The role of transmembrane AMPA receptor regulatory proteins (TARPs) in neurotransmission and receptor trafficking (Review)

References

• Hollmann M, Heinemann S. Cloned glutamate receptors. Ann Rev Neurosci 1994; 17: 31–108
   PubMed Web of Science ®Google Scholar
• Dingledine R, Borges K, Bowie D, Traynelis SF. The glutamate receptor ion channels. Pharm Rev 1999; 51: 7–61
   PubMed Web of Science ®Google Scholar
• Malenka RC, Nicoll RA. Long-term potentiation – a decade of progress?. Science. 1999; 285: 1870–1874
   PubMed Web of Science ®Google Scholar
• Malinow R, Malenka RC. AMPA Receptor Trafficking and Synaptic Plasticity. Ann Rev Neurosci 2002; 25: 103–126
   PubMed Web of Science ®Google Scholar
• Song I, Huganir RL. Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci 2002; 25: 578–588
   PubMed Web of Science ®Google Scholar
• Dong H, O'Brien RJ, Fung ET, Lanahan AA, Worley PF, Huganir RL. GRIP: A synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature. 1997; 386: 279–284
   PubMed Web of Science ®Google Scholar
• Srivastava S, Osten P, Vilim FS, Khatri L, Inman GJ, States BA, Daly C, DeSouza S, Abagyan R, Valtschanoff JG, Weinberg RJ, Ziff EB. Novel anchorage of GluR2/3 to postsynaptic density by an AMPA receptor binding protein ABP. Neuron 1998; 21: 581–591
   PubMedGoogle Scholar
• Dev KK, Nishimune A, Henley JM, Nakanishi S. The protein kinase C( binding protein PICK1 interacts with short but not long form alternative splice variants of AMPA receptor subunits. Neuropharm 1999; 38: 635–644
   PubMed Web of Science ®Google Scholar
• Xia J, Zhang X, Staudinger J, Huganir RL. Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1. Neuron 1999; 22: 179–187
   PubMed Web of Science ®Google Scholar
• Henley JM. Proteins interactions implicated in AMPA receptor trafficking: A clear destination and an improving route map. Neurosci Res 2003; 45: 243–254
   Google Scholar
• Bredt DS, Nicoll RA. AMPA receptor trafficking at excitatory synapses. Neuron 2003; 40: 361–379
   PubMed Web of Science ®Google Scholar
• Noebels JL, Qiao X, Bronson RT, Spencer C, Davisson MT. Stargazer: A new neurological mutant on chromosome 15 in the mouse with prolonged cortical seizures. Epilepsy Res 1990; 7: 129–135
   PubMed Web of Science ®Google Scholar
• Letts VA, Felix R, Biddlecome GH, Arikkath J, Mahaffey CL, Valenzuela A, Bartlett II FS, Mori Y, Campbell KP, Frankel WN. The mouse Stargazer gene encodes a neuronal Ca2 + -channel ( subunit. Nat Gen 1998; 19: 340–347
   PubMed Web of Science ®Google Scholar
• Klugbauer N, Dai S, Sprecht V, Lacinová L, Marais E, Bohn G, Hofmann F. A family of γ-like calcium channel subunits. Fed Euro Biochem Soc Lett 2000; 470: 189–197
   PubMed Web of Science ®Google Scholar
• Rousset M, Cens T, Restituito S, Barrere C, Black III JL, McEnery MW, Charnet P. Functional roles of γ2, γ3 and γ4, three new Ca2+ channel subunits, in P/Q-type Ca2+ channel expressed in Xenopus oocytes. J Physiol 2001; 532.3: 583–593
   Google Scholar
• Green PJ, Warre R, Hayes PD, McNaughton NCL, Medhurst AD, Pangalos M, Duckworth DM, Randall AD. Kinetic modification of the α1I subunit-mediated T-type Ca2+ channel by a human neuronal Ca2 +  channel γ subunit. J Physiol 2001; 533.2: 467–478
   Google Scholar
• Tomita S, Chen L, Kawasaki Y, Petralia RS, Wenthold RJ, Nicoll RA, Bredt DS. Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins. J Cell Biol 2003; 161: 805–816
   Google Scholar
• Sharp AH, Black III JL, Dubel SJ, Sundarraj S, Shen JP, Yunker AMR, Copeland TD, Mcenery MW. Biochemical and anatomical evidence for specialized voltage-dependent calcium channel γ isoform expression in the epileptic and ataxic mouse, Stargazer. Neuroscience 2001; 105: 599–617
   Google Scholar
• Chu PJ, Robertson HM, Best PM. Calcium channel γ subunits provide insights into the evolution of this gene family. Gene 2001; 280: 37–48
   Google Scholar
• Moss FJ, Viard P, Davies A, Bertaso F, Page KM, Graham A, Canti C, Plumpton M, Plumpton C, Clare JJ, Dolphin AC. The novel product of a five-exon stargazin-related gene abolishes Cav2.2 calcium channel expression. Eur Mol Biol Org 2002; 21: 1514–1523
   Google Scholar
• Inamura M, Itakura M, Okamoto H, Hoka S, Mizoguchi A, Fukazawa Y, Shigemoto R, Yamamori S, Takahashi M. Differential localization and regulation of stargazin-like protein, (-8 and stargazin in the plasma membrane of hippocampal and cortical neurons. Neurosci Res 2006; 55: 45–53
   Google Scholar
• Fukaya M, Tsujita M, Yamazaki M, Kushiya E, Abe M, Akashi K, Natsume R, Kano M, Kamiya H, Watanabe M, Sakimura K. Abundant distribution of TARP γ-8 in synaptic and extrasynaptic surface of hippocampal neurons and its major role in AMPA receptor expression on spines and dendrites. Eur J Neurosci 2006; 24: 2177–2190
   Google Scholar
• Rouach N, Byrd K, Petralia RS, Elias GM, Adesnik H, Tomita S, Karimzadegan S, Kealey C, Bredt DS, Nicoll RA. TARP γ-8 controls hippocampal AMPA receptor number, distribution and synaptic plasticity. Nat Neurosci 2005; 8: 1525–1533
   PubMedGoogle Scholar
• Kato AS, Zhou W, Milstein AD, Knierman MD, Siuda ER, Dotzlaf JE, Yu H, Hale JE, Nisenbaum ES, Nicoll RA, Bredt DS. New transmembrane AMPA receptor regulatory protein isoform, (7, differentially regulates AMPA receptors. J Neurosci 2007; 27: 4969–4977
   Google Scholar
• Vandenberghe W, Nicoll RA, Bredt DS. Stargazin is an AMPA receptor auxiliary subunit. PNAS 2005; 102: 485–490
   Google Scholar
• Ives JH, Fung S, Tiwari P, Payne HL, Thompson CL. Microtubule-associated Protein Light Chain 2 is a Stargazin-AMPA Receptor Complex-interacting Protein in vivo. J Biol Chem 2004; 279: 31002–31009
   Google Scholar
• Vandenberghe W, Nicoll RA, Bredt DS. Interaction with the Unfolded Protein Response reveals a role for stargazin in biosynthetic AMPA receptor transport. J Neurosci 2005; 25: 1095–1102
   Google Scholar
• Chen L, Chetkovich DM, Petralia RS, Sweeney NT, Kawasaki Y, Wenthold RJ, Bredt DS, Nicoll RA. Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 2000; 408: 936–943
   PubMed Web of Science ®Google Scholar
• Hashimoto K, Fukaya M, Qiao X, Sakimura K, Watanabe M, Kano M. Impairment of AMPA receptor function in cerebellar granule cells of ataxic mutant mouse Stargazer. J Neurosci 1999; 19: 6027–6036
   Google Scholar
• Cho C, St-Gelais F, Zhang W, Tomita S, Howe JR. Two families of TARP isoforms that have distinct effects on the kinetic properties of AMPA receptors and synaptic currents. Neuron 2007; 55: 890–904
   Google Scholar
• Cuadra AE, Kuo S, Kawasaki Y, Bredt DS, Chetkovich DM. AMPA receptor synaptic targeting regulated by stargazin interactions with the Golgi-resident PDZ protein nPIST. J Neurosci 2004; 24: 7491–7502
   Google Scholar
• Tomita S, Fukata M, Nicoll RA, Bredt DS. Dynamic interaction of stargazin-like TARPs with cycling AMPA receptors at synapses. Science 2004; 303: 1508–1511
   PubMed Web of Science ®Google Scholar
• Schnell E, Sizemore M, Karimzadegan S, Chen L, Bredt DS, Nicoll RA. Direct interactions between PSD-95 and stargazing control synaptic AMPA receptor number. PNAS 2002; 99: 13902–13907
   PubMed Web of Science ®Google Scholar
• Bats C, Groc L, Choquet D. The interaction between stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron 2007; 53: 719–734
   PubMed Web of Science ®Google Scholar
• Deng F, Price MG, Davis CF, Mori M, Burgess DL. Stargazin and other transmembrane AMPA receptor regulating proteins interact with synaptic scaffolding protein MAGI-2 in brain. J Neurosci 2006; 26: 7875–7884
   Google Scholar
• Choi J, Ko J, Park E, Lee J, Yoon J, Lim S, Kim E. Phosphorylation of stargazin by protein kinase A regulates its interaction with postsynaptic density-95 (PSD-95). J Biol Chem 2002; 277: 12359–12363
   Google Scholar
• Chetkovich DM, Chen L, Stocker TJ, Nicoll RA, Bredt DS. 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 2002; 22: 5791–5796
   Google Scholar
• Tomita S, Stein V, Stocker TJ, Nicoll RA, Bredt DS. Bidirectional synaptic plasticity regulated by phosphorylation of stargazin-like TARPs. Neuron 2005; 45: 269–277
   Google Scholar
• Yamasaki M, Ohno-Shosaku T, Fukaya M, Kano M, Watanabe M, Sakimura K. A novel action of stargazin as an enhancer of AMPA receptor activity. Neurosci Res 2004; 50: 369–374
   Google Scholar
• Priel A, Kolleker A, Ayalon G, Gillor M, Osten P, Stern-Bach Y. Stargazin reduces desensitization and slows deactivation of the AMPA-type glutamate receptors. J Neurosci 2005; 25: 2682–2686
   PubMed Web of Science ®Google Scholar
• Turetsky D, Garringer E, Patneau DK. Stargazin modulates native AMPA receptor functional properties by two distinct mechanisms. J Neurosci 2005; 25: 7438–7448
   Google Scholar
• Tomita S, Adesnik H, Sekiguchi M, Zhang W, Wada K, Howe JR, Nicoll RA, Bredt DS. Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature 2005; 435: 1052–1058
   PubMed Web of Science ®Google Scholar
• Kott S, Werner M, Korber C, Hollmann M. Electrophysiological properties of AMPA receptors are differentially modulated depending on the associated member of the TARP family. J Neurosci 2007; 27: 3780–3789
   Google Scholar
• Korber C, Werner M, Kott S, Ma Z, Hollmann M. The transmembrane AMPA receptor regulatory protein γ4 is a more effective modulator of AMPA receptor function than stargazin (γ2). J Neurosci 2007; 27: 8442–8447
   Google Scholar
• Milstein AD, Zhou W, Karimzadegan S, Bredt DS, Nicoll RA. TARP subtypes differentially and dose-dependently control synaptic AMPA receptor gating. Neuron 2007; 55: 905–918
   PubMedGoogle Scholar
• Soto D, Coombs ID, Kelly L, Farrant M, Cull-Candy SG. Stargazin attenuates intracellular polyamine block of calcium-permeable AMPA receptors. Nat Neurosci 2007; 10: 1260–1267
   Google Scholar
• Qiao X, Hefti F, Knusel B, Noebels JL. Selective failure of brain-derived neurotrophic factor mRNA expression in the cerebellum of stargazer, a mutant mouse with ataxia. J Neurosci 1996; 16: 640–648
   Google Scholar
• Qiao X, Chen L, Gao H, Bao S, Hefti F, Thompson RF, Knusel B. Cerebellar brain derived neurotrophic factor-TrkB defect associated with impairment of eyeblink conditioning in Stargazer mutant mice. J Neurosci 1998; 18: 6990–6999
   Google Scholar
• Qiao X, Noebels JL. Developmental analysis of hippocampal mossy fiber outgrowth in a mutant mouse with inherited spike-wave seizures. J Neurosci 1993; 13: 4622–4635
   Google Scholar
• Nusser Z, Sieghart W, Somogyi P. Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J Neurosci 1998; 18: 1693–1703
   PubMedGoogle Scholar
• Ives JH, Drewery DL, Thompson CL. Differential cell surface expression of GABAA receptor α1, α6, β2 and β3 subunits in cultured mouse cerebellar granule cells influence of cAMP-activated signalling. J Neurochem 2002; 80: 317–327
   Google Scholar
• Leroy C, Poisbeau P, Keller AF, Nehlig A. Pharmacological plasticity of GABAA receptors at dentate gyrus synapses in a rat model of temporal lobe epilepsy. J Physiol 2004; 557: 473–487
   PubMed Web of Science ®Google Scholar
• Peng Z, Huang CS, Stell BM, Mody I, Houser CR. Altered expression of the δ subunit of the GABAA receptor in a mouse model of temporal lobe epilepsy. J Neurosci 2004; 24: 8629–8639
   Google Scholar
• Yamada MK, Nakanishi K, Ohba S, Nakamura T, Ikegaya Y, Nishiyama N, Matsuki N. Brain-derived neurotrophic factor promotes the maturation of GABAergic mechanisms in cultured hippocampal neurons. J Neurosci 2002; 22: 7580–7585
   PubMed Web of Science ®Google Scholar
• Jovanovic JN, Thomas P, Kittler JT, Smart TG, Moss SJ. Brain-derived neurotrophic factor modulates fast synaptic inhibition by regulating GABAA receptor phosphorylation, activity and cell-surface stability. J Neurosci 2004; 24: 522–530
   Google Scholar
• Elmiariah SB, Crumling MA, Parsons TD, Balice-Gordon RJ. Postsynaptic TrkB-mediated signalling modulates excitatory and inhibitory neurotransmitter receptor clustering at hippocampal synapses. J Neurosci 2004; 24: 2380–2393
   Google Scholar
• Chen L, Bao S, Qiao X, Thompson RF. Impaired cerebellar synapse maturation in waggler, a mutant mouse with a disrupted neuronal calcium channel γ subunit. PNAS 1999; 96: 12132–12137
   Google Scholar
• Tia S, Wang JF, Kotchabhakdi N, Vicini S. Developmental changes of inhibitory synaptic currents in cerebellar granule neurons: role of GABAA receptor α6 subunit. J Neurosci 1996; 16: 3630–3640
   Google Scholar
• Payne HL, Connelly WMK, Ives JH, Lehner R, Furtmuller B, Sieghart W, Tiwari P, Lucocq JM, Lees G, Thompson CL. GABAA α6-containing receptors are selectively compromised in cerebellar granule cells of the ataxic mouse, stargazer. J Biol Chem 2007; 282: 29130–29143
   Google Scholar
• Brickley SG, Cull-Candy SG, Farrant M. Development of a tonic form of synaptic inhibition in rat cerebellar granule cells resulting from persistent activation of GABAA receptors. J Physiol 1996; 497: 753–759
   PubMed Web of Science ®Google Scholar
• Brickley SG, Cull-Candy SG, Farrant M. Single-channel properties of synaptic and extrasynaptic GABAA receptors suggest differential targeting of receptor subtypes. J Neurosci 1999; 19: 2960–2973
   Google Scholar
• Hamann M, Rossi DJ, Attwell D. Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron 2002; 33: 625–633
   Google Scholar
• Suzuki K, Sato M, Morishima Y, Nakanishi S. Neuronal depolarization controls brain-derived neurotrophic factor-induced upregulation of NR2C NMDA receptor via calcineurin signaling. J Neurosci 2005; 25: 9535–9543
   Google Scholar
• Bulleit RF, Hsieh T. MEK inhibitors block BDNF-dependent and -independent expression of GABAA receptor subunit mRNAs in cultured mouse cerebellar granule neurons. Dev Brain Res 2000; 119: 1–10
   PubMedGoogle Scholar
• Payne HL, Ives JH, Sieghart W, Thompson CL. 2007. AMPA and Kainate receptors mediate mutually exclusive effects on GABAA receptor expression in cultured mouse cerebellar granule neurons. J Neurochem ( in press).
   Google Scholar
• Brooks-kayal AR, Shumate MD, Jin H, Rikhter TY, Coulter DA. Selective changes in single cell GABAA receptor subunit expression and function in temporal lobe epilepsy. Nat Med 1998; 4: 1166–1172
   PubMed Web of Science ®Google Scholar
• Shumate MD, Lin DD, Gibbs JW, III, Holloway KL, Coulter DA. GABAA receptor function in epileptic human dentate granule cells: Comparison to epileptic and control rat. Epilepsy Res 1998; 32: 114–128
   Google Scholar
• Cohen AS, Lin DD, Quirk GL, Coulter DA. Dentate granule cell GABAA receptors in epileptic hippocampus: enhanced synaptic efficacy and altered pharmacology. Eur J Neurosci 2003; 17: 1607–1616
   Google Scholar
• Chaftez RS, Nahm WK, Noebels JL. Aberrant expression of neuropeptide Y in hippocampal mossy fibers in the absence of local cell injury following onset of spike-wave synchronisation. Mol Brain Res 1995; 31: 111–121
   Google Scholar
• Nahm WK, Noebels JL. Nonobligate role of early or sustained expression of immediate-early gene proteins c-Fos, c-Jun, and Zif/268 in hippocampal mossy fiber sprouting. J Neurosci 1998; 18: 9245–9255
   Google Scholar
• Payne HL, Donoghue PS, Connelly WMK, Hinterreiter S, Tiwari P, Ives JH, Hann V, Sieghart W, Lees G, Thompson CL. Aberrant GABAA receptor expression in the dentate gyrus of the epileptic mutant mouse Stargazer. J Neurosci 2006; 26: 8600–8608
   Google Scholar
• Nusser Z, Mody I. Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. J Neurophysiol 2002; 87: 2624–2628
   PubMed Web of Science ®Google Scholar
• Martinez-Turrillas R, Del Rio J, Frechilla D. Neuronal proteins involved in synaptic targeting of AMPA receptors in rat hippocampus by antidepressant drugs. Biochem Biophys Res Com 2007; 353: 750–755
   PubMed Web of Science ®Google Scholar
• Tomita S, Sekiguchi M, Wada K, Nicoll RA, Bredt DS. Stargazin controls the pharmacology of AMPA receptor potentiators. PNAS 2006; 103: 10064–10067
   Google Scholar