A role of TARPs in the expression and plasticity of calcium-permeable AMPARs: Evidence from cerebellar neurons and glia

Neuropharmacology

Volumn 74, Issue , 2013, Pages 76-85

  Bats, Cécile ^a   Farrant, Mark ^a   Cull Candy, Stuart G ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

AMPA receptors; Calcium permeable AMPA receptors; Cerebellum; Glutamate receptors; Plasticity; Synaptic transmission; TARPs

Indexed keywords

AMPA RECEPTOR; GLUA2 PROTEIN; MEMBRANE PROTEIN; RECEPTOR SUBTYPE; RECEPTOR SUBUNIT; TARP PROTEIN; UNCLASSIFIED DRUG;

BASKET CELL; BRAIN ISCHEMIA; BRAIN NERVE CELL; CALCIUM TRANSPORT; CEREBELLUM; DRUG DEPENDENCE; GLIA CELL; HUMAN; INTERNEURON; MEMBRANE PERMEABILITY; NERVE CELL PLASTICITY; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVIEW; STELLATE CELL; STEM CELL; SYNAPTIC TRANSMISSION;

AMPA RECEPTORS; CALCIUM-PERMEABLE AMPA RECEPTORS; CEREBELLUM; GLUTAMATE RECEPTORS; PLASTICITY; SYNAPTIC TRANSMISSION; TARPS;

ANIMALS; CALCIUM CHANNELS; CEREBELLUM; NEUROGLIA; NEURONAL PLASTICITY; PROTEIN SUBUNITS; RECEPTORS, AMPA; SYNAPTIC TRANSMISSION;

EID: 84885173630     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.03.037     Document Type: Review

References (88)

1. Adesnik, H., Nicoll, R.A., 2007. Conservation of glutamate receptor 2-containing AMPA receptors during long-term potentiation. J. Neurosci. 27, 4598-4602.
2. 2+ permeable AMPA receptor induced long-term potentiation requires PI3/MAP kinases but not Ca/CaM-dependent kinase II. PLoS One 4, e4339.
3. Bats, C, Soto, D., Studniarczyk, D., Farrant, M., Cull-Candy, S.G., 2012. Channel properties reveal differential expression of TARPed and TARPless AMPARs in stargazer neurons. Nat. Neurosci. 15, 853-861.
4. Bedoukian, M.A., Weeks, A.M., Partin, K.M., 2006. Different domains of the AMPA receptor direct stargazin-mediated trafficking and stargazin-mediated modulation of kinetics. J. Biol. Chem. 281, 23908-23921.
5. 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.
6. Bergles, D.E., Dzubay, J.A., Jahr, C.E., 1997. Glutamate transporter currents in bergmann glial cells follow the time course of extrasynaptic glutamate. Proc. Natl. Acad. Sci. U. S. A. 94, 14821-14825.
7. Borgdorff, A.J., Choquet, D., 2002. Regulation of AMPA receptor lateral movements. Nature 417, 649-653.
8. Bowie, D., Mayer, M.L., 1995. Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron 15, 453-462.
9. Bureau, I., Mulle, C., 1998. Potentiation of GABAergic synaptic transmission by AMPA receptors in mouse cerebellar stellate cells: changes during development. J. Physiol. 509, 817-831.
10. Carter, A.G., Regehr, W.G., 2002. Quantal events shape cerebellar interneuron firing. Nat. Neurosci. 5, 1309-1318.
11. Chadderton, P., Margrie, T.W., Hausser, M., 2004. Integration of quanta in cerebellar granule cells during sensory processing. Nature 428, 856-860.
12. Chaudhry, F.A., Lehre, K.P., van Lookeren Campagne, M., Ottersen, O.P., Danbolt, N.C., Storm-Mathisen, J., 1995. Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15, 711-720.
13. Chen, L., Chetkovich, D.M., Petralia, R.S., Sweeney, N.T., Kawasaki, Y., Wenthold, R.J., Bredt, D.S., Nicoll, R.A., 2000. Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408, 936-943.
14. Cho, C.H., St-Gelais, F., Zhang, W., Tomita, S., Howe, J.R., 2007. Two families of TARP isoforms that have distinct effects on the kinetic properties of AMPA receptors and synaptic currents. Neuron 55, 890-904.
15. Clark, B.A., Cull-Candy, S.G., 2002. Activity-dependent recruitment of extrasynaptic NMDA receptor activation at an AMPA receptor-only synapse. J. Neurosci. 22, 4428-4436.
16. Clem, R.L., Barth, A., 2006. Pathway-specific trafficking of native AMPARs by in vivo experience. Neuron 49, 663-670.
17. Clem, R.L., Huganir, R.L., 2010. Calcium-permeable AMPA receptor dynamics mediate fear memory erasure. Science 330, 1108-1112.
18. 2+-permeable AMPA receptors: synaptic plasticity and beyond. Curr. Opin. Neurobiol. 16, 288-297.
19. Deng, W., Neve, R.L., Rosenberg, P.A., Volpe, J.J., Jensen, F.E., 2006. Alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate receptor subunit composition and cAMP-response element-binding protein regulate oligodendrocyte excitotoxicity. J. Biol. Chem. 281, 36004-36011.
20. Dizon, M.J., Khodakhah, K., 2011. The role of interneurons in shaping Purkinje cell responses in the cerebellar cortex. J. Neurosci. 31, 10463-10473.
21. Feldmeyer, D., Kask, K., Brusa, R., Kornau, H.C., Kolhekar, R., Rozov, A., Burnashev, N., Jensen, V., Hvalby, O., Sprengel, R., Seeburg, P.H., 1999. Neurological dysfunctions in mice expressing different levels of the Q/R site-unedited AMPAR subunit GluR-B. Nat. Neurosci. 2, 57-64.
22. Fukaya, M., Yamazaki, M., Sakimura, K., Watanabe, M., 2005. Spatial diversity in gene expression for VDCCgamma subunit family in developing and adult mouse brains. Neurosci. Res. 53, 376-383.
23. Gardner, S.M., Takamiya, K., Xia, J., Suh, J.G., Johnson, R., Yu, S., Huganir, R.L., 2005. Calcium-permeable AMPA receptor plasticity is mediated by subunit-specific interactions with PICK1 and NSF. Neuron 45, 903-915.
24. 2+-permeable AMPA receptors. Science 312, 1533-1537.
25. 2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15, 193-204.
26. Gray, E.E., Fink, A.E., Sarinana, J., Vissel, B., O'Dell, T.J., 2007. Long-term potentiation in the hippocampal CA1 region does not require insertion and activation of GluR2-lacking AMPA receptors. J. Neurophysiol. 98, 2488-2492.
27. Hashimoto, K., Fukaya, M., Qiao, X., Sakimura, K., Watanabe, M., Kano, M., 1999. Impairment of AMPA receptor function in cerebellar granule cells of ataxic mutant mouse stargazer. J. Neurosci. 19, 6027-6036.
28. Hastie, P., Ulbrich, M.H., Wang, H.L., Arant, R.J., Lau, A.G., Zhang, Z., Isacoff, E.Y., Chen, L., 2013. AMPA receptor/TARP stoichiometry visualized by single-molecule subunit counting. Proc. Natl. Acad. Sci. U. S. A. 110, 5163-5168.
29. Häusser, M., Clark, B.A., 1997. Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19, 665-678.
30. Herring, B.E., Shi, Y., Suh, Y.H., Zheng, C.Y., Blankenship, S.M., Roche, K.W., Nicoll, R.A., 2013. Cornichon proteins determine the subunit composition of synaptic AMPA receptors. Neuron 77, 1083-1096.
31. 2+-permeable AMPA receptors in Bergmann glia. Science 292, 926-929.
32. Jackson, A.C., Nicoll, R.A., 2011. Stargazin (TARP gamma-2) is required for compartment-specific AMPA receptor trafficking and synaptic plasticity in cerebellar stellate cells. J. Neurosci. 31, 3939-3952.
33. Jorntell, H., Ekerot, C.F., 2003. Receptive field plasticity profoundly alters the cutaneous parallel fiber synaptic input to cerebellar interneurons in vivo. J. Neurosci. 23, 9620-9631.
34. Jorntell, H., Ekerot, C.F., 2006. Properties of somatosensory synaptic integration in cerebellar granule cells in vivo. J. Neurosci. 26, 11786-11797.
35. Kamboj, S.K., Swanson, G.T., Cull-Candy, S.G., 1995. Intracellular spermine confers rectification on rat calcium-permeable AMPA and kainate receptors. J. Physiol. 486, 297-303.
36. Karakossian, M.H., Otis, T.S., 2004. Excitation of cerebellar interneurons by group I metabotropic glutamate receptors. J. Neurophysiol. 92, 1558-1565.
37. Kato, A.S., Siuda, E.R., Nisenbaum, E.S., Bredt, D.S., 2008. AMPA receptor subunit-specific regulation by a distinct family of type II TARPs. Neuron 59, 986-996.
38. Kato, A.S., Zhou, W., Milstein, A.D., Knierman, M.D., Siuda, E.R., Dotzlaf, J.E., Yu, H., Hale, J.E., Nisenbaum, E.S., Nicoll, R.A., Bredt, D.S., 2007. New transmembrane AMPA receptor regulatory protein isoform, gamma-7, differentially regulates AMPA receptors. J. Neurosci. 27, 4969-4977.
39. Keinanen, K., Wisden, W., Sommer, B., Werner, P., Herb, A., Verdoorn, T.A., Sakmann, B., Seeburg, P.H., 1990. A family of AMPA-selective glutamate receptors. Science 249, 556-560.
40. Kelly, L., Farrant, M., Cull-Candy, S.G., 2009. Synaptic mGluR activation drives plasticity of calcium-permeable AMPA receptors. Nat. Neurosci. 12, 593-601.
41. Kim, K.S., Yan, D., Tomita, S., 2010. Assembly and stoichiometry of the AMPA receptor and transmembrane AMPA receptor regulatory protein complex. J. Neurosci. 30, 1064-1072.
42. 2+-permeable AMPA receptors in rat brain by intracellular polyamines generates double rectification. J. Physiol. 486, 305-312.
43. Korber, C., Werner, M., Kott, S., Ma, Z.L., Hollmann, M., 2007. The transmembrane AMPA receptor regulatory protein g4 is a more effective modulator of AMPA receptor function than stargazin (g2). J. Neurosci. 27, 8442-8447.
44. Kwak, S., Weiss, J.H., 2006. Calcium-permeable AMPA channels in neurodegenerative disease and ischemia. Curr. Opin. Neurobiol. 16, 281-287.
45. Lin, S.C., Huck, J.H., Roberts, J.D., Macklin, W.B., Somogyi, P., Bergles, D.E., 2005. Climbing fiber innervation of NG2-expressing glia in the mammalian cerebellum. Neuron 46, 773-785.
46. 2+-permeable AMPA receptor channels primes cell death in transient forebrain ischemia. Neuron 43, 43-55.
47. Liu, S.J., Cull-Candy, S.G., 2002. Activity-dependent change in AMPA receptor properties in cerebellar stellate cells. J. Neurosci. 22, 3881-3889.
48. 2+ permeability of AMPARs at cerebellar synapses. Nat. Neurosci. 8, 768-775.
49. 2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci. 30, 126-134.
50. Liu, S.Q., Cull-Candy, S.G., 2000. Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature 405, 454-458.
51. Liu, Y., Formisano, L., Savtchouk, I., Takayasu, Y., Szabo, G., Zukin, R.S., Liu, S.J., 2010. A single fear-inducing stimulus induces a transcription-dependent switch in synaptic AMPAR phenotype. Nat. Neurosci. 13, 223-231.
52. + channel activity alters synaptic AMPA receptor phenotype in mouse cerebellar stellate cells. J. Neurophysiol. 106, 144-152.
53. Lopez-Bayghen, E., Espinoza-Rojo, M., Ortega, A., 2003. Glutamate down-regulates GLAST expression through AMPA receptors in Bergmann glial cells. Brain Res. Mol. Brain Res. 115, 1-9.
54. Lu, W., Roche, K.W., 2012. Posttranslational regulation of AMPA receptor trafficking and function. Curr. Opin. Neurobiol. 22, 470-479.
55. Lu, Y., Allen, M., Halt, A.R., Weisenhaus, M., Dallapiazza, R.F., Hall, D.D., Usachev, Y.M., McKnight, G.S., Hell, J.W., 2007. Age-dependent requirement of AKAP150-anchored PKA and GluR2-lacking AMPA receptors in LTP. EMBO J. 26, 4879-4890.
56. 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.
57. Mathews, P.J., Lee, K.H., Peng, Z., Houser, C.R., Otis, T.S., 2012. Effects of climbing fiber driven inhibition on Purkinje neuron spiking. J. Neurosci. 32, 17988-17997.
58. Matsui, K., Jahr, C.E., Rubio, M.E., 2005. High-concentration rapid transients of glutamate mediate neural-glial communication via ectopic release. J. Neurosci. 25, 7538-7547.
59. Menuz, K., Nicoll, R.A., 2008. Loss of inhibitory neuron AMPA receptors contributes to ataxia and epilepsy in stargazer mice. J. Neurosci. 28, 10599-10603.
60. Menuz, K., O'Brien, J.L., Karmizadegan, S., Bredt, D.S., Nicoll, R.A., 2008. TARP redundancy is critical for maintaining AMPA receptor function. J. Neurosci. 28, 8740-8746.
61. Mi, R., Sia, G.M., Rosen, K., Tang, X., Moghekar, A., Black, J.L., McEnery, M., Huganir, R.L., O'Brien, R.J., 2004. AMPA receptor-dependent clustering of synaptic NMDA receptors is mediated by Stargazin and NR2A/B in spinal neurons and hippocampal interneurons. Neuron 44, 335-349.
62. Milstein, A.D., Zhou, W., Karimzadegan, S., Bredt, D.S., Nicoll, R.A., 2007. TARP subtypes differentially and dose-dependently control synaptic AMPA receptor gating. Neuron 55, 905-918.
63. Noh, K.M., Yokota, H., Mashiko, T., Castillo, P.E., Zukin, R.S., Bennett, 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, 12230-12235.
64. Nomura, T., Kakegawa, W., Matsuda, S., Kohda, K., Nishiyama, J., Takahashi, T., Yuzaki, M., 2012. Cerebellar long-term depression requires dephosphorylation of TARP in Purkinje cells. Eur. J. Neurosci. 35, 402-410.
65. Nusser, Z., Mulvihill, E., Streit, P., Somogyi, P., 1994. Subsynaptic segregation of metabotropic and ionotropic glutamate receptors as revealed by immunogold localization. Neuroscience 61, 421-427.
66. Plant, K., Pelkey, K.A., Bortolotto, Z.A., Morita, D., Terashima, A., McBain, C.J., Collingridge, G.L., Isaac, J.T., 2006. Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat. Neurosci. 9, 602-604.
67. Priel, A., Kolleker, A., Ayalon, G., Gillor, M., Osten, P., Stern-Bach, Y., 2005. Stargazin reduces desensitization and slows deactivation of the AMPA-type glutamate receptors. J. Neurosci. 25, 2682-2686.
68. Rossi, B., Maton, G., Collin, T., 2008. Calcium-permeable presynaptic AMPA receptors in cerebellar molecular layer interneurones. J. Physiol. 586, 5129-5145.
69. 2+ entry by AMPA receptors at individual GABAergic synapses in the cerebellum. J. Neurosci. 25, 4930-4940.
70. Saab, A.S., Neumeyer, A., Jahn, H.M., Cupido, A., Simek, A.A., Boele, H.J., Scheller, A., Le Meur, K., Gotz, M., Monyer, H., Sprengel, R., Rubio, M.E., Deitmer, J.W., De Zeeuw, C.I., Kirchhoff, F., 2012. Bergmann glial AMPA receptors are required for fine motor coordination. Science 337, 749-753.
71. Satake, S., Saitow, F., Yamada, J., Konishi, S., 2000. Synaptic activation of AMPA receptors inhibits GABA release from cerebellar interneurons. Nat. Neurosci. 3, 551-558.
72. Sato, K., Kiyama, H., Tohyama, M., 1993. The differential expression patterns of messenger RNAs encoding non-N-methyl-D-aspartate glutamate receptor sub-units (GluR1-4) in the rat brain. Neuroscience 52, 515-539.
73. Shi, Y., Lu, W., Milstein, A.D., Nicoll, R.A., 2009. The stoichiometry of AMPA receptors and TARPs varies by neuronal cell type. Neuron 62, 633-640.
74. Soler-Llavina, G.J., Sabatini, B.L., 2006. Synapse-specific plasticity and compartmentalized signaling in cerebellar stellate cells. Nat. Neurosci. 9, 798-806.
75. Soto, D., Coombs, I.D., Kelly, L., Farrant, M., Cull-Candy, S.G., 2007. Stargazin attenuates intracellular polyamine block of calcium-permeable AMPA receptors. Nat. Neurosci. 10, 1260-1267.
76. Soto, D., Coombs, I.D., Renzi, M., Zonouzi, M., Farrant, M., Cull-Candy, S.G., 2009. Selective regulation of long-form calcium-permeable AMPA receptors by an atypical TARP, g-5. Nat. Neurosci. 12, 277-285.
77. Sun, L., June Liu, S., 2007. Activation of extrasynaptic NMDA receptors induces a PKC-dependent switch in AMPA receptor subtypes in mouse cerebellar stellate cells. J. Physiol. 583, 537-553.
78. Swanson, G.T., Kamboj, S.K., Cull-Candy, S.G., 1997. Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J. Neurosci. 17, 58-69.
79. Szapiro, G., Barbour, B., 2007. Multiple climbing fibers signal to molecular layer interneurons exclusively via glutamate spillover. Nat. Neurosci. 10, 735-742.
80. Tomita, S., Adesnik, H., Sekiguchi, M., Zhang, W., Wada, K., Howe, J.R., Nicoll, R.A., Bredt, D.S., 2005a. Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature 435, 1052-1058.
81. Tomita, S., Chen, L., Kawasaki, Y., Petralia, R.S., Wenthold, R.J., Nicoll, R.A., Bredt, D.S., 2003. Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins. J. Cell. Biol. 161, 805-816.
82. Tomita, S., Stein, V., Stocker, T.J., Nicoll, R.A., Bredt, D.S., 2005b. Bidirectional synaptic plasticity regulated by phosphorylation of stargazin-like TARPs. Neuron 45, 269-277.
83. Turetsky, D., Garringer, E., Patneau, D.K., 2005. Stargazin modulates native AMPA receptor functional properties by two distinct mechanisms. J. Neurosci. 25, 7438-7448.
84. Vandenberghe, W., Nicoll, R.A., Bredt, D.S., 2005. Stargazin is an AMPA receptor auxiliary subunit. Proc. Natl. Acad. Sci. U. S. A. 102, 485-490.
85. Wulff, P., Schonewille, M., Renzi, M., Viltono, L., Sassoe-Pognetto, M., Badura, A., Gao, Z., Hoebeek, F.E., van Dorp, S., Wisden, W., Farrant, M., De Zeeuw, C.I., 2009. Synaptic inhibition of Purkinje cells mediates consolidation of vestibulo-cerebellar motor learning. Nat. Neurosci. 12, 1042-1049.
86. Yamazaki, M., Fukaya, M., Hashimoto, K., Yamasaki, M., Tsujita, M., Itakura, M., Abe, M., Natsume, R., Takahashi, M., Kano, M., Sakimura, K., Watanabe, M., 2010. TARPs γ-2 and γ-7 are essential for AMPA receptor expression in the cerebellum. Eur. J. Neurosci. 31, 2204-2220.
87. Yang, Y., Wang, X.B., Zhou, Q., 2010. Perisynaptic GluR2-lacking AMPA receptors control the reversibility of synaptic and spines modifications. Proc. Natl. Acad. Sci. U. S. A. 107, 11999-12004.
88. Zonouzi, M., Renzi, M., Farrant, M., Cull-Candy, S.G., 2011. Bidirectional plasticity of calcium-permeable AMPA receptors in oligodendrocyte lineage cells. Nat. Neurosci. 14, 1430-1438.