robberecht W. Ca(2+)-permeable AMPA receptors and selective vulnerability of motor neurons. J Neurol Sci 180 1-2 (2000) 29-34
33. Ugolini A., Corsi M., and Bordi F. Potentiation of NMDA and AMPA responses by group I mGluR in spinal cord motoneurons. Neuropharmacology 36 8 (1997) 1047-1055
34. Anneser J.M., Horstmann S., Weydt P., and Borasio G.D. Activation of metabotropic glutamate receptors delays apoptosis of chick embryonic motor neurons in vitro. Neuroreport 9 9 (1998) 2039-2043
35. Pizzi M., Benarese M., Boroni F., Goffi F., Valerio A., and Spano P.F. Neuroprotection by metabotropic glutamate receptor agonists on kainate-induced degeneration of motor neurons in spinal cord slices from adult rat. Neuropharmacology 39 5 (2000) 903-910
36. Tomiyama M., Kimura T., Maeda T., Tanaka H., Furusawa K., Kurahashi K., et al. Expression of metabotropic glutamate receptor mRNAs in the human spinal cord: implications for selective vulnerability of spinal motor neurons in amyotrophic lateral sclerosis. J Neurol Sci 189 1-2 (2001) 65-69
37. Williams T.L., Day N.C., Ince P.G., Kamboj R.K., and Shaw P.J. Calcium-permeable alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors: a molecular determinant of selective vulnerability in amyotrophic lateral sclerosis. Ann Neurol 42 2 (1997) 200-207
38. Carriedo S.G., Yin H.Z., Sensi S.L., and Weiss J.H. Rapid Ca2+ entry through Ca2+-permeable AMPA/kainate channels triggers marked intracellular Ca2+ rises and consequent oxygen radical production. J Neurosci 18 19 (1998) 7727-7738
39. Carriedo S.G., Sensi S.L., Yin H.Z., and Weiss J.H. AMPA exposures induce mitochondrial Ca(2+) overload and ROS generation in spinal motor neurons in vitro. J Neurosci 20 1 (2000) 240-250
40. Elliott J.L., and Snider W.D. Parvalbumin is a marker of ALS-resistant motor neurons. Neuroreport 6 3 (1995) 449-452
41. Ince P., Stout N., Shaw P., Slade J., Hunziker W., Heizmann C.W., et al. Parvalbumin and calbindin D-28k in the human motor system and in motor neuron disease. Neuropathol Appl Neurobiol 19 4 (1993) 291-299
42. Alexianu M.E., Ho B.K., Mohamed A.H., La Bella V., Smith R.G., and Appel S.H. The role of calcium-binding proteins in selective motoneuron vulnerability in amyotrophic lateral sclerosis. Ann Neurol 36 6 (1994) 846-858
43. Van Den Bosch L., Schwaller B., Vleminckx V., Meijers B., Stork S., Ruehlicke T., et al. Protective effect of parvalbumin on excitotoxic motor neuron death. Exp Neurol 174 2 (2002) 150-161
44. Beers D.R., Ho B.K., Siklos L., Alexianu M.E., Mosier D.R., Mohamed A.H., et al. Parvalbumin overexpression alters immune-mediated increases in intracellular calcium, and delays disease onset in a transgenic model of familial amyotrophic lateral sclerosis. J Neurochem 79 3 (2001) 499-509
45. Laslo P., Lipski J., Nicholson L.F., Miles G.B., and Funk G.D. Calcium binding proteins in motoneurons at low and high risk for degeneration in ALS. Neuroreport 11 15 (2000) 3305-3308
46. Winsky L., and Kuznicki J. Antibody recognition of calcium-binding proteins depends on their calcium-binding status. J Neurochem 66 2 (1996) 764-771
47. Grosskreutz J., Haastert K., Dewil M., Van Damme P., Callewaert G., Robberecht W., et al. Role of mitochondria in kainate-induced fast Ca2+ transients in cultured spinal motor neurons. Cell Calcium 42 1 (2007) 59-69
48. Martin L.J., Gertz B., Pan Y., Price A.C., Molkentin J.D., and Chang Q. The mitochondrial permeability transition pore in motor neurons: involvement in the pathobiology of ALS mice. Exp Neurol 218 2 (2009) 333-346
49. Nakagawa T., Cheng Y., Ramm E., Sheng M., and Walz T. Structure and different conformational states of native AMPA receptor complexes. Nature 433 7025 (2005) 545-549
50. Hollmann M., Hartley M., and Heinemann S. Ca2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 252 5007 (1991) 851-853
51. Hume R.I., Dingledine R., and Heinemann S.F. Identification of a site in glutamate receptor subunits that controls calcium permeability. Science 253 5023 (1991) 1028-1031
52. Burnashev N., Monyer H., Seeburg P.H., and Sakmann B. Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 8 1 (1992) 189-198
53. Keinanen K., Wisden W., Sommer B., Werner P., Herb A., Verdoorn T.A., et al. A family of AMPA-selective glutamate receptors. Science 249 4968 (1990) 556-560
54. Verdoorn T.A., Burnashev N., Monyer H., Seeburg P.H., and Sakmann B. Structural determinants of ion flow through recombinant glutamate receptor channels. Science 252 5013 (1991) 1715-1718
55. Sommer B., Kohler M., Sprengel R., and Seeburg P.H. RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67 1 (1991) 11-19
56. Jonas P., and Burnashev N. Molecular mechanisms controlling calcium entry through AMPA-type glutamate receptor channels. Neuron 15 5 (1995) 987-990
57. Peng P.L., Zhong X., Tu W., Soundarapandian M.M., Molner P., Zhu D., et al. ADAR2-dependent RNA editing of AMPA receptor subunit GluR2 determines vulnerability of neurons in forebrain ischemia. Neuron 49 5 (2006) 719-733
58. Riedmann E.M., Schopoff S., Hartner J.C., and Jantsch M.F. Specificity of ADAR-mediated RNA editing in newly identified targets. RNA 14 6 (2008) 1110-1118
59. Melcher T., Maas S., Herb A., Sprengel R., Seeburg P.H., and Higuchi M. A mammalian RNA editing enzyme. Nature 379 6564 (1996) 460-464
60. Higuchi M., Single F.N., Kohler M., Sommer B., Sprengel R., and Seeburg P.H. RNA editing of AMPA receptor subunit GluR-B: a base-paired intron-exon structure determines position and efficiency. Cell 75 7 (1993) 1361-1370
61. Seeburg P.H. A-to-I editing: new and old sites, functions and speculations. Neuron 35 1 (2002) 17-20
62. Ryman K., Fong N., Bratt E., Bentley D.L., and Ohman M. The C-terminal domain of RNA Pol II helps ensure that editing precedes splicing of the GluR-B transcript. RNA 13 7 (2007) 1071-1078
63. Higuchi M., Maas S., Single F.N., Hartner J., Rozov A., Burnashev N., et al. Point mutation in an AMPA receptor gene rescues lethality in mice deficient in the RNA-editing enzyme ADAR2. Nature 406 6791 (2000) 78-81
64. Carlson N.G., Howard J., Gahring L.C., and Rogers S.W. RNA editing (Q/R site) and flop/flip splicing of AMPA receptor transcripts in young and old brains. Neurobiol Aging 21 4 (2000) 599-606
65. Midgett C.R., and Madden D.R. The quaternary structure of a calcium-permeable AMPA receptor: conservation of shape and symmetry across functionally distinct subunit assemblies. J Mol Biol 382 3 (2008) 578-584
66. Seeburg P.H., Single F., Kuner T., Higuchi M., and Sprengel R. Genetic manipulation of key determinants of ion flow in glutamate receptor channels in the mouse. Brain Res 907 1-2 (2001) 233-243
67. Greger I.H., Khatri L., and Ziff E.B. RNA editing at arg607 controls AMPA receptor exit from the endoplasmic reticulum. Neuron 34 5 (2002) 759-772
68. Greger I.H., Khatri L., Kong X., and Ziff E.B. AMPA receptor tetramerization is mediated by Q/R editing. Neuron 40 4 (2003) 763-774
69. Greger I.H., Akamine P., Khatri L., and Ziff E.B. Developmentally regulated, combinatorial RNA processing modulates AMPA receptor biogenesis. Neuron 51 1 (2006) 85-97
70. Sun Y., Olson R., Horning M., Armstrong N., Mayer M., and Gouaux E. Mechanism of glutamate receptor desensitization. Nature 417 6886 (2002) 245-253
71. Zamanillo D., Sprengel R., Hvalby O., Jensen V., Burnashev N., Rozov A., et al. Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 284 5421 (1999) 1805-1811
72. Greger I.H., and Esteban J.A. AMPA receptor biogenesis and trafficking. Curr Opin Neurobiol 17 3 (2007) 289-297
73. Coleman S.K., Moykkynen T., Jouppila A., Koskelainen S., Rivera C., Korpi E.R., et al. Agonist occupancy is essential for forward trafficking of AMPA receptors. J Neurosci 29 2 (2009) 303-312
74. Vandenberghe W., and Bredt D.S. Early events in glutamate receptor trafficking. Curr Opin Cell Biol 16 2 (2004) 134-139
75. Dingledine R., Borges K., Bowie D., and Traynelis S.F. The glutamate receptor ion channels. Pharmacol Rev 51 1 (1999) 7-61
76. Bredt D.S., and Nicoll R.A. AMPA receptor trafficking at excitatory synapses. Neuron 40 2 (2003) 361-379
77. Liu S.J., and Cull-Candy S.G. Subunit interaction with PICK and GRIP controls Ca2+ permeability of AMPARs at cerebellar synapses. Nat Neurosci 8 6 (2005) 768-775
78. Barry M.F., and Ziff E.B. Receptor trafficking and the plasticity of excitatory synapses. Curr Opin Neurobiol 12 3 (2002) 279-286
79. Dong H., O'Brien R.J., Fung E.T., Lanahan A.A., Worley P.F., and Huganir R.L. GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature 386 6622 (1997) 279-284
80. DeSouza S., Fu J., States B.A., and Ziff E.B. Differential palmitoylation directs the AMPA receptor-binding protein ABP to spines or to intracellular clusters. J Neurosci 22 9 (2002) 3493-3503
81. Bassani S., Valnegri P., Beretta F., and Passafaro M. The GluR2 subunit of AMPA receptors: synaptic role. Neuroscience 158 1 (2009) 55-61
82. Daw M.I., Chittajallu R., Bortolotto Z.A., Dev K.K., Duprat F., Henley J.M., et al. PDZ proteins interacting with C-terminal GluR2/3 are involved in a PKC-dependent regulation of AMPA receptors at hippocampal synapses. Neuron 28 3 (2000) 873-886
83. Haglerod C., Kapic A., Boulland J.L., Hussain S., Holen T., Skare O., et al. Protein interacting with C kinase 1 (PICK1) and GluR2 are associated with presynaptic plasma membrane and vesicles in hippocampal excitatory synapses. Neuroscience 158 1 (2009) 242-252
84. Nishimune A., Isaac J.T., Molnar E., Noel J., Nash S.R., Tagaya M., et al. NSF binding to GluR2 regulates synaptic transmission. Neuron 21 1 (1998) 87-97
85. Mahajan S.S., and Ziff E.B. Novel toxicity of the unedited GluR2 AMPA receptor subunit dependent on surface trafficking and increased Ca2+-permeability. Mol Cell Neurosci 35 3 (2007) 470-481
86. Hanley J.G., Khatri L., Hanson P.I., and Ziff E.B. NSF ATPase and alpha-/beta-SNAPs disassemble the AMPA receptor-PICK1 complex. Neuron 34 1 (2002) 53-67
87. Ralph G.S., Bienemann A., Ma J., Tan H.K., Noel J., Henley J.M., et al. Disruption of the GluR2-NSF interaction protects primary hippocampal neurons from ischemic stress. Mol Cell Neurosci 17 4 (2001) 662-670
88. Hu B.R., Park M., Martone M.E., Fischer W.H., Ellisman M.H., and Zivin J.A. Assembly of proteins to postsynaptic densities after transient cerebral ischemia. J Neurosci 18 2 (1998) 625-633
89. Liu B., Liao M., Mielke J.G., Ning K., Chen Y., Li L., et al. Ischemic insults direct glutamate receptor subunit 2-lacking AMPA receptors to synaptic sites. J Neurosci 26 20 (2006) 5309-5319
90. Luscher C., Xia H., Beattie E.C., Carroll R.C., von Zastrow M., Malenka R.C., et al. Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24 3 (1999) 649-658
91. Tomita S., Chen L., Kawasaki Y., Petralia R.S., Wenthold R.J., Nicoll R.A., et al. Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins. J Cell Biol 161 4 (2003) 805-816
92. Chen L., Chetkovich D.M., Petralia R.S., Sweeney N.T., Kawasaki Y., Wenthold R.J., et al. Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408 6815 (2000) 936-943
93. Cuadra A.E., Kuo S.H., Kawasaki Y., Bredt D.S., and Chetkovich D.M. AMPA receptor synaptic targeting regulated by stargazin interactions with the Golgi-resident PDZ protein nPIST. J Neurosci 24 34 (2004) 7491-7502
94. Korber C., Werner M., Hoffmann J., Sager C., Tietze M., Schmid S.M., et al. Stargazin interaction with alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate (AMPA) receptors is critically dependent on the amino acid at the narrow constriction of the ion channel. J Biol Chem 282 26 (2007) 18758-18766
95. Zhu J.J., Esteban J.A., Hayashi Y., and Malinow R. Postnatal synaptic potentiation: delivery of GluR4-containing AMPA receptors by spontaneous activity. Nat Neurosci 3 11 (2000) 1098-1106
96. Wenthold R.J., Petralia R.S., Blahos II J., and Niedzielski A.S. Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J Neurosci 16 6 (1996) 1982-1989
97. Kawahara Y., and Kwak S. Excitotoxicity and ALS: what is unique about the AMPA receptors expressed on spinal motor neurons?. Amyotroph Lateral Scler Other Motor Neuron Disord 6 3 (2005) 131-144
98. Shi S., Hayashi Y., Esteban J.A., and Malinow R. Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105 3 (2001) 331-343
99. Esteban J.A., Shi S.H., Wilson C., Nuriya M., Huganir R.L., and Malinow R. PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6 2 (2003) 136-143
100. Garry E.M., Moss A., Rosie R., Delaney A., Mitchell R., and Fleetwood-Walker S.M. Specific involvement in neuropathic pain of AMPA receptors and adapter proteins for the GluR2 subunit. Mol Cell Neurosci 24 1 (2003) 10-22
101. Leonoudakis D., Zhao P., and Beattie E.C. Rapid tumor necrosis factor alpha-induced exocytosis of glutamate receptor 2-lacking AMPA receptors to extrasynaptic plasma membrane potentiates excitotoxicity. J Neurosci 28 9 (2008) 2119-2130
102. Zhao P., Ignacio S., Beattie E.C., and Abood M.E. Altered presymptomatic AMPA and cannabinoid receptor trafficking in motor neurons of ALS model mice: implications for excitotoxicity. Eur J Neurosci 27 3 (2008) 572-579
103. Tomiyama M., Rodriguez-Puertas R., Cortes R., Christnacher A., Sommer B., Pazos A., et al. Differential regional distribution of AMPA receptor subunit messenger RNAs in the human spinal cord as visualized by in situ hybridization. Neuroscience 75 3 (1996) 901-915
104. Bar-Peled O., O'Brien R.J., Morrison J.H., and Rothstein J.D. Cultured motor neurons possess calcium-permeable AMPA/kainate receptors. Neuroreport 10 4 (1999) 855-859
105. Kawahara Y., Kwak S., Sun H., Ito K., Hashida H., Aizawa H., et al. Human spinal motoneurons express low relative abundance of GluR2 mRNA: an implication for excitotoxicity in ALS. J Neurochem 85 3 (2003) 680-689
106. Pieri M., Gaetti C., Spalloni A., Cavalcanti S., Mercuri N., Bernardi G., et al. Alpha-amino-3-hydroxy-5-methyl-isoxazole-4-propionate receptors in spinal cord motor neurons are altered in transgenic mice overexpressing human Cu,Zn superoxide dismutase (Gly93→Ala) mutation. Neuroscience 122 1 (2003) 47-58
107. Rembach A., Turner B.J., Bruce S., Cheah I.K., Scott R.L., Lopes E.C., et al. Antisense peptide nucleic acid targeting GluR3 delays disease onset and progression in the SOD1 G93A mouse model of familial ALS. J Neurosci Res 77 4 (2004) 573-582
108. Tateno M., Sadakata H., Tanaka M., Itohara S., Shin R.M., Miura M., et al. Calcium-permeable AMPA receptors promote misfolding of mutant SOD1 protein and development of amyotrophic lateral sclerosis in a transgenic mouse model. Hum Mol Genet 13 19 (2004) 2183-2196
109. Petri S., Schmalbach S., Grosskreutz J., Krampfl K., Grothe C., Dengler R., et al. The cellular mRNA expression of GABA and glutamate receptors in spinal motor neurons of SOD1 mice. J Neurol Sci 238 1-2 (2005) 25-30
110. Kawahara Y., Ito K., Sun H., Aizawa H., Kanazawa I., and Kwak S. Glutamate receptors: RNA editing and death of motor neurons. Nature 427 6977 (2004) 801
111. Pellegrini-Giampietro D.E., Zukin R.S., Bennett M.V., Cho S., and Pulsinelli W.A. Switch in glutamate receptor subunit gene expression in CA1 subfield of hippocampus following global ischemia in rats. Proc Natl Acad Sci U S A 89 21 (1992) 10499-10503
112. Pellegrini-Giampietro D.E., Pulsinelli W.A., and Zukin R.S. NMDA and non-NMDA receptor gene expression following global brain ischemia in rats: effect of NMDA and non-NMDA receptor antagonists. J Neurochem 62 3 (1994) 1067-1073
113. Gorter J.A., Petrozzino J.J., Aronica E.M., Rosenbaum D.M., Opitz T., Bennett M.V., et al. Global ischemia induces downregulation of GluR2 mRNA and increases AMPA receptor-mediated Ca2+ influx in hippocampal CA1 neurons of gerbil. J Neurosci 17 16 (1997) 6179-6188
114. Pollard H., Heron A., Moreau J., Ben-Ari Y., and Khrestchatisky M. Alterations of the GluR-B AMPA receptor subunit flip/flop expression in kainate-induced epilepsy and ischemia. Neuroscience 57 3 (1993) 545-554
115. Friedman L.K., Segal M., and Veliskova J. GluR2 knockdown reveals a dissociation between [Ca2+]i surge and neurotoxicity. Neurochem Int 43 3 (2003) 179-189
116. Sanchez R.M., Koh S., Rio C., Wang C., Lamperti E.D., Sharma D., et al. Decreased glutamate receptor 2 expression and enhanced epileptogenesis in immature rat hippocampus after perinatal hypoxia-induced seizures. J Neurosci 21 20 (2001) 8154-8163
117. Van Damme P., Bogaert E., Dewil M., Hersmus N., Kiraly D., Scheveneels W., et al. Astrocytes regulate GluR2 expression in motor neurons and their vulnerability to excitotoxicity. Proc Natl Acad Sci U S A 104 37 (2007) 14825-14830
118. Bogaert E., Van Damme P., Poesen K., Dhondt J., Hersmus N., Kiraly D., et al. VEGF protects motor neurons against excitotoxicity by upregulation of GluR2. Neurobiol Aging (2009) doi: 10.1016/j.neurobiolaging.2008.12.007.
119. Kuner T., Beck C., Sakmann B., and Seeburg P.H. Channel-lining residues of the AMPA receptor M2 segment: structural environment of the Q/R site and identification of the selectivity filter. J Neurosci 21 12 (2001) 4162-4172
120. Anzai T., Tsuzuki K., Yamada N., Hayashi T., Iwakuma M., Inada K., et al. Overexpression of Ca2+-permeable AMPA receptor promotes delayed cell death of hippocampal CA1 neurons following transient forebrain ischemia. Neurosci Res 46 1 (2003) 41-51
121. Liu S., Lau L., Wei J., Zhu D., Zou S., Sun H.S., et al. Expression of Ca(2+)-permeable AMPA receptor channels primes cell death in transient forebrain ischemia. Neuron 43 1 (2004) 43-55
122. Kask K., Zamanillo D., Rozov A., Burnashev N., Sprengel R., and Seeburg P.H. The AMPA receptor subunit GluR-B in its Q/R site-unedited form is not essential for brain development and function. Proc Natl Acad Sci U S A 95 23 (1998) 13777-13782
123. Brusa R., Zimmermann F., Koh D.S., Feldmeyer D., Gass P., Seeburg P.H., et al. Early-onset epilepsy and postnatal lethality associated with an editing-deficient GluR-B allele in mice. Science 270 5242 (1995) 1677-1680
124. Jia Z., Agopyan N., Miu P., Xiong Z., Henderson J., Gerlai R., et al. Enhanced LTP in mice deficient in the AMPA receptor GluR2. Neuron 17 5 (1996) 945-956
125. Feldmeyer D., Kask K., Brusa R., Kornau H.C., Kolhekar R., Rozov A., et al. Neurological dysfunctions in mice expressing different levels of the Q/R site-unedited AMPAR subunit GluR-B. Nat Neurosci 2 1 (1999) 57-64
126. Kuner R., Groom A.J., Bresink I., Kornau H.C., Stefovska V., Muller G., et al. Late-onset motoneuron disease caused by a functionally modified AMPA receptor subunit. Proc Natl Acad Sci U S A 102 16 (2005) 5826-5831
127. Kwak S., and Kawahara Y. Deficient RNA editing of GluR2 and neuronal death in amyotropic lateral sclerosis. J Mol Med 83 2 (2005) 110-120
128. Lipton S.A. Sporadic ALS: blame it on the editor. Nat Med 10 4 (2004) 347
129. Engelhardt J.I., Siklos L., Komuves L., Smith R.G., and Appel S.H. Antibodies to calcium channels from ALS patients passively transferred to mice selectively increase intracellular calcium and induce ultrastructural changes in motoneurons. Synapse 20 3 (1995) 185-199
130. Schmidt H., Arendt O., Brown E.B., Schwaller B., and Eilers J. Parvalbumin is freely mobile in axons, somata and nuclei of cerebellar Purkinje neurones. J Neurochem 100 3 (2007) 727-735
131. Kawahara Y., Sun H., Ito K., Hideyama T., Aoki M., Sobue G., et al. Underediting of GluR2 mRNA, a neuronal death inducing molecular change in sporadic ALS, does not occur in motor neurons in ALS1 or SBMA. Neurosci Res 54 1 (2006) 11-14