Ca 2+ permeable AMPA receptors switch allegiances: Mechanisms and consequences

Journal of Physiology

Volumn 590, Issue 1, 2012, Pages 13-20

  Liu, Siqiong June ^a   Savtchouk, Iaroslav ^a  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CALCIUM ION; MESSENGER RNA;

ACTION POTENTIAL; BRAIN REGION; GENE; GENE EXPRESSION; GENE FUNCTION; GENETIC TRANSCRIPTION; GLUA2 GENE; HIPPOCAMPUS; MEMBRANE PERMEABILITY; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; PYRAMIDAL NERVE CELL; REVIEW; SYNAPTIC TRANSMISSION; TRANSLATION REGULATION; VENTRAL TEGMENTUM;

ACTION POTENTIALS; ANIMALS; CALCIUM; GABAERGIC NEURONS; PYRAMIDAL CELLS; RECEPTORS, AMPA; RECEPTORS, GLUTAMATE; SYNAPSES; SYNAPTIC POTENTIALS; TRANSCRIPTION, GENETIC; VENTRAL TEGMENTAL AREA;

EID: 84855185430     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2011.213926     Document Type: Review

References (68)

1. Adesnik H & Nicoll RA (2007). Conservation of glutamate receptor 2-containing AMPA receptors during long-term potentiation. J Neurosci 27, 4598-4602.
2. Aizenman CD, Munoz-Elias G & Cline HT (2002). Visually driven modulation of glutamatergic synaptic transmission is mediated by the regulation of intracellular polyamines. Neuron 34, 623-634.
3. Bellone C & Luscher C (2006). Cocaine triggered AMPA receptor redistribution is reversed in vivo by mGluR-dependent long-term depression. Nat Neurosci 9, 636-641.
4. Bredt DS & Nicoll RA (2003). AMPA receptor trafficking at excitatory synapses. Neuron 40, 361-379.
5. Calderone A, Jover T, Noh KM, Tanaka H, Yokota H, Lin Y, Grooms SY, Regis R, Bennett MV & Zukin RS (2003). Ischemic insults derepress the gene silencer REST in neurons destined to die. J Neurosci 23, 2112-2121.
6. Cho CH, St-Gelais F, Zhang W, Tomita S & Howe JR (2007). Two families of TARP isoforms that have distinct effects on the kinetic properties of AMPA receptors and synaptic currents. Neuron 55, 890-904.
7. Clem RL & Barth A (2006). Pathway-specific trafficking of native AMPARs by in vivo experience. Neuron 49, 663-670.
8. Clem RL & Huganir RL (2010). Calcium-permeable AMPA receptor dynamics mediate fear memory erasure. Science 330, 1108-1112.
9. 2+-permeable AMPA receptors: synaptic plasticity and beyond. Curr Opin Neurobiol 16, 288-297.
10. Dingledine R, Borges K, Bowie D & Traynelis SF (1999). The glutamate receptor ion channels. Pharmacol Rev 51, 7-61.
11. Gardner SM, Takamiya K, Xia J, Suh JG, Johnson R, Yu S & Huganir RL (2005). Calcium-permeable AMPA receptor plasticity is mediated by subunit-specific interactions with PICK1 and NSF. Neuron 45, 903-915.
12. Geiger JR, Lubke J, Roth A, Frotscher M & Jonas P (1997). Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18, 1009-1023.
13. 2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15, 193-204.
14. Goel A, Jiang B, Xu LW, Song L, Kirkwood A & Lee HK (2006). Cross-modal regulation of synaptic AMPA receptors in primary sensory cortices by visual experience. Nat Neurosci 9, 1001-1003.
15. 2+-permeable AMPA receptors. Nature 381, 793-796.
16. Guire ES, Oh MC, Soderling TR & Derkach VA (2008). Recruitment of calcium-permeable AMPA receptors during synaptic potentiation is regulated by CaM-kinase I. J Neurosci 28, 6000-6009.
17. 2+-permeable AMPA receptors at perisynaptic sites by GluR1-S845 phosphorylation. Proc Natl Acad Sci U S A 106, 20033-20038.
18. Higuchi M, Single FN, Kohler M, Sommer B, Sprengel R & Seeburg PH (1993). RNA editing of AMPA receptor subunit GluR-B: a base-paired intron-exon structure determines position and efficiency. Cell 75, 1361-1370.
19. Ho MT, Pelkey KA, Pelletier JG, Huganir RL, Lacaille JC & McBain CJ (2009). Burst firing induces postsynaptic LTD at developing mossy fibre-CA3 pyramid synapses. J Physiol 587, 4441-4454.
20. 2+-permeable AMPA receptors underlies depolarization-induced long-term depression at mossy fiber CA3 pyramid synapses. J Neurosci 27, 11651-11662.
21. Huang Y, Myers SJ & Dingledine R (1999). Transcriptional repression by REST: recruitment of Sin3A and histone deacetylase to neuronal genes. Nat Neurosci 2, 867-872.
22. Isaac JT, Ashby M & McBain CJ (2007). The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 54, 859-871.
23. Jia Z, Agopyan N, Miu P, Xiong Z, Henderson J, Gerlai R, Taverna FA, Velumian A, MacDonald J, Carlen P, Abramow-Newerly W & Roder J (1996). Enhanced LTP in mice deficient in the AMPA receptor GluR2. Neuron 17, 945-956.
24. Joshi I, Shokralla S, Titis P & Wang LY (2004). The role of AMPA receptor gating in the development of high-fidelity neurotransmission at the calyx of Held synapse. J Neurosci 24, 183-196.
25. Kato AS, Zhou W, Milstein AD, Knierman MD, Siuda ER, Dotzlaf JE, Yu H, Hale JE, Nisenbaum ES, Nicoll RA & Bredt DS (2007). New transmembrane AMPA receptor regulatory protein isoform, γ-7, differentially regulates AMPA receptors. J Neurosci 27, 4969-4977.
26. Kawahara Y, Ito K, Sun H, Aizawa H, Kanazawa I & Kwak S (2004). Glutamate receptors: RNA editing and death of motor neurons. Nature 427, 801.
27. Kelly L, Farrant M & Cull-Candy SG (2009). Synaptic mGluR activation drives plasticity of calcium-permeable AMPA receptors. Nat Neurosci 12, 593-601.
28. Koike M, Tsukada S, Tsuzuki K, Kijima H & Ozawa S (2000). Regulation of kinetic properties of GluR2 AMPA receptor channels by alternative splicing. J Neurosci 20, 2166-2174.
29. Kumar SS, Bacci A, Kharazia V & Huguenard JR (2002). A developmental switch of AMPA receptor subunits in neocortical pyramidal neurons. J Neurosci 22, 3005-3015.
30. Laezza F, Doherty JJ & Dingledine R (1999). Long-term depression in hippocampal interneurons: joint requirement for pre- and postsynaptic events. Science 285, 1411-1414.
31. Lamsa KP, Heeroma JH, Somogyi P, Rusakov DA & Kullmann DM (2007). Anti-Hebbian long-term potentiation in the hippocampal feedback inhibitory circuit. Science 315, 1262-1266.
32. Lawrence JJ & Trussell LO (2000). Long-term specification of AMPA receptor properties after synapse formation. J Neurosci 20, 4864-4870.
33. Lei S & McBain CJ (2004). Two Loci of expression for long-term depression at hippocampal mossy fiber-interneuron synapses. J Neurosci 24, 2112-2121.
34. Liu B, Liao M, Mielke JG, Ning K, Chen Y, Li L, El-Hayek YH, Gomez E, Zukin RS, Fehlings MG & Wan Q (2006). Ischemic insults direct glutamate receptor subunit 2-lacking AMPA receptors to synaptic sites. J Neurosci 26, 5309-5319.
35. 2+-permeable AMPA receptor channels primes cell death in transient forebrain ischemia. Neuron 43, 43-55.
36. 2+ permeability of AMPARs at cerebellar synapses. Nat Neurosci 8, 768-775.
37. 2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci 30, 126-134.
38. Liu SQ & Cull-Candy SG (2000). Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature 405, 454-458.
39. + channel activity alters synaptic AMPA receptor phenotype in mouse cerebellar stellate cells. J Neurophysiol 106, 144-152.
40. Liu Y, Formisano L, Savtchouk I, Takayasu Y, Szabo G, Zukin RS & Liu SJ (2010). A single fear-inducing stimulus induces a transcription-dependent switch in synaptic AMPAR phenotype. Nat Neurosci 13, 223-231.
41. Mahanty NK & Sah P (1998). Calcium-permeable AMPA receptors mediate long-term potentiation in interneurons in the amygdala. Nature 394, 683-687.
42. Malinow R & Malenka RC (2002). AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25, 103-126.
43. Mameli M, Balland B, Lujan R & Luscher C (2007). Rapid synthesis and synaptic insertion of GluR2 for mGluR-LTD in the ventral tegmental area. Science 317, 530-533.
44. Mameli M, Bellone C, Brown MT & Luscher C (2011). Cocaine inverts rules for synaptic plasticity of glutamate transmission in the ventral tegmental area. Nat Neurosci 14, 414-416.
45. Milstein AD & Nicoll RA (2008). Regulation of AMPA receptor gating and pharmacology by TARP auxiliary subunits. Trends Pharmacol Sci 29, 333-339.
46. Milstein AD, Zhou W, Karimzadegan S, Bredt DS & Nicoll RA (2007). TARP subtypes differentially and dose-dependently control synaptic AMPA receptor gating. Neuron 55, 905-918.
47. Noh KM, Yokota H, Mashiko T, Castillo PE, Zukin RS & Bennett MV (2005). Blockade of calcium-permeable AMPA receptors protects hippocampal neurons against global ischemia-induced death. Proc Natl Acad Sci U S A 102, 12230-12235.
48. 2+-permeable AMPA receptors in the developing rat retina. J Physiol 582, 95-111.
49. Partin KM, Fleck MW & Mayer ML (1996). AMPA receptor flip/flop mutants affecting deactivation, desensitization, and modulation by cyclothiazide, aniracetam, and thiocyanate. J Neurosci 16, 6634-6647.
50. Peng PL, Zhong X, Tu W, Soundarapandian MM, Molner P, Zhu D, Lau L, Liu S, Liu F & Lu Y (2006). ADAR2-dependent RNA editing of AMPA receptor subunit GluR2 determines vulnerability of neurons in forebrain ischemia. Neuron 49, 719-733.
51. Plant K, Pelkey KA, Bortolotto ZA, Morita D, Terashima A, McBain CJ, Collingridge GL & Isaac JT (2006). Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat Neurosci 9, 602-604.
52. Quirk JC, Siuda ER & Nisenbaum ES (2004). Molecular determinants responsible for differences in desensitization kinetics of AMPA receptor splice variants. J Neurosci 24, 11416-11420.
53. 2+-permeable AMPA receptors and spontaneous presynaptic transmitter release at developing excitatory spinal synapses. J Neurosci 19, 8528-8541.
54. Rozov A & Burnashev N (1999). Polyamine-dependent facilitation of postsynaptic AMPA receptors counteracts paired-pulse depression. Nature 401, 594-598.
55. Savtchouk I & Liu SJ (2011). Remodeling of synaptic AMPA receptor subtype alters the probability and pattern of action potential firing. J Neurosci 31, 501-511.
56. Schwenk J, Harmel N, Zolles G, Bildl W, Kulik A, Heimrich B, Chisaka O, Jonas P, Schulte U, Fakler B & Klocker N (2009). Functional proteomics identify cornichon proteins as auxiliary subunits of AMPA receptors. Science 323, 1313-1319.
57. Seifert G, Weber M, Schramm J & Steinhauser C (2003). Changes in splice variant expression and subunit assembly of AMPA receptors during maturation of hippocampal astrocytes. Mol Cell Neurosci 22, 248-258.
58. Soler-Llavina GJ & Sabatini BL (2006). Synapse-specific plasticity and compartmentalized signaling in cerebellar stellate cells. Nat Neurosci 9, 798-806.
59. Sommer B, Kohler M, Sprengel R & Seeburg PH (1991). RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67, 11-19.
60. Sommer B, Keinanen K, Verdoorn TA, Wisden W, Burnashev N, Herb A, Kohler M, Takagi T, Sakmann B & Seeburg PH (1990). Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science 249, 1580-1585.
61. Song I & Huganir RL (2002). Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci 25, 578-588.
62. Sutton MA, Ito HT, Cressy P, Kempf C, Woo JC & Schuman EM (2006). Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 125, 785-799.
63. Suzuki E, Kessler M & Arai AC (2008). The fast kinetics of AMPA GluR3 receptors is selectively modulated by the TARPs γ4 and γ8. Mol Cell Neurosci 38, 117-123.
64. Swanson GT, Kamboj SK & Cull-Candy SG (1997). Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J Neurosci 17, 58-69.
65. Tomita S, Adesnik H, Sekiguchi M, Zhang W, Wada K, Howe JR, Nicoll RA & Bredt DS (2005). Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature 435, 1052-1058.
66. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ & Dingledine R (2010). Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62, 405-496.
67. Vialou V, Robison AJ, Laplant QC, Covington HE 3rd, Dietz DM, Ohnishi YN, Mouzon E, Rush AJ 3rd, Watts EL, Wallace DL, Iniguez SD, Ohnishi YH, Steiner MA, Warren BL, Krishnan V, Bolanos CA, Neve RL, Ghose S, Berton O, Tamminga CA & Nestler EJ (2010). DeltaFosB in brain reward circuits mediates resilience to stress and antidepressant responses. Nat Neurosci 13, 745-752.
68. Washburn MS, Numberger M, Zhang S & Dingledine R (1997). Differential dependence on GluR2 expression of three characteristic features of AMPA receptors. J Neurosci 17, 9393-9406.