Essential role for dlg in synaptic clustering of Shaker K+ channels in vivo

Journal of Neuroscience

Volumn 17, Issue 1, 1997, Pages 152-159

  Tejedor, Francisco J ^b   Bokhari, Amr ^a   Rogero, Oscar ^b   Gorczyca, Michael ^a   Zhang, Jiangwen ^a   Kim, Eunjoon ^c   Sheng, Morgan ^c   Budnik, Vivian ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b UNIVERSITY OF ALICANTE   (Spain)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

discs large; Drosophila; glutamatergic synapse; I(A); ion channel clustering; MAGUK; neuromuscular junction; PDZ; potassium channels; PSD 95 SAP90; Shaker; synapse; synapse targeting

Indexed keywords

MEMBRANE PROTEIN; POTASSIUM CHANNEL;

ARTICLE; DROSOPHILA; GENE LOCATION; GENE MUTATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; TISSUE DISTRIBUTION;

EID: 0031034750     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.17-01-00152.1997     Document Type: Article

References (44)

1. Apel ED, Merlie JP (1995) The assembly of the postsynaptic apparatus. Curr Opin Neurobiol 5:62-67.
2. Bartel PL, Chien C-T, Sternglanz R, Fields S (1993) Using the 2-hybrid system to detect protein-protein interactions. In: Cellular interactions in development: a practical approach, pp 153-179. Oxford: Oxford UP.
3. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development (Camb) 118:401-415.
4. Broadie K, Bate M (1993) Activity-dependent development of the neuromuscular synapse during Drosophila embryogenesis. Neuron 11:607-619.
5. Budnik V (1996) Synapse maturation and structural plasticity at Drosophila neuromuscular junctions. Curr Opin Neurobiol, in press.
6. Budnik V, Zhong Y, Wu C-F (1990) Morphological plasticity of motor axon terminals in Drosophila mutants with altered excitability. J Neurosci 10:3754-3768.
7. Budnik V, Koh Y-H, Guan B, Haugh C, Woods D, Gorczyca M (1996) Regulation of synapse structure and function by the Drosophila tumor suppressor gene, dlg. Neuron 17:627-640.
8. Cho K-O, Hunt CA, Kennedy MB (1992) The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 9:929-942.
9. Doyle DA, Lee A, Lewis J, Kim E, Sheng M, MacKinnon R (1996) Crystal structures of a complexed and peptide-free membrane protein-binding domain: molecular basis of peptide recognition by PDZ. Cell 85:1067-1076.
10. Fehon RG, Dawson IA, Artavanis-Tsakonas S (1994) A Drosophila homologue of membrane-skeleton protein 4.1 is associated with septate junctions and is encoded by the coracle gene. Development (Camb) 120:545-547.
11. Ferrús A, Llamazares S, de la Pompa JL, Tanouye MA, Pongs O (1990) Genetic analysis of the Shaker gene complex of Drosophila melanogaster. Genetics 125:383-398.
12. Fields S, Song O-K (1989) A novel genetic system to detect protein-protein interactions. Nature 340:245-246.
13. Froehner SC (1993) Regulation of ion channel distribution at synapses. Annu Rev Neurosci 16:347-368.
14. Garner C, Kindler S (1996) Synaptic proteins and the assembly of synaptic junctions. Trends Cell Biol 6:429-433.
15. Gisselman G, Sewing S, Madsen BW, Mallart A, Angaut-Petit D, Müller-Holtkamp F, Ferrús A, Pongs O (1989) The interference of truncated with normal potassium channel subunits leads to abnormal behaviour in transgenic Drosophila melanogaster. EMBO J 8:2359-2364.
16. Gomperts SN (1996) Clustering membrane proteins: it's all coming together with the PSD-95/SAP-90 protein family. Cell 84:659-662.
17. Gorczyca MG, Augart C, Budnik V (1993) Insulin-like receptor and insulin-like peptide are localized at neuromuscular junctions in Drosophila. J Neurosci 13:3692-3704.
18. Guan B, Hartmann B, Koh Y-H, Gorczyca M, Budnik V (1996) The Drosophila tumor suppressor gene, dlg, is involved in structural plasticity at a glutamatergic synapse. Curr Biol 6:695-706.
19. Hall ZW, Sanes JR (1993) Synaptic structure and development: the neuromuscular junction. Neuron 10:99-121.
20. Haugland FN, Wu C-F (1990) A voltage-clamp analysis of gene-dosage effects of the Shaker locus on larval muscle potassium currents in Drosophila. J Neurosci 10:1357-1371.
21. Jarecki J, Keshishian H (1995) Role of neural activity during synaptogenesis in Drosophila. J Neurosci 15:8177-8190.
22. 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.
23. Khuse J, Betz H, Kirsch J (1995) The inhibitory glycine receptor: architecture, synaptic localization, and molecular pathology of a postsynaptic ion-channel complex. Curr Opin Neurobiol 5:318-323.
24. + channel clustering activity of PSD-95 and SAP-97, two related membrane-associated putative guanylate kinases. Neuropharmacology, in press.
25. + channels by interaction with a family of membrane-associated guanylate kinases. Nature 378:85-88.
26. Kim E, Cho K-O, Rothschild AR, Sheng M (1996) Heteromultimerization and NMDA receptor clustering activity of chapsyn-110, a member of the PSD-95 family of synaptic proteins. Neuron 17:103-113.
27. Kistner U, Wenzel BM, Veh RW, Cases-Langhoff C, Garner AM, Appeltauer U, Voss B, Gundelfinger ED, Garner CC (1993) SAP90, a rat presynaptic protein related to the product of the Drosophila tumor suppressor gene dlg-A. J Biol Chem 268:4580-4583.
28. Kornau H-C, Schenker LT, Kennedy MB, Seeburg PH (1995) Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269:1737-1740.
29. Lahey T, Gorczyca M, Jia X, Budnik V (1994) The Drosophila tumor suppressor gene dlg is required for normal synaptic bouton structure. Neuron 13:823-835.
30. Lindsley DL, Zimm GG (1992) The genome of Drosophila melanogaster. New York: Academic.
31. Lue RA, Marfatia SM, Branton D, Chrishti AH (1994) Cloning and characterization of hdlg: the human homologue of the Drosophila discslarge tumor suppressor binds to protein 4.1. Proc Natl Acad Sci USA 91:9818-9822.
32. Marchesi VT (1985) Stabilizing infrastructure of cell membranes. Annu Rev Cell Biol 1:531-561.
33. Monastirioti M, Gorczyca M, Rapus J, Eckert M, White K, Budnik V (1995) Octopamine-immunoreactivity in the fruit fly Drosophila melanogaster. J Comp Neurol 356:275-287.
34. Niethammer M, Kim E, Sheng M (1996) Interaction between the C terminus of NMDA receptor subunits and multiple members of the PSD95 family of membrane-associated guanylate kinases. J Neurosci 16:2157-2163.
35. Perrimon N (1989) The maternal effect of lelhal (1) discs-large-1: a recessive oncogene of Drosophila melanogaster. Dev Biol 127:392-407.
36. Pongs O, Kecskemethy N, Muller R, Krah-Jentgens I, Baumann A, Kiltz HH, Canal I, Llamazares S, Ferrús A (1988) Shaker encodes a family of putative potassium channel proteins in the nervous system of Drosophila. EMBO J 7:1087-1096.
37. Rogero O, Tejedor FJ (1995) Immunochemical characterization and developmental expression of Shaker potassium channels from the nervous system of Drosophila. J Biol Chem 270:25746-25751.
38. Schwarz TL, Tempel BL,Papazian DM, Jan YN, Jan LY (1988) Multiple potassium-channel components are produced by alternative splicing at the Shaker locus in Drosophila. Nature 331:137-142.
39. + channel proteins in rat central neurons. Neuron 9:271-284.
40. Singh S, Wu C-F (1989) Complete separation of four potassium currents in Drosophila. Neuron 2:1325-1329.
41. Woods DF, Bryant PJ (1991) The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 66:451-464.
42. Woods DF, Bryant PJ (1993) ZO-1, DLGA, and PSD-95/SAP-90: homologous proteins in tight, septate, and synaptic cell junctions. Mech Dev 44:85-89.
43. Woods DF, Hough C, Peel D, Callaini G, Bryant P (1996) The DLG protein is required for junction structure, cell polarity, and proliferation control in Drosophila epithelia. J Cell Biol 134:1469-1482.
44. Wu C-F, Haugland FN (1985) Voltage-clamp analysis of membrane currents in larval muscle fibers of Drosophila: alteration of potassium currents in Shaker mutants. J Neurosci 5:2626-2640.