The Library

Differential localization of glutamate receptor subunits at the drosophila neuromuscular junction

Tools

Marrus, Scott B., Portman, Scott L., Allen, Marcus James, 1970-, Moffat, Kevin G. and DiAntonio, Aaron. (2004) Differential localization of glutamate receptor subunits at the drosophila neuromuscular junction. Journal of Neuroscience, Vol.24 (No.6). pp. 1406-1415. ISSN 0270-6474

PDF
WRAP_Moffatt_Differential_localization.pdf - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader
Download (772Kb)

Official URL: http://dx.doi.org/10.1523/JNEUROSCI.1575-03.2004

Abstract

The subunit composition of postsynaptic neurotransmitter receptors is a key determinant of synaptic physiology. Two glutamate receptor subunits, Drosophila glutamate receptor IIA (DGluRIIA) and DGluRIIB, are expressed at the Drosophila neuromuscular junction and are redundant for viability, yet differ in their physiological properties. We now identify a third glutamate receptor subunit at the Drosophila neuromuscular junction, DGluRIII, which is essential for viability. DGluRIII is required for the synaptic localization of DGluRIIA and DGluRIIB and for synaptic transmission. Either DGluRIIA or DGluRIIB, but not both, is required for the synaptic localization of DGluRIII. DGluRIIA and DGluRIIB compete with each other for access to DGluRIII and subsequent localization to the synapse. These results are consistent with a model of a multimeric receptor in which DGluRIII is an essential component. At single postsynaptic cells that receive innervation from multiple motoneurons, DGluRIII is abundant at all synapses. However, DGluRIIA and DGluRIIB are differentially localized at the postsynaptic density opposite distinct motoneurons. Hence, innervating motoneurons may regulate the subunit composition of their receptor fields within a shared postsynaptic cell. The capacity of presynaptic inputs to shape the subunit composition of postsynaptic receptors could be an important mechanism for synapse-specific regulation of synaptic function and plasticity.

Item Type:	Journal Article
Subjects:	Q Science > QL Zoology R Medicine > RC Internal medicine > RC0321 Neuroscience. Biological psychiatry. Neuropsychiatry
Divisions:	Faculty of Science > Life Sciences (2010- ) > Biological Sciences ( -2010)
Library of Congress Subject Headings (LCSH):	Drosophila -- Genetics, Glutamic acid, Neuromuscular transmission, Neural transmission -- Regulation
Journal or Publication Title:	Journal of Neuroscience
Publisher:	Society for Neuroscience
ISSN:	0270-6474
Date:	11 February 2004
Volume:	Vol.24
Number:	No.6
Page Range:	pp. 1406-1415
Identification Number:	10.1523/JNEUROSCI.1575-03.2004
Status:	Peer Reviewed
Access rights to Published version:	Open Access
Funder:	National Institutes of Health (U.S.) (NIH), National Research Service Award Training Grant (NRSATG), W. M. Keck Foundation, McKnight Foundation (MF), Howard Hughes Medical Institute, Burroughs Wellcome Fund (BWF), Alfred P. Sloan Foundation
Grant number:	RO1 NS043171 (NIH), NS44754-01 (NRSATG)
References:	Atwood HL, Govind CK, Wu CF (1993) Differential ultrastructure of synaptic terminals on ventral longitudinal abdominal muscles in Drosophila larvae. J Neurobiol 24:1008–1024. Ayalon G, Stern-Bach Y (2001) Functional assembly of AMPA and kainate receptors is mediated by several discrete protein-protein interactions. Neuron 31:103–113. Barry MF, Ziff EB (2002) Receptor trafficking and the plasticity of excitatory synapses. Curr Opin Neurobiol 12:279–286. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–415. Craig AM, Boudin H (2001) Molecular heterogeneity of central synapses: afferent and target regulation. Nat Neurosci 4:569–578. Craig AM, Blackstone CD, Huganir RL, Banker G (1994) Selective clustering of glutamate and gamma-aminobutyric acid receptors opposite terminals releasing the corresponding neurotransmitters. Proc Natl Acad Sci USA 91:12373–12377. Davis GW, DiAntonio A, Petersen SA, Goodman CS (1998) Postsynaptic PKA controls quantal size and reveals a retrograde signal that regulates presynaptic transmitter release in Drosophila. Neuron 20:305–315. DiAntonio A, Petersen SA, Heckmann M, Goodman CS (1999) Glutamate receptor expression regulates quantal size and quantal content at the Drosophila neuromuscular junction. J Neurosci 19:3023–3032. Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7–61. Hoang B, Chiba A (2001) Single-cell analysis of Drosophila larval neuromuscular synapses. Dev Biol 229:55–70. Hollmann M, Heinemann S (1994) Cloned glutamate receptors. Annu Rev Neurosci 17:31–108. Hung AY, Sheng M (2002) PDZ domains: structural modules for protein complex assembly. J Biol Chem 277:5699–5702. Jia XX, Gorczyca M, Budnik V (1993) Ultrastructure of neuromuscular junctions in Drosophila: comparison of wild type and mutants with increased excitability. J Neurobiol [Erratum (1994) 25:893–895] 24:1025–1044. Johansen J, Halpern ME, Johansen KM, Keshishian H (1989) Stereotypic morphology of glutamatergic synapses on identified muscle cells of Drosophila larvae. J Neurosci 9:710–725. Jonas P, Racca C, Sakmann B, Seeburg PH, Monyer H (1994) Differences in Ca2 permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression. Neuron 12:1281–1289. Karunanithi S, Marin L, Wong K, Atwood HL (2002) Quantal size and variation determined by vesicle size in normal and mutant Drosophila glutamatergic synapses. J Neurosci 22:10267–10276. Kawakami R, Shinohara Y, Kato Y, Sugiyama H, Shigemoto R, Ito I (2003) Asymmetrical allocation of NMDA receptor epsilon2 subunits in hippocampal circuitry. Science 300:990–994. Kurdyak P, Atwood HL, Stewart BA, Wu CF (1994) Differential physiology and morphology of motor axons to ventral longitudinal muscles in larval Drosophila. J Comp Neurol 350:463–472. Littleton JT, Ganetzky B (2000) Ion channels and synaptic organization: analysis of the Drosophila genome. Neuron 26:35–43. Lnenicka GA, Keshishian H (2000) Identified motor terminals in Drosophila larvae show distinct differences in morphology and physiology. J Neurobiol 43:186–197. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103–126. McGee AW, Bredt DS (2003) Assembly and plasticity of the glutamatergic postsynaptic specialization. Curr Opin Neurobiol 13:111–118. Petersen SA, Fetter RD, Noordermeer JN, Goodman CS, DiAntonio A (1997) Genetic analysis of glutamate receptors in Drosophila reveals a retrograde signal regulating presynaptic transmitter release. Neuron 19:1237–1248. Schuster CM, Ultsch A, Schloss P, Cox JA, Schmitt B, Betz H (1991) Molecular cloning of an invertebrate glutamate receptor subunit expressed in Drosophila muscle. Science 254:112–114. Schuster CM, Davis GW, Fetter RD, Goodman CS (1996) Genetic dissection of structural and functional components of synaptic plasticity. I. Fasciclin II controls synaptic stabilization and growth. Neuron 17:641–654. Sheng M, Pak DT (1999) Glutamate receptor anchoring proteins and the molecular organization of excitatory synapses. Ann NY Acad Sci 868:483–493. Sigrist SJ, Thiel PR, Reiff DF, Schuster CM (2002) The postsynaptic glutamate receptor subunit DGluR-IIA mediates long-term plasticity in Drosophila. J Neurosci 22:7362–7372. Sigrist SJ, Reiff DF, Thiel PR, Steinert JR, Schuster CM (2003) Experiencedependent strengthening of Drosophila neuromuscular junctions. J Neurosci 23:6546–6556. Sone M, Suzuki E, Hoshino M, Hou D, Kuromi H, Fukata M, Kuroda S, Kaibuchi K, Nabeshima Y, Hama C (2000) Synaptic development is controlled in the periactive zones of Drosophila synapses. Development 127:4157–4168. Stewart BA, Atwood HL, Renger JJ, Wang J, Wu CF (1994) Improved stability of Drosophila larval neuromuscular preparations in haemolymphlike physiological solutions. J Comp Physiol [A] 175:179–191. Tautz D, Pfeifle C (1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98:81–85. Toth K, McBain CJ (1998) Afferent-specific innervation of two distinct AMPA receptor subtypes on single hippocampal interneurons. Nat Neurosci 1:572–578. Toth K, McBain CJ (2000) Target-specific expression of pre- and postsynaptic mechanisms. J Physiol (Lond) 525:41–51. Ultsch A, Schuster CM, Laube B, Schloss P, Schmitt B, Betz H (1992) Glutamate receptors of Drosophila melanogaster: cloning of a kainateselective subunit expressed in the central nervous system. Proc Natl Acad Sci USA 89:10484–10488. Ultsch A, Schuster CM, Laube B, Betz H, Schmitt B (1993) Glutamate receptors of Drosophila melanogaster. Primary structure of a putative NMDA receptor protein expressed in the head of the adult fly. FEBS Lett 324:171–177. Ve`olkner M, Lenz-Be`ohme B, Betz H, Schmitt B (2000) Novel CNS glutamate receptor subunit genes of Drosophila melanogaster. J Neurochem 75:1791–1799. Wan HI, DiAntonio A, Fetter RD, Bergstrom K, Strauss R, Goodman CS (2000) Highwire regulates synaptic growth in Drosophila. Neuron 26:313–329. 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. Westbrook GL (1994) Glutamate receptor update. Curr Opin Neurobiol 4:337–346. Zito K, Parnas D, Fetter RD, Isacoff EY, Goodman CS (1999) Watching a synapse grow: noninvasive confocal imaging of synaptic growth in Drosophila. Neuron 22:719–729.
URI:	http://wrap.warwick.ac.uk/id/eprint/2678