The essential role of AMPA receptor GluA2 subunit RNA editing in the normal and diseased brain

Frontiers in Molecular Neuroscience

Volumn , Issue APRIL, 2012, Pages

  Wright, Amanda ^a,b   Vissel, Bryce ^a,b  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Adenosine deaminases acting on RNA; AMPA receptor; Excitotoxicity; GluA2; GluR B,RNA editing; GluR2

Indexed keywords

AMPA RECEPTOR; CALCIUM ION; GLUTAMATE RECEPTOR 2;

AMYOTROPHIC LATERAL SCLEROSIS; BRAIN DISEASE; BRAIN FUNCTION; BRAIN REGION; CALCIUM TRANSPORT; CELL DEATH; CELL LOSS; CELL MIGRATION; CELL SURVIVAL; CODON; DOWN REGULATION; EXCITOTOXICITY; GENE; GLUA2 GENE; INTRON; ISCHEMIA; NERVE CELL; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; RNA EDITING; SITE DIRECTED MUTAGENESIS; SYNAPSE;

EID: 84863992209     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2012.00034     Document Type: Review

References (99)

1. Aizawa, H., Sawada, J., Hideyama, T., Yamashita, T., Katayama, T., Hasebe, N., Kimura, T., Yahara, O., and Kwak, S. (2010). TDP-43 pathology in sporadicALS occurs in motor neurons lacking the RNA editing enzyme ADAR2. Acta Neuropathol. 120, 75-84.
2. Akbarian, S., Smith, M. A., and Jones, E. G. (1995). Editing for an AMPA receptor subunit RNA in prefrontal cortex and striatum in Alzheimer's disease, Huntington's disease and schizophrenia. Brain Res. 699, 297-304.
3. Araki, Y., Lin, D., and Huganir, R. L. (2010). Plasma membrane insertion of the AMPA receptor GluA2 subunit is regulated by NSF binding and Q/R editing of the ion pore. Proc. Natl. Acad. Sci. U.S.A. 107, 11080-11085.
4. 2+ permeable AMPA receptor induced longterm potentiation requires Pi3/MAP kinases but not Ca/CaM-dependent kinase II. PLoS ONE 4, e4339. doi: 10.1371/journal.pone.0004339
5. Bartus, R. T., Hayward, N. J., Elliott, P. J., Sawyer, S. D., Baker, K. L., Dean, R. L., Akiyama, A., Straub, J. A., Harbe-son, S. L., and Li, Z. (1994). Calpain inhibitor AK295 protects neurons from focal brain ischemia. Effects of postocclusion intra-arterial administration. Stoke 25, 2265-2270.
6. Bass, B. L. (2002). RNA editing by adenosine deaminases that act on RNA. Annu. Rev. Biochem. 71, 817-846.
7. Bassani, S., Valnegri, P., Beretta, F., and Passafaro, M. (2009). The GluR2 subunit of AMPA receptors: synaptic role. Neuroscience 158, 55-61.
8. Bellone, C., and Luscher, C. (2006). Cocaine triggered AMPA receptor redistribution is reversed in vivo by mGluR-dependent long-term depression. Nat. Neurosci. 9, 636-641.
9. Biou, V., Bhattacharyya, S., and Malenka, R. C. (2008). Endocyto-sis and recycling of AMPA receptors lacking GluR2/3. Proc. Natl. Acad. Sci. U.S.A. 150, 1038-1043.
10. Brusa, R., Zimmermann, F., Koh, D. S., Feldmeyer, D., Gass, P., Seeburg, P. H., and Sprengel, R. (1995). Early-onset epilepsy and postnatal lethality associated with an editing-deficient GluR-B allele in mice. Science 270, 1677-1680.
11. Buchan, A. M., Li, H., Cho, S., and Pulsinelli, W. A. (1991). Blockade of the AMPA receptor prevents CA1 hippocampal injury following severe but transient forebrain ischemia in adult rats. Neurosci. Lett. 132, 255-258.
12. Burnashev, N., Villarroel, A., and Sakmann, B. (1996). Dimensions and ion selectivity of recombinant AMPA and kainate receptor channels and their dependence on Q/R site residues. J. Physiol. 496, 165-173.
13. Burns, C., Chu, H., Rueter, S., Hutchinson, L., Canton, H., Sanders-Bush, E., and Emerson, R. (1997). Regulation of serotonin-2C receptor G-protein coupling byRNAediting. Nature 387, 303-308.
14. Calderone, A., Jover, T., Noh, K., Tanaka, H., Yokota, H., Lin, Y., Grooms, S., Regis, R., Bennet, M., and Zukin, S. (2003). Ischemic insults derepress the gene silencer REST in neurons destined to die. J. Neurosci. 23, 2112-2121.
15. Chen, C., Cho, D., Wang, Q., Lai, F., Carter, K., and Nishikura, K. (2000). A third member of the RNA-specific adenosine deaminase gene family, ADAR3, contains both single-and double-stranded RNA binding domains. RNA 6, 755-767.
16. Clem, R. L., and Barth, A. (2006). Pathway-specific trafficking of native AMPARs by in vivo experience. Neuron 49, 663-670.
17. Conrad, K. L., Tseng, K. Y., Uejima, J. L., Reimers, J. M., Jun-Heng, L. J., Shaham, Y., Marinelli, M., and Wolf, M. E. (2008). Formation of accumbens GluR2-lacking AMPA receptors mediates incubation of cocaine craving. Nature 454, 118-121.
18. 2+-permeable AMPA receptors: synaptic plasticity and beyond. Curr. Opin. Neurobiol. 16, 288-297.
19. Dabiri, G. A., Lai, F., Drakes, R. A., and Nishikura, K. (1996). Editing of the GluR-B ion channel RNA in vitro by recombinant double-stranded RNA adenosine deaminase. EMBO J. 15, 34-45.
20. Dingledine, R., Borges, K., Bowie, D., andTraynelis, S. F. (1999). The glutamate receptor ion channels. Pharmacol. Rev. 51, 7-61.
21. Doble, A. (1999). The role of excito-toxicityin neurodegenerative disease: implications for therapy. Pharmacol. Ther. 81, 163-221.
22. Feldmeyer, D., Kask, K., Brusa, R., Kor-nau, H. C., Kolhekar, R., Rozov, A., Burnashev, N., Jensen, V., Hvalby, O., Sprengel, R., and Seeburg, P. H. (1999). Neurological dysfunctions in mice expressing different levels of the Q/R site-unedited AMPAR subunit GluR-B. Nat. Neuroci. 2, 57-64.
23. 2+ influx in hippocampal CA1 neurons of gerbil. J. Neurosci. 17, 6179-6188.
24. Greger, I. H., Akamine, P., Khatri, L., and Ziff, E. B. (2006). Developmentally regulated, combinatorial RNA processing modulates AMPA receptor biogenesis. Neuron 51, 85-97.
25. Greger, I. H., Khatri, L., Kong, X., and Ziff, E. B. (2003). AMPA receptor tetramerization is mediated by Q/R editing. Neuron 40, 763-774.
26. Greger, I. H., Khatri, L., and Ziff, E. B. (2002). RNA editing at arg607 controls AMPA receptor exit from the endoplasmic reticulum. Neuron 34, 759-772.
27. Greger, I. H., Ziff, E. B., and Penn, A. C. (2007). Molecular determinants of AMPA receptor subunit assembly. Trends Neurosci. 30, 407-416.
28. Hardingham, G. E., and Badling, H. (2003). The Yin and Yang of NMDA receptor signalling. Trends Neurosci. 26, 81-89.
29. Harvery, S. C., Koster, A., Yu, H., Skolnick, P., Baumbarger, P., and Nisenbaum, E. S. (2001). AMPA receptor function is altered in GluR2-deficient Mice. J. Mol. Neurosci. 17, 35-43.
30. Hideyama, T., Yamashita, T., Suzuki, T., Tsuji, S., Higuchi, M., Seeburg, P. H., Takashashi, R., Misawa, H., and Kwak, S. (2010). Induced loss of ADAR2 engenders slow death of motor neurons from Q/R site-unedited GluR2. J. Neurosci. 30, 11917-11925.
31. Higuchi, M., Maas, S., Single, F. N., Hartner, J., Rozov, A., Burnashev, N., Feldmeyer, D., Sprengel, R., and See-burg, P. H. (2000). Point mutation in the AMPA receptor gene rescues lethality in mice deficient in the RNA-editing enzyme ADAR2. Nature 406, 78-81.
32. Higuchi, M., Single, F. N., Kohler, M., Sommer, B., Sprengel, R., and Seeburg, P. H. (1993). RNA editing of AMPA receptor subunit GluR-B: a base paired intron-exon structure determines position and efficiency. Cell75, 1361-1370.
33. 2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 252, 851-853.
34. Hollmann, M., and Heinemann, S. (1994). Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31-108.
35. Horsch, M., Seeburg, P. H., Adler, T., Aguilar-Pimentel, J. A., Becker, L., Calzada-Wack, J., Garret, L., Gotz, A., Hans, W., Higuchi, M., Holter, S. M., Naton, B., Prehn, C., Puk, O., Racz, I., Rathkolb, B., Rozman, J., Schrewe, A., Adamski, J., Busch, D. H., Esposito, I., Graw, J., Ivandic, B., Klingen-spor, M., Klopstock, T., Mempel, M., Ollert, M., Schulz, H., Wolf, E., Wurst, W., Zimmer, A., Gailus-Durner, V., Fuchs, H., De Angelis, M., and Beckers, J. (2011). Requirement of the RNA-editing enzyme ADAR2 fornormalphysiologyinmice. J. Biol. Chem. 286, 18614-18622.
36. Hume, R. I., Dingledine, R., and Heine-mann, S. F. (1991). Identification of a site in glutamate receptor subunits that controls calcium permeability. Science253, 1028-1031.
37. Isaac, J. T., Ashby, M. C., and Mcbain, C. J. (2007). The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 54, 859-871.
38. Jackson, A. C., and Nicoll, R. A. (2011). The expanding social network of ionotropic glutamate receptors: TARPs and other transmembrane auxiliary subunits. Neuron 70, 178-199.
39. Jacobs, M. M., Fogg, R. L., Emeson, R. B., and Stanwood, G. D. (2009). ADAR1 and ADAR2 expression and editing activity during forebrain development. Dev. Neurosci. 31, 223-237.
40. Jansson, L. C., Wigren, H. K., Nordstrom, T., and Akerman, K. E. (2011). Functional a-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptors in differentiating embryonic neural progenitor cells. Neuroreport 22, 282-287.
41. 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. (1996). Enhanced LTP in mice deficient in the AMPA receptor GluR2. Neuron 17, 945-956.
42. Kask, K., Zamanillo, D., Rozov, A., Burnashev, N., Sprengel, R., and Seeburg, P. H. (1998). 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, 13777-13782.
43. Kawahara, Y., Ito, K., Sun, H., Aizawa, H., Kanazawa, I., and Kwak, S. (2004a). Glutamate receptors: RNA editing and death of motor neurons. Nature 427, 801.
44. Kawahara, Y., Ito, K., Sun, H., Ito, M., Kanazawa, I., and Kwak, S. (2004b). Regulation of glutamate receptor RNA editing and ADAR mRNA expression in developing human normal and Down's syndrome brains. Brain Res. Dev. Brain Res. 148, 151-155.
45. Kawahara, Y., Ito, K., Sun, H., Kanazawa, I., and Kwak, S. (2003). 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, 23-33.
46. Kawahara, Y., andKwak, S. (2005). Exci-totoxicity and ALS: what is unique about the AMPA receptors expressed on spinal motor neurons? Amyotroph. Lateral Scler. Other Motor Neuron Disord. 6, 131-144.
47. Kawahara, Y., Sun, H., Ito, K., Hideyama, T., Aoki, M., Sobue, G., Tsuji, S., and Kwak, S. (2006). 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, 11-14.
48. Keifer, J., and Zheng, Z. (2010). AMPA receptor trafficking and learning. Eur. J. Neurosci. 32, 269-277.
49. Kessels, H., and Malinow, R. (2009). Synaptic AMPA receptor plasticity and behaviour. Neuron 61, 340-350.
50. Kortenbruck, G., Berger, E., Speck-mann, E. J., and Musshoff, U. (2001). 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, 459-468.
51. Kullmann, D. M., and Lamsa, K. (2008). Roles of distinct glutamate receptors in induction of anti-Hebbian longterm potentiation. J. Physiol. 586, 1481-1486.
52. Kuner, R., Groom, A. J., Bresink, I., Kornau, H., Stefovska, V., Muller, G., Hartmann, B., Tschauner, K., Waibel, S., Ludolph, A. C., Ikonomi-dou, C., Seeburg, P. H., and Turski, L. (2005). Late-onset motoneuron disease caused by a functionally modified AMPA receptor subunit. Proc. Natl. Acad. Sci. U.S.A. 102, 5826-5831.
53. Kuner, T., Beck, C., Sakmann, B., and Seeburg, P. (2001). 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, 4162-4172.
54. Kung, S. S., Chen, Y. C., Lin, W. H., Chen, C. C., and Chow, W. Y. (2001). Q/R RNA editing of the AMPA receptor subunit 2 (GRIA2) transcript evolves no later than the appearance of cartilaginous fishes. FEBSLett 509, 277-281.
55. Kwak, S., Hideyama, T., Yamashita, T., and Aizawa, H. (2010). AMPA receptor-mediated neuronal death in sporadic ALS. Neuropathology 30, 182-188.
56. Kwak, S., and Kawahara, Y. (2005). Deficient RNA editing of GluR2 and neuronal death in amyotropic lateral sclerosis. J. Mol. Med. 83, 110-120.
57. Kwak, S., and Weiss, J. H. (2006). Calcium-permeable AMPA channels in neurodegenerative disease and ischemia. Curr. Opin. Neurobiol. 16, 281-287.
58. Lamsa, K. P., Heeroma, J. H., Som-ogyi, P., Rusakov, D. A., and Kull-mann, D. M. (2007). Anti-Hebbian long-term potentiation in the hippocampal feedback inhibitorycircuit. Science 315, 1262-1266.
59. Lerma, J. (2003). Roles and rules of kainate receptors in synaptic transmission. Nat. Rev. Neurosci. 4, 481-495.
60. Liu, B., Liau, M., Mielke, J. G., Ning, K., Chen, Y., Li, L., El-Hayek, Y. H., Gomez, E., Zukin, R. S., Fehlings, M. G., and Wan, Q. (2006). Ischemic insults directs glutamate receptor subunit 2-lacking AMPA receptors to synaptic sites. J. Neurosci. 26, 5309-5319.
61. 2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci. 30, 126-134.
62. Lomeli, H., Mosbacher, J., Melcher, T., Hoger, T., Geiger, J., Kuner, T., Monyer, H., Higuchi, M., Bach, A., and Seeburg, P. (1994). Control of kinetic properties of AMPA receptor channels by nuclear RNA editing. Science 266, 1709-1713.
63. Lu, Y., Allen, M., Halt, A. R., Weisen-haus, M., Dallapiazza, R. F., Hall, D. D., Usachev, Y. M., Mcknight, G. S., and Hell, J. W. (2007). Age-dependent requirement of AKAP150-anchored PKA and GluR2-lacking AMPA receptors in LTP. EMBO J. 26, 4879-4890.
64. Maas, S., Patt, S., Schrey, M., and Rich, A. (2001). Underediting of glutamate receptor GluR-B mRNA in malignant gliomas. Proc. Natl. Acad. Sci. U.S.A. 98, 14687-14692.
65. Mahajan, S. S., Thai, K. H., Chen, K., and Ziff, E. B. (2011). Exposure of neurons to excitotoxic levels of glutamate induces cleavage of the RNA editing enzyme, adenosine deaminase acting on RNA 2, and loss of GLUR2 editing. Neuroscience 189, 305-315.
66. 2 +-permeability. Mol. Cell. Neurosci. 35, 470-481.
67. Malinow, R., and Malenka, R. C. (2002). AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25, 103-126.
68. Man, H. Y. (2011). GluA2-lacking, calcium-permeable AMPA receptors-inducers of plasticity? Curr. Opin. Neurobiol. 21, 291-298.
69. Marcucci, R., Brindle, J., Paro, S., Casa-dio, A., Hempel, S., Morrice, N., Bisso, A., Keegen, L. P., Del Sal, G., and O'Connell, M. A. (2011). Pin1 and WWP2 regulate GluR2 Q/R site RNA editing by ADAR2 with opposing effects. EMBO J. 30, 4211-4222.
70. Mattick, J., and Mehler, M. (2008). RNA editing, DNA recoding and the evolution of human cognition. Trends Neurosci. 31, 227-233.
71. Melcher, T., Maas, S., Herb, A., Sprengel, R., Seeburg, P. H., and Higuchi, M. (1996). A mammalian RNA editing enzyme. Nature 379, 460-464.
72. Meng, Y., Zhang, Y., and Jia, Z. (2003). Synaptic transmission and plasticity in the absence of AMPA glutamate receptor GluR2 and GluR3. Neuron 39, 163-176.
73. Mosbacher, J., Schoepfer, R., Monyer, H., Burnashev, N., Seeburg, P. H., and Ruppersber, J. P. (1994). A molecular determinant for submillisecond desensitization in glutamate receptors. Science 266, 1059-1062.
74. Nakagawa, T. (2010). The biochemistry, ultrastructure, and subunit assembly mechanism of AMPA receptors. Mol. Neurobiol. 42, 161-184.
75. Noh, K. M., Yokota, H., Mashiko, T., Castillo, P. E., Zukin, R. S., Bennet, M. V. (2005). Blockade of calcium-permeable AMPA receptors protects hippocampal neurons against global ischemia-induced death. Proc. Natl. Acad. Sci. U.S.A. 102, 1223012235.
76. Nutt, S. L., and Kamboj, R. K. (1994). Differential RNA editing efficiency of AMPA receptor GluR-2 in human brain. Neuroreport 5, 1679-1683.
77. Panicker, S., Brown, K., and Nicoll, R. A. (2008). Synaptic AMPA receptor subunit trafficking is independent of the C terminus in the GluR2-lacking mouse. Proc. Natl. Acad. Sci. U.S.A. 105, 1032-1037.
78. Parsons, C. G., Stoffler, A., and Danysz, W. (2007). Memantine: a NMDA receptor antagonist that improves memory by restoration of homeostasis in the glutamatergic system-too little activation is bad, too much is even worse. Neuropharmacology 53, 699-723.
79. Paupard, M.-C., O'Connell, M. A., Greber, A. P., and Zukin, R. S. (1999). Patterns of developmental expression of the RNA editing enzyme rADAR2. Neuroscience 95, 869-879.
80. 2+-permeable AMPA receptors in neurological disorders. Trends Neurosci. 20, 464-470.
81. Pellegrini-Giampietro, D. E., Zukin, R. S., Bennet, M. V., Cho, S., and Pulsinelli, W.A. (1992). Switchinglu-tamate receptor subunit gene expression in CA1 subfield of hippocampus following global ischemia in rats. Proc. Natl. Acad. Sci. U.S.A. 89, 10499-10503.
82. Peng, P. L., Zhong, X., Tu, W., Soundara-pandian, M. M., Molner, P., Zhu, D., Lau, L., Liu, S., Liu, F., and Lu, Y. (2006). ADAR2-dependent RNA editing of AMPA receptor subunit GluR2 determines vulnerability of neurons in forebrain ischemia. Neuron 49, 719-733.
83. Pollard, H., Heron, A., Moreau, J., Ben-Ari, Y., and Khrestchatisky, M. (1993). Alterations of the GluR-B AMPA receptor subunit flip/flop expression in kainate-induced epilepsy and ischemia. Neuroscience 57, 545-554.
84. Riedel, G., Micheau, J., Lam, A. G., Roloff, E. L., Martin, S. J., Bridge, H., De Hoz, L., Poeschel, B., Mcculloch, J., and Morris, R. G. (1999). Reversibleneuralinactivation reveals hippocampal participation in several memory processes. Nature 2, 898-905.
85. Rosenmund, C., Stern-Bach, Y., and Stevens, C. F. (1998). The tetrameric structure of a glutamate receptor channel. Science 280, 1596-1599.
86. Rump, A., Sommer, C., Gass, P., Bele, P., Meissner, D., and Kiessling, M. (1996). Editing of GluR2 RNA in the gerbil hippocampus after global cerebral ischemia. J. Cereb. Blood Flow Metab. 16, 1362-1365.
87. Sans, N., Vissel, B., Petralia, R. S., Wang, Y. X., Chang, K., Royle, G. A., Wang, C. Y., O'Gorman, S., Heinemann, S. F., and Wenthold, R. J. (2003). Aberrant formation of glutamate receptor complexes in hippocampal neurons of mice lacking the GluR2 AMPA receptor subunit. J. Neurosci. 23, 9367-9373.
88. Schiffer, H. H., and Heinemann, S. F. (1999). A quantitative method to detect RNA editing events. Anal. Biochem. 276, 257-260.
89. Sobolevsky, A., Rosconi, M., and Gouaux, E. (2009). X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 462, 745-756.
90. Sommer, B., Keinanen, K., Verdoorn, T. A., Wisden, W., Burnashev, N., Herb, A., Kohler, M., Takagi, T., Sak-mann, B., and Seeburg, P. H. (1990). Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science 249, 1580-1585.
91. Sommer, B., Köhler, M., Sprengel, R., and Seeburg, P. H. (1991). RNA editing in brain controls a determinant of ion flowin glutamate-gated channels. Cell67, 11-19.
92. Sun, H. Y., Bartley, A. F., and Dobrunz, L. E. (2009). Calcium-permeable presynaptic kainate receptors involved in excitatory shortterm facilitation onto somatostatin interneurons during natural stimulus patterns. J. Neurophysiol. 101, 1043-1055.
93. Takuma, H., Kwak, S., Yoshizawa, T., and Kanazawa, I. (1999). 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, 806-815.
94. Tanaka, H., Grooms, S. Y., Bennet, M. V., and Zukin, R. S. (2000). The AMPAR subunit GluR2: still front and center-stage. Brain Res. 886, 190-207.
95. Vissel, B., Royle, G. A., Christie, B. R., Schiffer, H. H., Ghetti, A., Tritto, T., Perez-Otano, I., Radcliffe, R. A., Seamans, J., Sejnowski, T., Wehner, J. M., Collins, A. C., O'Gorman, S., and Heinemann, S. F. (2001). The role of RNA editing of kainate receptors in synaptic plasticity and seizures. Neuron 29, 217-227.
96. Wenthold, R. J., Petralia, R. S., Bla-hos, J. I., and Niedzielski, A. S. (1996). Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J. Neurosci. 16, 1982-1989.
97. Whitney, N. P., Peng, H., Erdmann, N. B., Tian, C., Monaghan, D. T., and Zheng, J. C. (2008). Calcium-permeable AMPA receptors containing Q/R-unedited GluR2 direct human neural progenitor cell differentiation to neurons. FASEB J. 22, 2888-2900.
98. Wiltgen, B. J., Royle, G. A., Gray, E. E., Abdipranoto, A., Thangthaeng, N., Jacobs, N., Saab, F., Tonegawa, S., Heinemann, S. F., O'Dell, T. J., Fanselow, M. S., andVissel, B. (2010). A role for calcium-permeable AMPA receptors in synaptic plasticity and learning. PLoS ONE 5, e12818. doi: 10.1371/journal.pone.0012818
99. Ziff, E. B. (2007). TARPs and the AMPA receptor trafficking paradox. Neuron 53, 627-633.