Glutamate receptors localize postsynaptically at neuromuscular junctions in mice

Muscle and Nerve

Volumn 39, Issue 3, 2009, Pages 343-349

  Mays, Tessily A ^a   Sanford, Jamie L ^a   Hanada, Toshihiko ^b   Chishti, Athar H ^b   Rafael Fortney, Jill A ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

Author keywords

AMPA; Dlg SAP97; Kir2; Neuromuscular junction; NMDA

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN; PROTEIN DIG; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; MOUSE; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; TISSUE DISTRIBUTION;

ANIMALS; BUNGAROTOXINS; GLUTAMIC ACID; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; NERVE TISSUE PROTEINS; NEUROMUSCULAR JUNCTION; POTASSIUM CHANNELS; RECEPTORS, GLUTAMATE; SODIUM CHANNELS; SYNAPTIC MEMBRANES; SYNAPTOPHYSIN;

EID: 62849098741     PISSN: 0148639X     EISSN: 10974598     Source Type: Journal    
DOI: 10.1002/mus.21099     Document Type: Article

References (41)

1. Bassand P, Bernard A, Rafiki A, Gayet D, Khrestchatisky M. Differential interaction of the tSXV motifs of the NR1 and NR2A NMDA receptor subunits with PSD-95 and SAP97. Eur J Neurosci 1999;11:2031-2043.
2. Berger UV, Carter RE, Coyle JT. The immunocytochemical localization of N-acetylaspartyl glutamate, its hydrolysing enzyme NAALADase, and the NMDAR-1 receptor at a vertebrate neuromuscular junction. Neuroscience 1995;64:847-850.
3. Borodinsky LN, Spitzer NC. Activity-dependent neurotransmitter-receptor matching at the neuromuscular junction. Proc Natl Acad Sci U S A 2007;104:335-340.
4. Brunelli G, Spano P, Barlati S, Guarneri B, Barbon A, Bresciani R, et al. Glutamatergic reinnervation through peripheral nerve graft dictates assembly of glutamatergic synapses at rat skeletal muscle. Proc Natl Acad Sci U S A 2005;102:8752-8757.
5. Budnik V, Koh Y, Guan B, Hartmann B, Hough C, Woods D, et al. Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg. Neuron 1996;17:627-640.
6. Cai C, Coleman SK, Niemi K, Keinanen K. Selective binding of synapse-associated protein 97 to GluR-A alpha-amino-5-hydroxy-3-methyl-4- isoxazole propionate receptor subunit is determined by a novel sequence motif. J Biol Chem 2002;277:31484-31490.
7. Caruana G, Bernstein A. Craniofacial dysmorphogenesis including cleft palate in mice with an insertional mutation in the discs large gene. Mol Cell Biol 2001;21:1475-1483.
8. Chen K, Featherstone DE. Discs-large (DLG) is clustered by presynaptic innervation and regulates postsynaptic glutamate receptor subunit composition in Drosophila. BMC Biol 2005;3:1.
9. Feldmeyer D, Kask K, Brusa R, Kornau HC, Kolhekar R, Rozov A, et al. Neurological dysfunctions in mice expressing different levels of the Q/R site-unedited AMPAR subunit GluR-B. Nat Neurosci 1999;2:57-64.
10. Flucher BE, Daniels MP. Distribution of Na+ channels and ankyrin in neuromuscular junctions is complementary to that of acetylcholine receptors and the 43 kd protein. Neuron 1989;3:163-175.
11. Garcia RA, Vasudevan K, Buonanno A. The neuregulin receptor ErbB-4 interacts with PDZ-containing proteins at neuronal synapses. Proc Natl Acad Sci U S A 2000;97:3596-3601.
12. Gardoni F, Mauceri D, Fiorentini C, Bellone C, Missale C, Cattabeni F, et al. CaMKII-dependent phosphorylation regulates SAP97/NR2A interaction. J Biol Chem 2003;278:44745-44752.
13. Grozdanovic Z, Gossrau R. Co-localization of nitric oxide synthase I (NOS I) and NMDA receptor subunit 1 (NMDAR-1) at the neuromuscular junction in rat and mouse skeletal muscle. Cell Tissue Res 1998;291:57-63.
14. Huang YZ, Wang Q, Won S, Luo ZG, Xiong WC, Mei L. Compartmentalized NRG signaling and PDZ domain-containing proteins in synapse structure and function. Int J Dev Neurosci 2002;20:173-185.
15. Koyuncuoglu H, Kara I, Gunel MA, Nurten A, Yamanturk P. N-methyl-D-aspartate antagonists, glutamate release inhibitors, 4-aminopyridine at neuromuscular transmission. Pharmacol Res 1998;37:485-491.
16. Kummer TT, Misgeld T, Sanes JR. Assembly of the postsynaptic membrane at the neuromuscular junction: paradigm lost. Curr Opin Neurobiol 2006;16:74-82.
17. Kuner R, Groom AJ, Bresink I, Kornau HC, Stefovska V, Muller G, et al. Late-onset motoneuron disease caused by a functionally modified AMPA receptor subunit. Proc Natl Acad Sci U S A 2005;102:5826-5831.
18. Lai KO, Ip NY. Postsynaptic signaling of new players at the neuromuscular junction. J Neurocytol 2003;32:727-741.
19. Leonoudakis D, Conti LR, Anderson S, Radeke CM, McGuire LM, Adams ME, et al. Protein trafficking and anchoring complexes revealed by proteomic analysis of inward rectifier potassium channel (Kir2.x)-associated proteins. J Biol Chem 2004;279:22331-22346.
20. Leonoudakis D, Conti LR, Radeke CM, McGuire LM, Vandenberg CA. A multiprotein trafficking complex composed of SAP97, CASK, Veli, and Mint1 is associated with inward rectifier Kir2 potassium channels. J Biol Chem 2004;279:19051-19063.
21. Leonoudakis D, Mailliard W, Wingerd K, Clegg D, Vandenberg C. Inward rectifier potassium channel Kir2.2 is associated with synapse-associated protein SAP97. J Cell Sci 2001;114:987-998.
22. Lin L, Sahr K, Chishti A. Identification of the mouse homologue of human discs large and rat SAP97 genes. Biochim Biophys Acta 1997;1362:1-5.
23. Luck G, Hoch W, Hopf C, Blottner D. Nitric oxide synthase (NOS-1) coclustered with agrin-induced AChR-specializations on cultured skeletal myotubes. Mol Cell Neurosci 2000;16:269-281.
24. Lue R, Marfatia S, Branton D, Chishti A. Cloning and characterization of hdlg: the human homologue of the Drosophila discs large tumor suppressor binds to protein 4.1. Proc Natl Acad Sci U S A 1994;91:9818-9822.
25. Malomouzh AI, Nikolsky EE, Lieberman EM, Sherman JA, Lubischer JL, Grossfeld RM, et al. Effect of N-acetylaspartyl-glutamate (NAAG) on non-quantal and spontaneous quantal release of acetylcholine at the neuromuscular synapse of rat. J Neurochem 2005;94:257-267.
26. Meng Y, Zhang Y, Jia Z. Synaptic transmission and plasticity in the absence of AMPA glutamate receptor GluR2 and GluR3. Neuron 2003;39:163-176.
27. Muller B, Kistner U, Veh R, Cases-Langhoff C, Becker B, Gundelfinger E, et al. Molecular characterization and spatial distribution of SAP97, a novel presynaptic protein homologous to SAP90 and the Drosophila discs-large tumor suppressor protein. J Neuroscience 1995;15:2354-2366.
28. Nakagawa T, Futai K, Lashuel HA, Lo I, Okamoto K, Walz T, et al. Quaternary structure, protein dynamics, and synaptic function of SAP97 controlled by L27 domain interactions. Neuron 2004;44:453-467.
29. Plaster NM, Tawil R, Tristani-Firouzi M, Canun S, Bendahhou S, Tsunoda A, et al. Mutations in Kir2.1 cause the developmental and episodic electrical phenotypes of Andersen's syndrome. Cell 2001;105:511-519.
30. Rafael JA, Brown SC. Dystrophin and utrophin: genetic analyses of their role in skeletal muscle. Microsc Res Tech 2000;48:155-166.
31. Regalado MP, Terry-Lorenzo RT, Waites CL, Garner CC, Malenka RC. Transsynaptic signaling by postsynaptic synapse-associated protein 97. J Neurosci 2006;26:2343-2357.
32. Rinholm JE, Slettalokken G, Marcaggi P, Skare O, Storm-Mathisen J, Bergersen LH. Subcellular localization of the glutamate transporters GLAST and GLT at the neuromuscular junction in rodents. Neuroscience 2007;145:579-591.
33. Rumbaugh G, Sia GM, Garner CC, Huganir RL. Synapse-associated protein-97 isoform-specific regulation of surface AMPA receptors and synaptic function in cultured neurons. J Neurosci 2003;23:4567-4576.
34. Sanes JR, Lichtman JW. Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 1999;22:389-442.
35. Sanford JL, Mays TA, Rafael-Fortney JA. CASK and Dlg form a PDZ protein complex at the mammalian neuromuscular junction. Muscle Nerve 2004;30:164-171.
36. Sans N, Racca C, Petralia RS, Wang YX, McCallum J, Wenthold RJ. Synapse-associated protein 97 selectively associates with a subset of AMPA receptors early in their biosynthetic pathway. J Neurosci 2001;21:7506-7516.
37. Schluter OM, Xu W, Malenka RC. Alternative N-terminal domains of PSD-95 and SAP97 govern activity-dependent regulation of synaptic AMPA receptor function. Neuron 2006;51:99-111.
38. Single FN, Rozov A, Burnashev N, Zimmermann F, Hanley DF, Forrest D, et al. Dysfunctions in mice by NMDA receptor point mutations NR1(N598Q) and NR1(N598R). J Neurosci 2000;20:2558-2566.
39. Tiffany AM, Manganas LN, Kim E, Hsueh YP, Sheng M, Trimmer JS. PSD-95 and SAP97 exhibit distinct mechanisms for regulating K(+) channel surface expression and clustering. J Cell Biol 2000;148:147-158.
40. Trinidad JC, Fischbach GD, Cohen JB. The Agrin/MuSK signaling pathway is spatially segregated from the neuregulin/ErbB receptor signaling pathway at the neuromuscular junction. J Neurosci 2000;20:8762-8770.
41. Zaritsky JJ, Eckman DM, Wellman GC, Nelson MT, Schwarz TL. Targeted disruption of Kir2.1 and Kir2.2 genes reveals the essential role of the inwardly rectifying K(+) current in K(+)-mediated vasodilation. Circ Res 2000;87:160-166.