Transmembrane AMPA receptor regulatory proteins and AMPA receptor function in the cerebellum

Neuroscience

Volumn 162, Issue 3, 2009, Pages 656-665

  Coombs, I D ^a   Cull Candy, S G ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

cerebellar cells; glutamate receptors; single channels; stargazin; synaptic transmission

Indexed keywords

AMPA RECEPTOR; RECEPTOR SUBTYPE; RECEPTOR SUBUNIT; REGULATOR PROTEIN; STARGAZIN; TRANSMEMBRANE AMPA RECEPTOR REGULATOR PROTEIN; UNCLASSIFIED DRUG;

CEREBELLUM; GLIA CELL; GRANULE CELL; MOSSY FIBER; NERVE CELL; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; WILD TYPE;

ANIMALS; CEREBELLUM; MEMBRANE PROTEINS; NEURONS; PROTEIN TRANSPORT; RECEPTORS, AMPA; SYNAPTIC TRANSMISSION;

EID: 67650686804     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.01.004     Document Type: Review

References (102)

1. Bahn S., and Wisden W. A map of non-NMDA receptor subunit expression in the vertebrate brain derived from in situ hybridisation histochemistry. In: Monaghan D., and Wenthold R. (Eds). The ionotropic glutamate receptor (1997), Humana Press, Totowa, NJ 149-189
2. Bats C., Groc L., and Choquet D. The interaction between stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron 5 (2007) 719-734
3. Bedoukian M.A., Weeks A.M., and Partin K.M. Different domains of the AMPA receptor direct stargazin-mediated trafficking and stargazin-mediated modulation of kinetics. J Biol Chem 281 (2006) 23908-23921
4. Bedoukian M.A., Whitesell J.D., Peterson E.J., Clay C.M., and Partin K.M. The stargazin C terminus encodes an intrinsic and transferable membrane sorting signal. J Biol Chem 283 (2008) 1597-1600
5. Bergles D.E., Dzubay J.A., and Jahr C.E. Glutamate transporter currents in bergmann glial cells follow the time course of extrasynaptic glutamate. PNAS 94 (1997) 14821-14825
6. Bergles D.E., Roberts J.D., Somogyi P., and Jahr C.E. Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405 (2000) 187-191
7. Bowie D., and Mayer M.L. Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron 15 (1995) 453-462
8. 2+ channel gamma subunit genes reveals molecular diversification by tandem and chromosome duplication. Genome Res 9 (1999) 1204-1213
9. + channel gamma subunit genes on chromosome 19q134: evolution and expression profile of the gamma subunit gene family. Genomics 71 (2001) 339-350
10. Burnashev N., Khodorova A., Jonas P., Helm P.J., Wisden W., Monyer H., Seeburg P.H., and Sakmann B. Calcium-permeable AMPA-kainate receptors in fusiform cerebellar glial cells. Science 256 (1992) 1566-1570
11. Carter A.G., and Regehr W.G. Prolonged synaptic currents and glutamate spillover at the parallel fiber to stellate cell synapse. J Neurosci 20 (2000) 4423-4434
12. Cathala L., Holderith N.B., Nusser Z., DiGregorio D.A., and Cull-Candy S.G. Changes in synaptic structure underlie the developmental speeding of AMPA receptor-mediated EPSCs. Nat Neurosci 8 (2005) 1310-1318
13. Chen L., Bao S., Qiao X., and Thompson R.F. Impaired cerebellar synapse maturation in waggler, a mutant mouse with a disrupted neuronal calcium channel gamma subunit. Proc Natl Acad Sci U S A 96 (1999) 12132-12137
14. Chen L., Chetkovich D.M., Petralia R.S., Sweeney N.T., Kawasaki Y., Wenthold R.J., Bredt D.S., and Nicoll R.A. Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408 (2000) 936-943
15. Chetkovich D.M., Chen L., Stocker T.J., Nicoll R.A., and Bredt D.S. Phosphorylation of the postsynaptic density-95 (PSD-95)/discs large/zona occludens-1 binding site of stargazin regulates binding to PSD-95 and synaptic targeting of AMPA receptors. J Neurosci 22 (2002) 5791-5796
16. Cho C.H., St-Gelais F., Zhang W., Tomita S., and Howe J.R. Two families of TARP isoforms that have distinct effects on the kinetic properties of AMPA receptors and synaptic currents. Neuron 55 (2007) 890-904
17. Choi J., Ko J., Park E., Lee J.R., Yoon J., Lim S., and Kim E. Phosphorylation of stargazin by protein kinase A regulates its interaction with PSD-95. J Biol Chem 277 (2002) 12359-12363
18. Claudepierre T., Dalloz C., Mornet D., Matsumura K., Sahel J., and Rendon A. Characterization of the intermolecular associations of the dystrophin-associated glycoprotein complex in retinal Müller glial cells. J Cell Sci 113 (2000) 3409-3417
19. Coleman S.K., Möykkynen T., Cai C., von Ossowski L., Kuismanen E., Korpi E.R., and Keinänen K. Isoform-specific early trafficking of AMPA receptor flip and flop variants. J Neurosci 26 (2006) 11220-11229
20. 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 (2004) 7491-7502
21. Dakoji S., Tomita S., Karimzadegan S., Nicoll R.A., and Bredt D.S. Interaction of transmembrane AMPA receptor regulatory proteins with multiple membrane associated guanylate kinases. Neuropharmacology 45 (2003) 849-856
22. Deng F., Price M.G., Davis C.F., Mori M., and Burgess D.L. Stargazin and other transmembrane AMPA receptor regulating proteins interact with synaptic scaffolding protein magi-2 in brain. J Neurosci 26 (2006) 7875-7884
23. DiGregorio D.A., Nusser Z., and Silver R.A. Spillover of glutamate onto synaptic AMPA receptors enhances fast transmission at a cerebellar synapse. Please provide the city name for each publisher 35 (2002) 521-533
24. 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
25. Douyard J., Shen L., Huganir R.L., and Rubio M.E. Differential neuronal and glial expression of GluR1 AMPA receptor subunit and the scaffolding proteins sap 97 and 4.1 N during rat cerebellar development. J Comp Neurol 502 (2007) 141-156
26. Dzubay J.A., and Jahr C.E. The concentration of synaptically released glutamate outside of the climbing fiber-Purkinje cell synaptic cleft. J Neurosci 19 (1999) 5265-5274
27. Ferron L., Davies A., Page K.M., Cox D.J., Leroy J., Waithe D., Butcher A.J., Sellaturay P., Bolsover S., Pratt W.S., Moss F.J., and Dolphin A.C. The stargazin-related protein gamma 7 interacts with the mRNA-binding protein heterogeneous nuclear ribonucleoprotein A2 and regulates the stability of specific mRNAs, including CaV22. J Neurosci 28 (2008) 10604-10617
28. Fukata Y., Tzingounis A.V., Trinidad J.C., Fukata M., Burlingame A.L., Nicoll R.A., and Bredt D.S. Molecular constituents of neuronal AMPA receptors. J Cell Biol 169 (2005) 399-404
29. Fukaya M., Yamazaki M., Sakimura K., and Watanabe M. Spatial diversity in gene expression for VDCCgamma subunit family in developing and adult mouse brains. Neurosci Res 53 (2005) 376-383
30. Gall D., Prestori F., Sola E., D'Errico A., Roussel C., Forti L., Rossi P., and D'Angelo E. Intracellular calcium regulation by burst discharge determines bidirectional long-term synaptic plasticity at the cerebellum input stage. J Neurosci 25 (2005) 4813-4822
31. Gallo V. Suprising synapses deep in the brain. Nat Neurosci 10 (2007) 267-269
32. Gallo V., Upson L.M., Hayes W.P., Vyklicky Jr. L., Winters C.A., and Buonanno A. Molecular cloning and development analysis of a new glutamate receptor subunit isoform in cerebellum. J Neurosci 12 (1992) 1010-1023
33. 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
34. 2+ channel gamma subunit. J Physiol 533 (2001) 467-478
35. 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
36. 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
37. Greger I.H., and Esteban J.A. AMPA receptor biogenesis and trafficking. Curr Opin Neurobiol 17 (2007) 289-297
38. Hashimoto K., Fukaya M., Qiao X., Sakimura K., Watanabe M., and Kano M. Impairment of AMPA receptor function in cerebellar granule cells of ataxic mutant mouse stargazer. J Neurosci 19 (1999) 6027-6036
39. 2+-permeable AMPA receptors in Bergmann glia. Science 292 (2001) 926-929
40. Ives J.H., Fung S., Tiwari P., Payne H.L., and Thompson C.L. Microtubule-associated protein light chain 2 is a stargazin-AMPA receptor complex-interacting protein in vivo. J Biol Chem 279 (2004) 31002-31009
41. Jay S.D., Ellis S.B., McCue A.F., Williams M.E., Vedvick T.S., Harpold M.M., and Campbell K.P. Primary structure of the gamma subunit of the DHP-sensitive calcium channel from skeletal muscle. Science 248 (1990) 490-492
42. Kamboj S.K., Swanson G.T., and Cull-Candy S.G. Intracellular spermine confers rectification on rat calcium-permeable AMPA and kainate receptors. J Physiol 486 (1995) 297-303
43. 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., and Bredt D.S. New transmembrane AMPA receptor regulatory protein isoform, gamma-7, differentially regulates AMPA receptors. J Neurosci 27 (2007) 4969-4977
44. Kato A.S., Siuda E.R., Nisenbaum E.S., and Bredt D.S. AMPA receptor subunit-specific regulation by a distinct family of type II TARPs. Neuron 59 (2008) 986-996
45. Keinänen K., Wisden W., Sommer B., Werner P., Herb A., Verdoorn T.A., Sakmann B., and Seeburg P.H. A family of AMPA-selective glutamate receptors. Science 249 (1990) 556-560
46. Klugbauer N., Dai S., Specht V., Lacinová L., Marais E., Bohn G., and Hofmann F. A family of gamma-like calcium channel subunits. FEBS Lett 470 (2000) 189-197
47. 2+-permeable AMPA receptors in rat brain by intracellular polyamines generates double rectification. J Physiol 486 (1995) 305-312
48. Korber C., Werner M., Kott S.Z.L., and Hollmann M. The transmembrane AMPA receptor regulatory protein gamma 4 is a more effective modulator of AMPA receptor function than stargazin (gamma 2). J Neurosci 27 (2007) 8442-8447
49. Kott S., Werner M., Körber C., and Hollmann M. Electrophysiological properties of AMPA receptors are differentially modulated depending on the associated member of the TARP family. J Neurosci 27 (2007) 3780-3789
50. Kristensen A.S., and Traynelis S.F. Neuroscience: an intrusive chaperone. Nature 435 (2005) 1042-1043
51. Kukley M., Capetillo-Zarate E., and Dietrich D. Vesicular glutamate release from axons in white matter. Nat Neurosci 10 (2007) 311-320
52. Lambolez B., Audinat E., Bochet P., Crépel F., and Rossier J. AMPA receptor subunits expressed by single Purkinje cells. Neuron 9 (1992) 247-258
53. Lein E.S., et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445 (2007) 168-176
54. Leonoudakis D., Mailliard W., Wingerd K., Clegg D., and Vandenberg C. Inward rectifier potassium channel Kir22 is associated with synapse-associated protein SAP97. J Cell Sci 114 (2001) 987-998
55. 2+-channel gamma subunit. Nat Genet 19 (1998) 340-347
56. Lin S.C., Huck J.H., Roberts J.D., Macklin W.B., Somogyi P., and Bergles D.E. Climbing fiber innervation of NG2-expressing glia in the mammalian cerebellum. Neuron 46 (2005) 773-785
57. 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
58. 2+ permeability of AMPARs at cerebellar synapses. Nat Neurosci 8 (2005) 768-775
59. Liu S.J. Biphasic modulation of GABA release from stellate cells by glutamatergic receptor subtypes. J Neurophysiol 98 (2007) 550-556
60. Mapelli J., and D'Angelo E. The spatial organization of long-term synaptic plasticity at the input stage of cerebellum. J Neurosci 27 (2007) 1285-1296
61. Matsuda S., Miura E., Matsuda K., Kakegawa W., Kohda K., Watanabe M., and Yuzaki M. Accumulation of AMPA receptors in autophagosomes in neuronal axons lacking adaptor protein AP-4. Neuron 57 (2008) 730-745
62. Matsui K., and Jahr C.E. Ectopic release of synaptic vesicles. Neuron 40 (2003) 1173-1183
63. Matsui K., Jahr C.E., and Rubio M.E. High-concentration rapid transients of glutamate mediate neural-glial communication via ectopic release. J Neurosci 25 (2005) 7538-7547
64. Menuz K., Stroud R.M., Nicoll R.A., and Hays F.A. TARP auxiliary subunits switch AMPA receptor antagonists into partial agonists. Science 318 (2007) 815-817
65. Menuz K., O'Brien J.L., Karmizadegan S., Bredt D.S., and Nicoll R.A. TARP redundancy is critical for maintaining AMPA receptor function. J Neurosci 28 (2008) 8740-8746
66. Menuz K., and Nicoll R.A. Loss of inhibitory neuron AMPA receptors contributes to ataxia and epilepsy in stargazer mice. J Neurosci 28 (2008) 10599-10603
67. Milstein A.D., Zhou W., Karimzadegan S., Bredt D.S., and Nicoll R.A. TARP subtypes differentially and dose-dependently control synaptic AMPA receptor gating. Neuron 55 (2007) 905-918
68. Momiyama A., Silver R.A., Hausser M., Notomi T., Wu Y., Shigemoto R., and Cull-Candy S.G. The density of AMPA receptors activated by a transmitter quantum at the climbing fibre-Purkinje cell synapse in immature rats. J Physiol 549 (2003) 75-92
69. Morimoto-Tomita M., Zhang W., Straub C., Cho C.H., Kim K.S., Howe J.R., and Tomita S. Autoinactivation of neuronal AMPA receptors via glutamate-regulated TARP interaction. Neuron 61 (2009) 101-112
70. Mosbacher J., Schoepfer R., Monyer H., Burnashev N., Seeburg P.H., and Ruppersberg J.P. A molecular determinant for submillisecond desensitization in glutamate receptors. Science 266 (1994) 1059-1062
71. Nicoll R.A., Tomita S., and Bredt D.S. Auxiliary subunits assist AMPA-type glutamate receptors. Science 311 (2006) 1253-1256
72. Noebels J.L., Qiao X., Bronson R.T., Spencer C., and Davisson M.T. Stargazer: a new neurological mutant on chromosome 15 in the mouse with prolonged cortical seizures. Epilepsy Res 7 (1990) 129-135
73. Osten P., and Stern-Bach Y. Learning from stargazin: the mouse, the phenotype and the unexpected. Curr Opin Neurobiol 16 (2006) 275-280
74. Petralia R.S., Wang Y.X., Mayat E., and Wenthold R.J. Glutamate receptor subunit 2-selective antibody shows a differential distribution of calcium-impermeable AMPA receptors among populations of neurons. J Comp Neurol 385 (1997) 456-476
75. Piet R., and Jahr C.E. Glutamatergic and purinergic receptor-mediated calcium transients in Bergmann glial cells. J Neurosci 27 (2007) 4027-4035
76. Price M.G., Davis C.F., Deng F., and Burgess D.L. The alpha-amino-3-hydroxyl-5-methyl-4-isoxazolepropionate receptor trafficking regulator "stargazin" is related to the claudin family of proteins by its ability to mediate cell-cell adhesion. J Biol Chem 280 (2005) 19711-19720
77. 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
78. Rossi B., Maton G., and Collin T. Calcium permeable presynaptic AMPA receptors in cerebellar molecular layer interneurons. J Physiol 586 (2008) 5129-5145
79. 2+ channel expressed in Xenopus oocytes. J Physiol 532 (2001) 583-593
80. 2+ entry by AMPA receptors at individual GABAergic synapses in the cerebellum. J Neurosci 25 (2005) 4930-4940
81. Satake S., Saitow F., Yamada J., and Konishi S. Synaptic activation of AMPA receptors inhibits GABA release from cerebellar interneurons. Nat Neurosci 3 (2000) 551-558
82. Sharpey-Schafer E. The essentials of histology (1929), Longmans, Green, & Co, London
83. Soto D., Coombs I.D., Kelly L., Farrant M., and Cull-Candy S.G. Stargazin attenuates intracellular polyamine block of calcium-permeable AMPA receptors. Nat Neurosci 10 (2007) 1260-1267
84. Soto D., Coombs I.D., Renzi M., Zonouzi M., Farrant M., and Cull-Candy S.G. Selective regulation of long-form calcium-permeable AMPA receptors by a novel TARP. Nat Neurosci (2009) (in press)
85. 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
86. Tomita S., Chen L., Kawasaki Y., Petralia R.S., Wenthold R.J., Nicoll R.A., and Bredt D.S. Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins. J Cell Biol 161 (2003) 805-816
87. Tomita S., Fukata M., Nicoll R.A., and Bredt D.S. Dynamic interaction of stargazin-like TARPs with cycling AMPA receptors at synapses. Science 303 (2004) 1508-1511
88. Tomita S., Sekiguchi M., Wada K., Nicoll R.A., and Bredt D.S. Stargazin controls the pharmacology of AMPA receptor potentiators. PNAS 103 (2006) 10064-10067
89. Tomita S., Stein V., Stocker T.J., Nicoll R.A., and Bredt D.S. Bidirectional synaptic plasticity regulated by phosphorylation of stargazin-like TARPs. Neuron 45 (2005) 269-277
90. Tomita S., Adesnik H., Sekiguchi M., Zhang W., Wada K., Howe J.R., Nicoll R.A., and Bredt D.S. Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature 435 (2005) 1052-1058
91. Tomita S., Shenoy A., Fukata Y., Nicoll R.A., and Bredt D.S. Stargazin interacts functionally with the AMPA receptor glutamate-binding module. Neuropharmacology 52 (2007) 87-91
92. Turetsky D., Garringer E., and Patneau D.K. Stargazin modulates native AMPA receptor functional properties by two distinct mechanisms. J Neurosci 25 (2005) 7438-7448
93. Vandenberghe W., Nicoll R.A., and Bredt D.S. Stargazin is an AMPA receptor auxiliary subunit. Proc Natl Acad Sci U S A 102 (2005) 485-490
94. Vandenberghe W., Nicoll R.A., and Bredt D.S. Interaction with the unfolded protein response reveals a role for stargazin in biosynthetic AMPA receptor transport. J Neurosci 25 (2005) 1095-1102
95. Walker C.S., Brockie P.J., Madsen D.M., Francis M.M., Zheng Y., Koduri S., Mellem J.E., Strutz-Seebohm N., and Maricq A.V. Reconstitution of invertebrate glutamate receptor function depends on stargazin-like proteins. Proc Natl Acad Sci U S A 103 (2006) 10781-10786
96. 2+-permeable glutamate receptors. TINS 25 (2002) 5-6
97. Wisden W., and Seeburg P.H. Mammalian ionotropic glutamate receptors. Curr Opin Neurobiol 3 (1993) 291-298
98. Wyllie D.J., Mathie A., Symonds C.J., and Cully-Candy S.G. Activation of glutamate receptors and glutamate uptake in identified macroglial cells in rat cerebellar cultures. J Physiol 432 (1991) 235-258
99. 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
100. Yamazaki M., Ohno-Shosaku T., Fukaya M., Kano M., Watanabe M., and Sakimura K. A novel action of stargazin as an enhancer of AMPA receptor activity. Neurosci Res 50 (2004) 369-374
101. Ziff E.B. TARPs and the AMPA receptor trafficking paradox. Neuron 5 (2007) 627-633
102. Ziskin J.L., Nishiyama A., Rubio M., Fukaya M., and Bergles D.E. Vesicular release of glutamate from unmyelinated axons in white matter. Nat Neurosci 10 (2007) 321-330