Abstract
For synapses to form and function, neurotransmitter receptors must be recruited to a location on the postsynaptic cell in direct apposition to presynaptic neurotransmitter release. However, once receptors are inserted into the postsynaptic membrane, they are not fixed in place but are continually exchanged between synaptic and extrasynaptic regions, and they cycle between the surface and intracellular compartments. This article highlights and compares the current knowledge about the dynamics of acetylcholine receptors at the vertebrate peripheral neuromuscular junction and AMPA, N-methyl-d-aspartate, and γ-aminobutyric acid receptors in central synapses.
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Malenka R. C. (2003) Synaptic plasticity and AMPA receptor trafficking. Ann. NY Acad. Sci. 1003, 1–11.
Collingridge G. L., Isaac J. T., and Wang Y. T. (2004) Receptor trafficking and synaptic plasticity. Nat. Rev. Neurosci. 5, 952–962.
Bredt D. S. and Nicoll R. A. (2003) AMPA receptor trafficking at excitatory synapses. Neuron 40, 361–379.
Bliss T. V. and Lomo T. (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232, 331–356.
Bear M. F. and Malenka R. C. (1994) Synaptic plasticity: LTP and LTD. Curr. Opin. Neurobiol. 4, 389–399.
Hollmann M. and Heinemann S. (1994) Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31–108.
Zhu J. J., Esteban J. A., Hayashi Y., and Malinow R. (2000) Postnatal synaptic potentiation: delivery of GluR4-containing AMPA receptors by spontaneous activity. Nat. Neurosci. 3, 1098–1106.
Huh K. H. and Wenthold R. J. (1999) Turnover analysis of glutamate receptors identifies a rapidly degraded pool of the N-methyl-D-aspartate receptor subunit, NR1, in cultured cerebellar granule cells. J. Biol. Chem. 274, 151–157.
Archibald K., Perry M. J., Molnar E., and Henley J. M. (1998) Surface expression and metabolic half-life of AMPA receptors in cultured rat cerebellar granule cells. Neuropharmacology 37, 1345–1353.
Mammen A. L., Huganir R. L., and O'Brien R. J. (1997) Redistribution and stabilization of cell surface glutamate receptors during synapse formation. J. Neurosci. 17, 7351–7358.
O'Brien, R. J., Kamboj, S., Ehlers, M. D., Rosen, K. R., Fischbach, G. D., and Huganir, R. L. (1998) Activity-dependent modulation of synaptic AMPA receptor accumulation. Neuron 21, 1067–1078.
Ehlers M. D. (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28, 511–525.
Park M., Penick E. C., Edwards, J. G., Kauer J. A., and Ehlers M. D. (2004) Recycling endosomes supply AMPA receptors for LTP. Science 305, 1972–1975.
Passafaro M., Piech V., and Sheng M. (2001) Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat. Neurosci. 4, 917–926.
Lin, J. W., Ju, W., Foster, K., et al. (2000) Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization. Nat. Neurosci. 3, 1282–1290.
Sekine-Aizawa Y. and Huganir R. L. (2004) Imaging of receptor trafficking by using alpha-bungarotoxin-binding-site-tagged receptors. Proc. Natl. Acad. Sci. USA 101, 17,114–17,119.
Luscher, C., Xia, H., Beattie, E. C., et al. (1999) Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24, 649–658.
Luthi, A., Chittajallu, R., Duprat, F., et al. (1999) Hippocampal LTD expression involves a pool of AMPARs regulated by the NSF-GluR2 interaction. Neuron 24, 389–399.
Lee S. H., Simonetta A., and Sheng M. (2004) Subunit rules governing the sorting of internalized AMPA receptors in hippocampal neurons. Neuron 43, 221–236.
Nishimune, A., Isaac, J. T., Molnar, E., et al. (1998) NSF binding to GluR2 regulates synaptic transmission. Neuron 21, 87–97.
Adesnik, H., Nicoll R. A., and England P. M. (2005) Photoinactivation of native AMPA receptors reveals their real-time trafficking. Neuron 48, 977–985.
Gomes A. R., Correia S. S., Carvalho A. L., and Duarte C. B. (2003) Regulation of AMPA receptor activity, synaptic targeting and recycling: role in synaptic plasticity. Neurochem. Res. 28, 1459–1473.
Palmer C. L., Cotton, L., and Henley J. M. (2005) The molecular pharmacology and cell biology of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors. Pharmacol. Rev. 57, 253–277.
Shi, S., Hayashi, Y., Esteban, J. A., and Malinow, R. (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105, 331–343.
Hayashi, Y., Shi, S. H., Esteban, J. A., Piccini, A., Poncer, J. C., and Malinow, R. (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287, 2262–2267.
Shi, S. H., Hayashi, Y., Petralia, R. S., et al. (1999) Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284, 1811–1816.
Lu, W., Man, H., Ju, W., Trimble, W. S., Mac-Donald, J. F., and Wang, Y. T. (2001) Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 29, 243–254.
Lee S. H., Liu L., Wang Y. T., and Sheng M. (2002) Clathrin adaptor AP2 and NSF interact with overlapping sites of GluR2 and play distinct roles in AMPA receptor trafficking and hippocampal LTD. Neuron 36, 661–674.
Brown T. C., Tran I. C., Backos D. S., and Esteban J. A. (2005) NMDA receptor-dependent activation of the small GTPase Rab5 drives the removal of synaptic AMPA receptors during hippocampal LTD. Neuron 45, 81–94.
Jia, Z., Agopyan, N., Miu, P., et al. (1996) Enhanced LTP in mice deficient in the AMPA receptor GluR2. Neuron 17, 945–956.
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.
Zamanillo D., Sprengel, R., Hvalby, O., et al. (1999) Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 284, 1805–1811.
Reisel, D., Bannerman, D. M., Schmitt, W. B., et al. (2002) Spatial memory dissociations in mice lacking GluR1. Nat. Neurosci. 5, 868–873.
Schmitt W. B., Deacon R. M., Seeburg P. H., Rawlins J. N., and Bannerman D. M. (2003) A within-subjects, within-task demonstration of intact spatial reference memory and impaired spatial working memory in glutamate receptor-A-deficient mice. J. Neurosci. 23, 3953–3959.
Schmitt, W. B., Sprengel, R., Mack, V., et al. (2005). Restoration of spatial working memory by genetic rescue of GluR-A-deficient mice. Nat. Neurosci. 8, 270–272.
Rumpel S., LeDoux J., Zador A., and Malinow R. (2005) Postsynaptic receptor trafficking underlying a form of associative learning. Science 308, 83–88.
Heynen, A. J., Yoon, B. J., Liu, C. H., Chung, H. J., Huganir, R. L., and Bear, M. F. (2003) Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation. Nat. Neurosci. 6, 854–862.
Takahashi, T., Svoboda K., and Malinow R. (2003) Experience strengthening transmission by driving AMPA receptors into synapses. Science 299, 1585–1588.
Schnell, E., Sizemore, M., Karimzadegan, S., Chen, L., Bredt, D. S., and Nicoll, R. A. (2002) Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor numben. Proc. Natl. Acad. Sci. USA 99, 13,902–13,907.
Nicoll R. A., Tomita S., and Bredt D. S. (2006) Auxiliary subunits assist AMPA-type glutamate receptors. Science 311, 1253–1256.
Chen, L., Chetkovich, D. M., Petralia, R. S., et al. (2000) Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408, 936–943.
Hashimoto, K., Fukaya, M., Qiao, X., Sakimura, K., Watanabe, M., and Kano, M. (1999) Impairment of AMPA receptor function in cerebellar granule cells of ataxic mutant mouse stargazer. J. Neurosci. 19, 6027–6036.
Rouach, N., Byrd, K., Petralia, R. S., et al. (2005) TARP gamma-8 controls hippocampal AMPA receptor number, distribution and synaptic plasticity. Nat. Neurosci. 8, 1525–1533.
Tomita S., Stein V., Stocker T. J., Nicoll R. A., and Bredt D. S. (2005) Bidirectional synaptic plasticity regulated by phosphorylation of stargazin-like TARPs. Neuron 45, 269–277.
Tomita S., Fukata M., Nicoll R. A., and Bredt D. S. (2004) Dynamic interaction of stargazinlike TARPs with cycling AMPA receptors at synapses. Science 303, 1508–1511.
Tomita, S., Adesnik, H., Sekiguchi, M., et al. (2005) Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature 435, 1052–1058.
Triller A. and Choquet D. (2003) Synaptic structure and diffusion dynamics of synaptic receptors. Biol. Cell. 95, 465–476.
Axelrod, D., Ravdin, P., Koppel, D. E., et al. (1976) Lateral motion of fluorescently labeled acetylcholine receptors in membranes of developing muscle fibers. Proc. Natl. Acad. Sci. USA 73, 4594–4598.
Blanpied T. A., Scott D. B., and Ehlers M. D. (2002) Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines. Neuron 36, 435–449.
Ashby, M. C., De La Rue, S. A., Ralph, G. S., Uney, J., Collingridge, G. L., and Henley, J. M. (2004) Removal of AMPA receptors (AMPARs) from synapses is preceded by transient endocytosis of extrasynaptic AMPARs. J. Neurosci. 24, 5172–5176.
Borgdorff A. J. and Choquet D. (2002) Regulation of AMPA receptor lateral movements. Nature 417, 649–653.
Tardin C., Cognet L., Bats C., Lounis B., and Choquet D. (2003) Direct imaging of lateral movements of AMPA receptors inside synapses. EMBO J. 22, 4656–4665.
Groc, L., Heine, M., Cognet, L., et al. (2004) Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors. Nat. Neurosci. 7, 695–696.
Hanley J. G., Khatri L., Hanson P. I., and Ziff E. B. (2002) NSF ATPase and alpha-/beta-SNAPs disassemble the AMPA receptor-PICK1 complex. Neuron 34, 53–67.
Braithwaite S. P., Xia H., and Malenka R. C. (2002) Differential roles for NSF and GRIP/ABP in AMPA receptor cycling. Proc. Natl. Acad. Sci. USA 99, 7096–7101.
Osten, P., Khatri, L., Perez, J. L., et al. (2000) Mutagenesis reveals a role for ABP/GRIP binding to GluR2 in synaptic surface accumulation of the AMPA receptor. Neuron 27, 313–325.
Dong, H., O'Brien, R. J., Fung, E. T., Lanahan, A. A., Worley, P. F., and Huganir, R. L. (1997) GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature 386, 279–284.
Hanley J. G. and Henley J. M. (2005) PICK1 is a calcium-sensor for NMDA-induced AMPA receptor trafficking. EMBO J. 24, 3266–3278.
Lu W. and Ziff E. B. (2005) PICK1 interacts with ABP/GRIP to regulate AMPA receptor trafficking. Neuron 47, 407–421.
Perez, J. L., Khatri, L., Chang, C., Srivastava, S., Osten, P., and Ziff, E. B. (2001) PICK1 targets activated protein kinase Calpha to AMPA receptor clusters in spines of hippocampal neurons and reduces surface levels of the AMPA-type glutamate receptor subunit 2. J. Neurosci. 21, 5417–5428.
Seidenman K. J., Steinberg J. P., Huganir R., and Malinow R. (2003) Glutamate receptor subunit 2 Serine 880 phosphorylation modulates synaptic transmission and mediates plasticity in CA1 pyramidal cells. J. Neurosci. 23, 9220–9228.
Chung H. J., Steinberg J. P., Huganir R. L., and Linden D. J. (2003) Requirement of AMPA receptor GluR2 phosphorylation for cerebellar long-term depression. Science 300, 1751–1755.
Chung H. J., Xia J., Scannevin R. H., Zhang, X., and Huganir R. L. (2000) Phosphorylation of the AMPA receptor subunit GluR2 differentially regulates its interaction with PDZ domain-containing proteins. J. Neurosci. 20, 7258–7267.
Hayashi T. and Huganir R. L. (2004) Tyrosine phosphorylation and regulation of the AMPA receptor by SRC family tyrosine kinases. J. Neurosci. 24, 6152–6160.
Leonard A. S., Davare M. A., Horne M. C., Garner C. C., and Hell J. W. (1998) SAP97 is associated with the alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor GluR1 subunit. J. Biol. Chem. 273, 19,518–19,524.
Valtschanoff, J. G., Burette, A., Davare, M. A., Leonard, A. S., Hell, J. W., and Weinberg, R. J. (2000) SAP97 concentrates at the postsynaptic density in cerebral cortex. Eur. J. Neurosci. 12, 3605–3614.
Gardoni, F., Mauceri, D., Fiorentini, C., et al. (2003) CaMKII-dependent phosphorylation regulates SAP97/NR2A interaction. J. Biol. Chem. 278, 44,745–44,752.
Jin W., Ge, W. P., Xu, J., et al (2006) Lipid binding regulates synaptic targeting of PICK1, AMPA receptor trafficking, and synaptic plasticity. J. Neurosci. 26, 2380–2390.
Rumbaugh, G., Sia, G. M., Garner, C. C., and Huganir, R. L. (2003) Synapse-associated protein-97 isoform-specific regulation of surface AMPA receptors and synaptic function in cultured neurons. J. Neurosci. 23, 4567–4576.
Cai C., Li H., Rivera C. and Keinanen K. (2006) Interaction between SAP97 and PSD-95, two Maguk proteins involved in synaptic trafficking of AMPA receptors. J. Biol. Chem. 281, 4267–4273.
Mauceri D., Cattabeni F. Di Luca M., and Gardoni F. (2004) Calcium/calmodulin-dependent protein kinase II phosphorylation drives synapse-associated protein 97 into spines. J. Biol. Chem. 279, 23,813–23,821.
Nakagawa, T., Futai, K., Lashuel, H. A., et al. (2004) Quaternary structure protein dynamics, and synaptic function of SAP97 controlled by L27 domain interactions. Neuron 44, 453–467.
Kim, C. H., Takamiya, K., Petralia, R. S., et al. (2005). Persistent hippocampal CA1 LTP in mice lacking the C-terminal PDZ ligand of GluR1. Nat. Neurosci. 8, 985–987.
Ehrlich I. and Malinow R. (2004) Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity. J. Neurosci. 24, 916–927.
Tovar K. R. and Westbrook G. L. (1999) The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J. Neurosci. 19, 4180–4188.
Kew J. N., Richards J. G., Mutel, V., and Kemp J. A. (1998) Developmental changes in NMDA receptor glycine affinity and ifenprodil sensitivity reveal three distinct populations of NMDA receptors in individual rat cortical neurons J. Neurosci. 18, 1935–1943.
Rumbaugh G. and Vicini S. (1999) Distinct synaptic and extrasynaptic NMDA receptors in developing cerebellar granule neurons. J. Neurosci. 19, 10,603–10,610.
Vicini, S., Wang, J. F., Li, J. H., et al. (1998). Functional and pharmacological differences between recombinant N-methyl-d-aspartate receptors. J. Neurophysiol. 79, 555–566.
Carroll, R. C. and Zukin, R. S. (2002) NMDA-receptor trafficking and targeting: implications for synaptic transmission and plasticity. Trends Neurosci. 25, 571–577.
Nong Y., Huang Y. Q., and Salter M. W. (2004) NMDA receptors are movin' in. Curr. Opin. Neurobiol. 14, 353–361.
Perez-Otano I. and Ehlers M. D. (2005) Homeostatic plasticity and NMDA receptor trafficking Trends Neurosci. 28, 229–238.
Wenthold R. J., Prybylowski, K., Standley, S., Sans N. and Petralia R. S. (2003) Trafficking of NMDA receptors, Annu. Rev. Pharmacol. Toxicol. 43, 335–358.
Roche, K. W., Standley, S., McCallum, J., Dune Ly C., Ehlers, M. D., and Wenthold, R. J. (2001) Molecular determinants of NMDA receptor internalization. Nat. Neurosci. 4, 794–802.
Sharma K., Fong D. K., and Craig A. M. (2006) Postsynaptic protein mobility in dendritic spines: long-term regulation by synaptic NMDA receptor activation. Mol. Cell Neurosci. 31 702–712.
Nong, Y., Huang, Y. Q., Ju, W., et al. (2003) Glycine binding primes NMDA receptor internalization. Nature 422, 302–307.
Grosshans, D. R., Clayton, D. A., Coultrap, S. I., and Browning M. D. (2002) LTP leads to rapid surface expression of NMDA but not AMPA receptors in adult, rat CA1. Nat. Neurosci. 5, 27–33.
Quinlan E. M., Philpot, B. D., Huganir R. L., and Bear M. F. (1999) Rapid, experience dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat. Neurosci 2, 352–357.
Scott D. B., Blanpied T. A., Swanson, G. T., Zhang, C., and Ehlers M. D. (2001) An NMDA receptor ER retention signal regulated by phosphorylation and alternative splicing. J. Neurosci. 21, 3063–3072.
Mu Y., Otsuka T., Horton A. C., Scott D. B., and Ehlers M. D. (2003) Activity-dependent mRNA splicing controls ER export and synaptic delivery of NMDA receptors. Neuron 40, 581–594.
Standley, S., Roche, K. W., McCallum, J., Sans N., and Wenthold R. J. (2000) PDZ domain suppression of an ER retention signal in NMDA receptor NR1 splice variants. Neuron 28, 887–898.
Xia H., Hornby Z. D., and Malenka, R. C. (2001) An ER retention signal explains differences in surface expression of NMDA and AMPA receptor subunits. Neuropharmacology 41, 714–723.
Scott D. B., Blanpied T. A., and Ehlers M. D. (2003) Coordinated PKA and PKC phosphorylation suppresses RXR-mediated ER retention and regulates the surface delivery of NMDA receptors. Neuropharmacology 45, 755–767.
Kim C. H., Chung H. J., Lee H. K., and Huganir, R. L. (2001) Interaction of the AMPA receptor subunit GluR2/3 with PDZ domains regulates hippocampal long-term depression. Proc. Natl. Acad. Sci. USA 98, 11,725–11,730.
Connolly, C. N., Kittler, J. T., Thomas, P., et al. (1999) Cell surface stability of gamma-aminobutyric acid type A receptors. Dependence on protein kinase C activity and subunit composition. J. Biol. Chem. 274, 36,565–36,572.
Lan, J. Y., Skeberdis, V. A., Jover, T., et al. (2001) Protein kinase C modulates NMDA receptor trafficking and gating. Nat. Neurosci. 4, 382–390.
Scott D. B., Michailidis I., Mu Y., Logothetis D., and Ehlers M. D. (2004) Endocytosis and degradative sorting of NMDA receptors by conserved membrane-proximal signals. J. Neurosci. 24, 7096–7109.
Sans, N., Prybylowski, K., Petralia, R. S. et al. (2003) NMDA receptor trafficking through an interaction between PDZ proteins and the exocyst complex. Nat. Cell. Biol. 5, 520–530.
Lau, L. F., Mammen, A., Ehlers, M. D., et al. (1996) Interaction of the N-methyl-d-aspartate receptor complex with a novel synapse associated protein, SAP102. J. Biol. Chem. 271, 21,622–21,628.
Muller, B. M., Kistner, U., Kindler, S., et al. (1996) SAP102, a novel postsynaptic protein that interacts with NMDA receptor complexes in vivo. Neuron 17, 255–265.
Sans, N., Wang, P. Y., Du, Q., et al. (2005) mPins modulates PSD-95 and SAP102 trafficking and influences NMDA receptor surface expression. Nat. Cell. Biol. 7, 1079–1090.
Barria A. and Malinow R. (2002) Subunit-specific NMDA receptor trafficking to synapses. Neuron 35, 345–353.
Chung H. J., Huang Y. H., Lau L. F., and Huganir R. L. (2004) Regulation of the NMDA receptor complex and trafficking by activity-dependent phosphorylation of the NR2B subunit PDZ ligand. J. Neurosci. 24, 10,248–10,259.
Washbourne P., Liu X. B., Jones E. G., and McAllister A. K. (2004) Cycling of NMDA receptors during trafficking in neurons before synapse formation. J. Neurosci. 24, 8253–8264.
Migaud, M., Charlesworth, P., Dempster, M., et al. (1998) Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 396, 433–439.
Lavezzari G., McCallum J., Lee R., and Roche K. W. (2003) Differential binding of the AP-2 adaptor complex and PSD-95 to the C-terminus of the NMDA receptor subunit NR2B regulates surface expression. Neuropharmacology 45, 729–737.
Prybylowski, K., Chang, K., Sans, N., Kan L., Vicini, S., and Wenthold, R. J. (2005) The synaptic localization of NR2B-containing NMDA receptors is controlled by interactions with PDZ proteins and AP-2. Neuron 47 845–857.
Lavezzari G., McCallum J., Dewey C. M., and Roche K. W. (2004) Subunit-specific regulation of NMDA receptor endocytosis. J. Neurosci. 24, 6383–6391.
Snyder, E. M., Philpot, B. D., Huber, K. M., Dong, X., Fallon, J. R., and Bear, M. F. (2001) Internalization of ionotropic glutamate receptors in response to mGluR activation. Nat. Neurosci. 4, 1079–1085.
Tovar K. R. and Westbrook G. L. (2002) Mobile NMDA receptors at hippocampal synapses. Neuron 34, 255–264.
Rabow L. E., Russek S. J., and Farb D. H. (1995) From ion currents to genomic analysis recent advances in GABAA receptor research. Synapse 21, 189–274.
Sieghart W. and Sperk G. (2002) Subunit composition, distribution and function of GABA(A) receptor subtypes. Curr. Top Med. Chem. 2 795–816.
Luscher B. and Keller C. A. (2004) Regulation of GABAA receptor trafficking, channel activity, and functional plasticity of inhibitory synapses. Pharmacol. Ther. 102, 195–221.
Hanus C., Vannier C., and Triller A. (2004) Intracellular association of glycine receptor with gephyrin increases its plasma membrane accumulation rate. J. Neurosci. 24, 1119–1128.
Wang H., Bedford F. K., Brandon N. J., Moss S. J., and Olsen R. W. (1999) GABA(A)-receptor-associated protein links GABA(A) receptors and the cytoskeleton. Nature 397 69–72.
Wan, Q., Xiong, Z. G., Man, H. Y., et al. (1997) Recruitment of functional GABA(A) receptors to postsynaptic domains by insulin. Nature 388, 686–690.
Kumar S., Kralic J. E., O'Buckley T. K., Grobin A. C., and Morrow A. L. (2003) Chronic ethanol consumption enhances internalization of alphal subunit-containing GABAA receptors in cerebral cortex. J. Neurochem. 86, 700–708.
Kneussel M. (2002) Dynamic regulation of GABA(A) receptors at synaptic sites. Brain. Res. Rev. 39, 74–83.
Borden L. A., Czajkowski C., Chan C. Y., and Farb D. H. (1984) Benzodiazepine receptor synthesis and degradation by neurons in culture. Science 226, 857–860.
Kittler, J. T., Chen, G., Honing, S., et al. (2005) Phospho-dependent binding of the clathrin AP2 adaptor complex to GABAA receptors regulates the efficacy of inhibitory synaptic transmission. Proc. Natl. Acad. Sci. USA 102, 14,871–14,876.
Kittler, J. T., Rostaing, P., Schiavo, et al. (2001) The subcellular distribution of GABARAP and its ability to interact with NSF suggest a role for this protein in the intracellular transport of GABA(A) receptors. Mol. Cell Neurosci. 18, 13–25.
Herring, D., Huang, R., Singh, M., Robinson, L. C., Dillon, G. H., and Leidenheimer, N. J. (2003) Constitutive GABAA receptor endocytosis is dynamin-mediated and dependent on a difeucine AP2 adaptin-binding motif within the beta 2 subunit of the receptor. J. Biol. Chem. 278, 24,046–24,052.
Connolly, C. N., Uren, J. M., Thomas, P., et al. (1999) Subcellular localization and endocytosis of homomeric gamma2 subunit splice variants of gamma-aminobutyric acid type A receptors. Mol. Cell Neurosci. 13, 259–271.
Barnes E. M. Jr. (2000) Intracellular trafficking of GABA(A) receptors. Life Sci. 66, 1063–1070.
Bedford, F. K., Kittler, J. T., Muller, E., et al. (2001) GABA(A) receptor cell surface number and subunit stability are regulated by the ubuquitin-like protein Plic-1. Nat. Neurosci. 4, 908–916.
Goto, H., Terunuma, M., Kanematsu, T., Misumi, Y., Moss, S. J., and Hirata, M. (2005) Direct interaction of N-ethylmaleimide-sensitive factor with GABA(A) receptor beta subunits. Mol. Cell Neurosci. 30, 197–206.
Kittler, J. T., Arancibia-Carcamo I. L., and Moss S. J. (2004) Association of GRIP1 with a GABA(A) receptor associated protein suggests a role for GRIP1 at inhibitory synapses. Biochem. Pharmacol. 68, 1649–1654.
Knuesel, I., Mastrocola, M., Zuellig, R. A., Bornhauser, B., Schaub, M. C., and Fritschy, J. M. (1999) Short communication: altered synaptic clustering of GABAA receptors in mice lacking dystrophin (mdx mice). Eur. J. Neurosci. 11 4457–4462.
Mishina, M., Takai, T., Imoto, K., et al. (1986) Molecular distinction between fetal and adult forms of muscle acetylcholine receptor. Nature 321, 406–411.
Gu Y. and Hall Z. W. (1988) Immunological evidence for a change in subunits of the acetylcholine receptor in developing and denervated rat muscle. Neuron 1, 117–125.
Missias A. C., Chu, G. C., Klocke, B. J., Sanes J. R., and Merlie J. P. (1996) Maturation of the acetylcholine receptor in skeletal muscle: regulation of the AChR gamma-to-epsilon switch. Dev. Biol. 179, 223–238.
Salpeter M. M. and Loring R. H. (1985) Nicotinic acetylcholine receptors in vertebrate muscle: properties, distribution and neural control. Prog. Neurobiol. 25, 297–325.
Bevan S. and Steinbach J. H. (1983) Denervation increases the degradation rate of acetylcholine receptors at end-plates in vivo and in vitro. J. Physiol. 336, 159–177.
Stanley E. F. and Drachman D. B. (1983) Rapid degradation of “new” acetylcholine receptors at neuromuscular junctions. Science 222, 67–69.
Green D. P., Miledi R., Perez de la Mora M., and Vincent A. (1975) Acetylcholine receptors. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 270, 551–559.
Fambrough D. M. (1979) Control of acetylcholine receptors in skeletal muscle. Physiol. Rev. 59, 165–227.
Akaaboune M., Culican S. M., Turney S. G. and Lichtman J. W. (1999) Rapid and reversible effects of activity on acetylcholine receptor density at the neuromuscular junction in vivo. Science 286, 503–507.
Gardner J. M. and Fambrough D. M. (1979) Acetylcholine receptor degradation, measured by density labeling: effects of cholinergic ligands and evidence against recycling. Cell 16, 661–674.
Bruneau E., Sutter D., Hume R. I., and Akaaboune M. (2005) Identification of nicotinic acetylcholine receptor recycling and its role in maintaining receptor density at the neuromuscular junction in vivo. J. Neurosci. 25, 9949–9959.
Akaaboune M., Grady R. M., Turney S., Sanes J. R., and Lichtman J. W. (2002) Neurotransmitter receptor dynamics studied in vivo by reversible photo-unbinding of fluorescent ligands. Neuron 34, 865–876.
Andreose J. S., Xu R., Lomo T., Salpeter M. M., and Fumagalli G. (1993) Degradation of two AChR populations at rat neuromuscular junctions: regulation in vivo by electrical stimulation. J. Neurosci. 13, 3433–3438.
Caroni P., Rotzler S., Britt J. C., and Brenner H. R. (1993) Calcium influx and protein phosphorylation mediate the metabolic stabilization of synaptic acetylcholine receptors in muscle. J. Neurosci. 13, 1315–1325.
Bruneau E. G., Macpherson P. C., Goldman D., Hume R. I., and Akaaboune M. (2005) The effect of agrin and laminin on acetylcholine receptor dynamics in vitro. Dev. Biol. 288, 248–258.
Shyng S. L. and Salpeter M. M. (1989) Degradation rate of acetylcholine receptors inserted into denervated vertebrate neuromuscular junctions. J. Cell. Biol. 108, 647–651.
Rotzler S., Schramek H., and Brenner H. R. (1991) Metabolic stabilization of endplate acetylcholine receptors regulated by Ca2+ influx associated with muscle activity. Nature 349, 337–339.
Rotzler S. and Brenner H. R. (1990) Metabolic stabilization of acetylcholine receptors in vertebrate neuromuscular junction by muscle activity. J. Cell Biol. 111, 655–661.
Bezakova G., Rabben I., Sefland I., Fumagalli G., and Lomo T. (2001) Neural agrin controls acetylcholine receptor stability in skeletal muscle fibers. Proc. Natl. Acad. Sci. USA 98, 9924–9929.
Adams, M. E., Kramarcy, N., Krall, S. P., et al. (2000) Absence of alpha-syntrophin leads to structurally aberrant neuromuscular synapses deficient in utrophin. J. Cell Biol. 150, 1385–1398.
Gervasio O. L. and Phillips W. D. (2005) Increased ratio of rapsyn to ACh receptor stabilizes postsynaptic receptors at the mouse neuromuscular synapse. J. Physiol. 562, 673–685.
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Bruneau, E.G., Akaaboune, M. Running to stand still. Mol Neurobiol 34, 137–151 (2006). https://doi.org/10.1385/MN:34:2:137
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DOI: https://doi.org/10.1385/MN:34:2:137