Novel toxicity of the unedited GluR2 AMPA receptor subunit dependent on surface trafficking and increased Ca2+-permeability

Molecular and Cellular Neuroscience

Volumn 35, Issue 3, 2007, Pages 470-481

  Mahajan, S S ^a   Ziff, E B ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AMPA receptor; Excitotoxicity; RNA editing; Trafficking

Indexed keywords

AMPA RECEPTOR; CALCIUM; GLUTAMATE RECEPTOR 2;

ANIMAL CELL; ARTICLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; EMBRYO; EXCITOTOXICITY; HIPPOCAMPUS; NERVE CELL; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT;

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; CALCIUM; CELL DEATH; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO; EXCITATORY AMINO ACID AGONISTS; HIPPOCAMPUS; IN SITU NICK-END LABELING; MUTAGENESIS; NEURONS; PERMEABILITY; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; SINDBIS VIRUS; TIME FACTORS; TRANS-ACTIVATION (GENETICS);

EID: 34250904342     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2007.04.006     Document Type: Article

References (79)

1. Akbarian S., Smith M.A., and Jones E.G. Editing for an AMPA receptor subunit RNA in prefrontal cortex and striatum in Alzheimer's disease, Huntington's disease and schizophrenia. Brain Res. 699 (1995) 297-304
2. 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 (1994) 846-858
3. Arundine M., and Tymianski M. Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium 34 (2003) 325-337
4. Arundine M., and Tymianski M. Molecular mechanisms of glutamate-dependent neurodegeneration in ischemia and traumatic brain injury. Cell. Mol. Life Sci. 61 (2004) 657-668
5. Barry M.F., and Ziff E.B. Receptor trafficking and the plasticity of excitatory synapses. Curr. Opin. Neurobiol. 12 (2002) 279-286
6. Bredt D.S., and Nicoll R.A. AMPA receptor trafficking at excitatory synapses. Neuron 40 (2003) 361-379
7. Bredt D.S., and Snyder S.H. Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 9030-9033
8. Brusa R., Zimmermann F., Koh D.S., Feldmeyer D., Gass P., Seeburg P.H., and Sprengel R. Early-onset epilepsy and postnatal lethality associated with an editing-deficient GluR-B allele in mice. Science 270 (1995) 1677-1680
9. Choi D.W. Calcium-mediated neurotoxicity: relationship to specific channel types and role in ischemic damage. Trends Neurosci. 11 (1988) 465-469
10. Cleveland D.W., and Rothstein J.D. From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat. Rev., Neurosci. 2 (2001) 806-819
11. Coan E.J., and Collingridge G.L. Magnesium ions block an N-methyl-d-aspartate receptor-mediated component of synaptic transmission in rat hippocampus. Neurosci. Lett. 53 (1985) 21-26
12. Dawson V.L., and Dawson T.M. Nitric oxide in neurodegeneration. Prog. Brain Res. 118 (1998) 215-229
13. 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 (2002) 3493-3503
14. Dingledine R., Borges K., Bowie D., and Traynelis S.F. The glutamate receptor ion channels. Pharmacol. Rev. 51 (1999) 7-61
15. 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 (1997) 279-284
16. Feldmeyer D., Kask K., Brusa R., Kornau H.C., Kolhekar R., Rozov A., Burnashev N., Jensen V., Hvalby O., Sprengel R., and Seeburg P.H. Neurological dysfunctions in mice expressing different levels of the Q/R site-unedited AMPAR subunit GluR-B. Nat. Neurosci. 2 (1999) 57-64
17. Gardner S.M., Takamiya K., Xia J., Suh J.G., Johnson R., Yu S., and Huganir R.L. Calcium-permeable AMPA receptor plasticity is mediated by subunit-specific interactions with PICK1 and NSF. Neuron 45 (2005) 903-915
18. Geiger J.R., Melcher T., Koh D.S., Sakmann B., Seeburg P.H., Jonas P., and Monyer H. Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15 (1995) 193-204
19. Ghadge G.D., Lee J.P., Bindokas V.P., Jordan J., Ma L., Miller R.J., and Roos R.P. Mutant superoxide dismutase-1-linked familial amyotrophic lateral sclerosis: molecular mechanisms of neuronal death and protection. J. Neurosci. 17 (1997) 8756-8766
20. Greene J.G., and Greenamyre J.T. Manipulation of membrane potential modulates malonate-induced striatal excitotoxicity in vivo. J. Neurochem. 66 (1996) 637-643
21. Greger I.H., Khatri L., Kong X., and Ziff E.B. AMPA receptor tetramerization is mediated by Q/R editing. Neuron 40 (2003) 763-774
22. Greger I.H., Khatri L., and Ziff E.B. RNA editing at arg607 controls AMPA receptor exit from the endoplasmic reticulum. Neuron 34 (2002) 759-772
23. 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 (2002) 53-67
24. Hayashi Y., Shi S.H., Esteban J.A., Piccini A., Poncer J.C., and Malinow R. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287 (2000) 2262-2267
25. Herron C.E., Lester R.A., Coan E.J., and Collingridge G.L. Frequency-dependent involvement of NMDA receptors in the hippocampus: a novel synaptic mechanism. Nature 322 (1986) 265-268
26. Hollmann M., and Heinemann S. Cloned glutamate receptors. Annu. Rev. Neurosci. 17 (1994) 31-108
27. Ince P., Stout N., Shaw P., Slade J., Hunziker W., Heizmann C.W., and Baimbridge K.G. Parvalbumin and calbindin D-28k in the human motor system and in motor neuron disease. Neuropathol. Appl. Neurobiol. 19 (1993) 291-299
28. Jia Z., Agopyan N., Miu P., Xiong Z., Henderson J., Gerlai R., Taverna F.A., Velumian A., MacDonald J., Carlen P., Abramow-Newerly W., and Roder J. Enhanced LTP in mice deficient in the AMPA receptor GluR2. Neuron 17 (1996) 945-956
29. Kamphuis W., and Lopes da Silva F.H. Editing status at the Q/R site of glutamate receptor-A, -B, -5 and -6 subunit mRNA in the hippocampal kindling model of epilepsy. Brain Res. Mol. Brain Res. 29 (1995) 35-42
30. Kawahara Y., Ito K., Sun H., Aizawa H., Kanazawa I., and Kwak S. Glutamate receptors: RNA editing and death of motor neurons. Nature 427 (2004) 801
31. Kawahara Y., Ito K., Sun H., Kanazawa I., and Kwak S. Low editing efficiency of GluR2 mRNA is associated with a low relative abundance of ADAR2 mRNA in white matter of normal human brain. Eur. J. Neurosci. 18 (2003) 23-33
32. Kortenbruck G., Berger E., Speckmann E.J., and Musshoff U. RNA editing at the Q/R site for the glutamate receptor subunits GLUR2, GLUR5, and GLUR6 in hippocampus and temporal cortex from epileptic patients. Neurobiol. Dis. 8 (2001) 459-468
33. Kuner R., Groom A.J., Bresink I., Kornau H.C., Stefovska V., Muller G., Hartmann B., Tschauner K., Waibel S., Ludolph A.C., Ikonomidou C., Seeburg P.H., and Turski L. Late-onset motoneuron disease caused by a functionally modified AMPA receptor subunit. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 5826-5831
34. Kuner R., Groom A.J., Muller G., Kornau H.C., Stefovska V., Bresink I., Hartmann B., Tschauner K., Waibel S., Ludolph A.C., Ikonomidou C., Seeburg P.H., and Turski L. Mechanisms of disease: motoneuron disease aggravated by transgenic expression of a functionally modified AMPA receptor subunit. Ann. N.Y. Acad. Sci. 1053 (2005) 269-286
35. Lee S.H., Liu L., Wang Y.T., and Sheng M. Clathrin adaptor AP2 and NSF interact with overlapping sites of GluR2 and play distinct roles in AMPA receptor trafficking and hippocampal LTD. Neuron 36 (2002) 661-674
36. Liu S.J., and Cull-Candy S.G. Subunit interaction with PICK and GRIP controls Ca(2+) permeability of AMPARs at cerebellar synapses. Nat. Neurosci. 8 (2005) 768-775
37. Liu S.Q., and Cull-Candy S.G. Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature 405 (2000) 454-458
38. Lu W., and Ziff E.B. PICK1 interacts with ABP/GRIP to regulate AMPA receptor trafficking. Neuron 47 (2005) 407-421
39. Maas S., Patt S., Schrey M., and Rich A. Underediting of glutamate receptor GluR-B mRNA in malignant gliomas. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 14687-14692
40. Malenka R.C., and Nicoll R.A. NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms. Trends Neurosci. 16 (1993) 521-527
41. Malinow R., and Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25 (2002) 103-126
42. Mayer M.L., Westbrook G.L., and Guthrie P.B. Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones. Nature 309 (1984) 261-263
43. McDonald J.W., Althomsons S.P., Hyrc K.L., Choi D.W., and Goldberg M.P. Oligodendrocytes from forebrain are highly vulnerable to AMPA/kainate receptor-mediated excitotoxicity. Nat. Med. 4 (1998) 291-297
44. Nishimune A., Isaac J.T., Molnar E., Noel J., Nash S.R., Tagaya M., Collingridge G.L., Nakanishi S., and Henley J.M. NSF binding to GluR2 regulates synaptic transmission. Neuron 21 (1998) 87-97
45. Noel J., Ralph G.S., Pickard L., Williams J., Molnar E., Uney J.B., Collingridge G.L., and Henley J.M. Surface expression of AMPA receptors in hippocampal neurons is regulated by an NSF-dependent mechanism. Neuron 23 (1999) 365-376
46. Nutt S.L., and Kamboj R.K. Differential RNA editing efficiency of AMPA receptor subunit GluR-2 in human brain. Neuroreport 5 (1994) 1679-1683
47. Osten P., and Ziff E.B. AMPA receptor forms a biochemically functional complex with NSF and alpha- and beta-SNAPs. Ann. N. Y. Acad. Sci. 868 (1999) 558-560
48. Osten P., Khatri L., Perez J.L., Kohr G., Giese G., Daly C., Schulz T.W., Wensky A., Lee L.M., and Ziff E.B. Mutagenesis reveals a role for ABP/GRIP binding to GluR2 in synaptic surface accumulation of the AMPA receptor. Neuron 27 (2000) 313-325
49. Osten P., Srivastava S., Inman G.J., Vilim F.S., Khatri L., Lee L.M., States B.A., Einheber S., Milner T.A., Hanson P.I., and Ziff E.B. The AMPA receptor GluR2 C terminus can mediate a reversible, ATP-dependent interaction with NSF and alpha- and beta-SNAPs. Neuron 21 (1998) 99-110
50. Otis T., Zhang S., and Trussell L.O. Direct measurement of AMPA receptor desensitization induced by glutamatergic synaptic transmission. J. Neurosci. 16 (1996) 7496-7504
51. Passafaro M., Piech V., and Sheng M. Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat. Neurosci. 4 (2001) 917-926
52. Pitt D., Werner P., and Raine C.S. Glutamate excitotoxicity in a model of multiple sclerosis. Nat. Med. 6 (2000) 67-70
53. Plant K., Pelkey K.A., Bortolotto Z.A., Morita D., Terashima A., McBain C.J., Collingridge G.L., and Isaac J.T. Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat. Neurosci. 9 (2006) 602-604
54. Priel A., Kolleker A., Ayalon G., Gillor M., Osten P., and Stern-Bach Y. Stargazin reduces desensitization and slows deactivation of the AMPA-type glutamate receptors. J. Neurosci. 25 (2005) 2682-2686
55. Rosen D., Siddique R., Patterson T., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J.P., Deng H.X., et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362 (1993) 59-62
56. Rowland L.P., and Shneider N.A. Amyotrophic lateral sclerosis. N. Engl. J. Med. 344 (2001) 1688-1700
57. Roy J., Minotti S., Dong L., Figlewicz D.A., and Durham H.D. Glutamate potentiates the toxicity of mutant Cu/Zn-superoxide dismutase in motor neurons by postsynaptic calcium-dependent mechanisms. J. Neurosci. 18 (1998) 9673-9684
58. Sans N., Racca C., Petralia R.S., Wang Y.X., McCallum J., and Wenthold R.J. Synapse-associated protein 97 selectively associates with a subset of AMPA receptors early in their biosynthetic pathway. J. Neurosci. 21 (2001) 7506-7516
59. Schinder A.F., Olson E.C., Spitzer N.C., and Montal M. Mitochondrial dysfunction is a primary event in glutamate neurotoxicity. J. Neurosci. 16 (1996) 6125-6133
60. Seeburg P.H., Higuchi M., and Sprengel R. RNA editing of brain glutamate receptor channels: mechanism and physiology. Brain Res. Brain Res. Rev. 26 (1998) 217-229
61. Sheng M., and Kim M.J. Postsynaptic signaling and plasticity mechanisms. Science 298 (2002) 776-780
62. 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 (2001) 331-343
63. Siklos L., Engelhardt J.I., Alexianu M.E., Gurney M.E., Siddique T., and Appel S.H. Intracellular calcium parallels motoneuron degeneration in SOD-1 mutant mice. J. Neuropathol. Exp. Neurol. 57 (1998) 571-587
64. Smith T., Groom A., Zhu B., and Turski L. Autoimmune encephalomyelitis ameliorated by AMPA antagonists. Nat. Med. 6 (2000) 62-66
65. Song I., and Huganir R.L. Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci. 25 (2002) 578-588
66. Song I., Kamboj S., Xia J., Dong H., Liao D., and Huganir R.L. Interaction of the N-ethylmaleimide-sensitive factor with AMPA receptors. Neuron 21 (1998) 393-400
67. Spruston N., Jonas P., and Sakmann B. Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons. J. Physiol. 482 Pt 2 (1995) 325-352
68. Srivastava S., Osten P., Vilim F.S., Khatri L., Inman G., States B., Daly C., DeSouza S., Abagyan R., Valtschanoff J.G., Weinberg R.J., and Ziff E.B. Novel anchorage of GluR2/3 to the postsynaptic density by the AMPA receptor-binding protein ABP. Neuron 21 (1998) 581-591
69. Stern-Bach Y., Russo S., Neuman M., and Rosenmund C. A point mutation in the glutamate binding site blocks desensitization of AMPA receptors. Neuron 21 (1998) 907-918
70. Sun Y., Olson R., Horning M., Armstrong N., Mayer M., and Gouaux E. Mechanism of glutamate receptor desensitization. Nature 417 (2002) 245-253
71. 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 (1999) 806-815
72. Tanaka H., Grooms S.Y., Bennett M.V., and Zukin R.S. The AMPAR subunit GluR2: still front and center-stage. Brain Res. 886 (2000) 190-207
73. Tateno M., Sadakata H., Tanaka M., Itohara S., Shin R.M., Miura M., Masuda M., Aosaki T., Urushitani M., Misawa H., and Takahashi R. 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 (2004) 2183-2196
74. Tomita S., Sekiguchi M., Wada K., Nicoll R.A., and Bredt D.S. Stargazin controls the pharmacology of AMPA receptor potentiators. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 10064-10067
75. Tomiyama M., Rodriguez-Puertas R., Cortes R., Pazos A., Palacios J.M., and Mengod G. Flip and flop splice variants of AMPA receptor subunits in the spinal cord of amyotrophic lateral sclerosis. Synapse 45 (2002) 245-249
76. Van Damme P., Braeken D., Callewaert G., Robberecht W., and Van Den Bosch L. GluR2 deficiency accelerates motor neuron degeneration in a mouse model of amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 64 (2005) 605-612
77. 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 (2000) 29-34
78. 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 (1996) 1982-1989
79. Xia J., Zhang X., Staudinger J., and Huganir R.L. Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1. Neuron 22 (1999) 179-187