Drosophila neto is essential for clustering glutamate receptors at the neuromuscular junction

Genes and Development

Volumn 26, Issue 9, 2012, Pages 974-987

  Kim, Young Jun ^a   Bao, Hong ^b   Bonanno, Liana ^a   Zhang, Bing ^b   Serpel, Mihaela ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

Auxiliary subunits; Drosophila; Glutamate receptor; Glutamatergic synapses; Neuromuscular junction; Postsynaptic density; Synapse assembly

Indexed keywords

GLUTAMATE RECEPTOR; IONOTROPIC RECEPTOR; NEUROPILIN; TOLLOID METALLOPROTEINASE;

ARTICLE; DROSOPHILA; GENE CLUSTER; GENE EXPRESSION; GENE FUNCTION; MUSCLE FUNCTION; NERVE GROWTH; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SYNAPSE; TRANSGENE;

MAMMALIA;

EID: 84860543993     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.185165.111     Document Type: Article

References (74)

1. Aberle H, Haghighi AP, Fetter RD, McCabe BD, Magalhaes TR, Goodman CS. 2002. Wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 33: 545-558.
2. Ahmari SE, Buchanan J, Smith SJ. 2000. Assembly of presynaptic active zones from cytoplasmic transport packets. Nat Neurosci 3: 445-451.
3. Akins MR, Biederer T. 2006. Cell-cell interactions in synaptogenesis. Curr Opin Neurobiol 16: 83-89.
4. Anderson MJ, Cohen MW. 1977. Nerve-induced and spontaneous redistribution of acetylcholine receptors on cultured muscle cells. I Phvsiol 268: 757-773.
5. 2+-triggered exocytosis. J Neurophysiol 94: 1888-1903.
6. Bellen HJ, Levis RW, He Y, Carlson JW, Evans-Holm M, Bae E, Kim J, Metaxakis A, Savakis C, Schulze KL, et al. 2011. The Drosophila gene disruption project: Progress using transposons with distinctive site specificities. Genetics 188: 731-743.
7. Bogdanik L, Framery B, FrOlich A, Franco B, Mornet D, Bockaert J, Sigrist SJ, Grau Y, Parmentier ML. 2008. Muscle dystroglycan organizes the postsynapse and regulates presynaptic neurotransmitter release at the Drosophila neuromuscular junction. PLoS ONE e2084: 3. doi: 10.1371/journal.pone.0002084
8. Bresler T, Shapira M, Boeckers T, Dresbach T, Futter M, Garner CC, Rosenblum K, Gundelfinger ED, Ziv NE. 2004. Postsynaptic density assembly is fundamentally different from presynaptic active zone assembly. J Neurosci 24: 1507-1520.
9. Broadie KS. 1999. Development of electrical properties and synaptic transmission at the embryonic neuromuscular junction. Int Rev Neurnhinl 43: 45-67
10. Broadie K, Bate M. 1993a. Activity-dependent development of the neuromuscular synapse during Drosophila embryogenesis. Neuron 11: 607-619.
11. Broadie K, Bate M. 1993b. Innervation directs receptor synthesis and localization in Drosophila embryo synaptogenesis. Nature 361: 350-353.
12. Budnik V, Gorczyca M, Prokop A. 2006. Selected methods for the anatomical study of Drosophila embryonic and larval neuromuscular junctions. Int Rev Neurobiol 75: 323-365.
13. Chen K, Featherstone DE. 2005. Discs-large (DLG) is clustered by presynaptic innervation and regulates postsynaptic glutamate receptor subunit composition in Drosophila. BMC Biol 3: 1. doi: 10.1186/1741-7007-3-1
14. Chen K, Featherstone DE. 2011. Pre and postsynaptic roles for Drosophila CASK. Mol Cell Neurosci 48: 171-182.
15. Chen K, Merino C, Sigrist SJ, Featherstone DE. 2005. The 4.1 protein coracle mediates subunit-selective anchoring of Drosophila glutamate receptors to the postsynaptic actin cytoskeleton. J Neurosci 25: 6667-6675.
16. Conder R, Yu H, Ricos M, Hing H, Chia W, Lim LHarden N. 2004. dPak is required for integrity of the leading edge cytoskeleton during Drosophila dorsal closure but does not signal through the INK cascade. Dev Biol 276: 378-390.
17. Copits BA, Robbins JS, Frausto S, Swanson GT. 2011. Synaptic targeting and functional modulation of G1uK1 kainate receptors by the auxiliary neuropilin and tolloid-like (NETO) proteins. J Neurosci 31: 7334-7340.
18. DiAntonio A. 2006. Glutamate receptors at the Drosophila neuromuscular junction. Int Rev Neurobiol 75: 165-179.
19. 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.
20. Featherstone DE, Davis WS, Dubreuil RR, Broadie K. 2001. Drosophila α- and ββ-spectrin mutations disrupt presynaptic neurotransmitter release. J. Neurosci 21: 4215-4224.
21. Featherstone DE, Rushton E, Rohrbough J, Liebl F, Karr J, Sheng Q, Rodesch CK, Broadie K. 2005. An essential Drosophila glutamate receptor subunit that functions in both central neuropil and neuromuscular junction. J Neurosci 25: 3199-3208.
22. Feeney CJ, Karunanithi S, Pearce J, Govind CK, Atwood HL. 1998. Motor nerve terminals on abdominal muscles in larval flesh flies, Sarcophaga bullata: Comparisons with Drosophila. J Comp Neurol 402: 197-209.
23. Gally C, Eimer S, Richmond JE, Bessereau JL. 2004. A transmembrane protein required for acetylcholine receptor clustering in Caenorhabditis elegans. Nature 431: 578-582.
24. Gho M. 1994. Voltage-clamp analysis of gap junctions between embryonic muscles in Drosophila. J Physiol 481: 371-383.
25. Groc L, Choquet D. 2006. AMPA and NMDA glutamate receptor trafficking: Multiple roads for reaching and leaving the synapse. Cell Tissue Res 326: 423-438.
26. Hansen KB, Furukawa H, Traynelis SF. 2010. Control of assembly and function of glutamate receptors by the aminoterminal dnmain. Mol Pharmacol: 78: 535-549.
27. Jackson AC, Nicoll RA. 2011. The expanding social network of ionotropic glutamate receptors: TARPs and other transmembrane auxiliary subunits. Neuron 70: 178-199.
28. Jan LY, Jan YN. 1976. Properties of the larval neuromuscular junction in Drosophila melanogaster. J Physiol 262: 189-214.
29. Kalashnikova E, Lorca RA, Kaur I, Barisone GA, Li B, Ishimaru T, Trimmer JS, Mohapatra DP, Diaz E. 2010. SynDIG1: An activity-regulated, AMPA- receptor-interacting transmembrane protein that regulates excitatory synapse development. Neuron 65: 80-93
30. Keshishian H, Chiba A, Chang TN, Halfon MS, Harkins EW, Jarecki J, Wang L, Anderson M, Cash S, Halpern ME, et al. 1993. Cellular mechanisms governing synaptic development in Drosophila melanogaster. J Neurobiol 24: 757-787.
31. Kim E, Sheng M. 2004. PDZ domain proteins of synapses. Nat Rev Neurosci 5: 771-781.
32. Kumar J, Schuck P, Mayer ML. 2011. Structure and assembly mechanism for heteromeric kainate receptors. Neuron 71: 319-331.
33. Lagow RD, Bao H, Cohen EN, Daniels RW, Zuzek A, Williams WH, Macleod GT, Sutton RB, Zhang B. 2007. Modification of a hydrophobic layer by a point mutation in syntaxin 1A regulates the rate of synaptic vesicle fusion. PLoS Biol e72: 5. doi: 10.1371/journal.pbio.0050072
34. Lahey T, Gorczyca M, Jia XX, Budnik V. 1994. The Drosophila tumor suppressor gene dlg is required for normal synaptic bouton structure. Neuron 13: 823-835.
35. Liebl FL, Featherstone DE. 2008. Identification and investigation of Drosophila postsynaptic density homologs. Bioinform Biol Insights 2: 375-387.
36. Marrus SB, DiAntonio A. 2004. Preferential localization of glutamate receptors opposite sites of high presynaptic release. Curr Biol 14: 924-931.
37. Marrus SB, Portman SL, Allen MJ, Moffat KG, DiAntonio A. 2004. Differential localization of glutamate receptor subunits at the Drosophila neuromuscular junction. J Neurosci 24: 1406-1415.
38. McMahan UJ. 1990. The agrin hypothesis. Cold Spring Harb Symp Quant Biol 55: 407-418.
39. Milstein AD, Nicoll RA. 2008. Regulation of AMPA receptor gating and pharmacology by TARP auxiliary subunits. Trends Pharmacol Sci 29: 333-339.
40. Morimoto T, Nobechi M, Komatsu A, Miyakawa H, Nose A. 2009. Subunit-specific and homeostatic regulation of glutamate receptor localization by CaMKII in Drosophila neuromuscular junctions. Neuroscience 165: 1284-1292.
41. Ng D, Pitcher GM, Szilard RK, Sertie A, Kanisek M, Clapcote SJ, Lipina T, Kalia LV, Joo D, McKerlie C, et al. 2009. Netol is a novel CUB-domain NMDA receptor-interacting protein required for synaptic plasticity and learning. PLoS Biol. 7: e1000041. doi: 10.1371 /journal.pbio.1000041.
42. O'Brien RJ, Xu D, Petralia RS, Steward O, Huganir RL, Worley P. 1999. Synaptic clustering of AMPA receptors by the extracellular immediate-early gene product Narp. Neuron 23: 309-323.
43. Parnas D, Haghighi AP, Fetter RD, Kim SW, Goodman CS. 2001. Regulation of postsynaptic structure and protein localization by the Rho-type guanine nucleotide exchange factor dPix. Neuron 32: 415-424.
44. Passafaro M, Nakagawa T, Sala C, Sheng M. 2003. Induction of dendritic spines by an extracellular domain of AMPA receptor subunit GluR2. Nature 424: 677-681.
45. 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.
46. Pielage J, Fetter RD, Davis GW. 2005. Presynaptic spectrin is essential for synapse stabilization. Curr Biol 15: 918-928.
47. Qin G, Schwarz T, Kittel RJ, Schmid A, Rasse TM, Kappei D, Ponimaskin E, Heckmann M, Sigrist SJ. 2005. Four different subunits are essential for expressing the synaptic glutamate receptor at neuromuscular junctions of Drosophila. J Neurosci 25: 3209-3218.
48. Ramachandran P, Budnik V. 2010. Electron microscopy of Drosophila larval neuromuscular junctions. Cold Spring Harb Protoc 8: pdb.prot5474. doi: 10.1101/pdb.prot5474.
49. Rasse TM, Fouquet W, Schmid A, Kittel RJ, Mertel S, Sigrist CB, Schmidt M, Guzman A, Merino C, Qin G, et al. 2005. Glutamate receptor dynamics organizing synapse formation in vivo. Nat Neurosci 8: 898-905.
50. Regus-Leidig H, Tom Dieck S, Specht D, Meyer L, Brandstatter JH. 2009. Early steps in the assembly of photoreceptor ribbon synapses in the mouse retina: The involvement of precursor spheres. J Comp Neurol 512: 814-824.
51. Rohrbough J, Rushton E, Woodruff E III, Fergestad T, Vigneswaran K, Broadie K. 2007. Presynaptic establishment of the synaptic cleft extracellular matrix is required for post-synaptic differentiation. Genes & Dev 21: 2607-2628.
52. Saglietti L, Dequidt C, Kamieniarz K, Rousset MC, Valnegri P, Thoumine O, Beretta F, Fagni L, Choquet D, Sala C, et al. 2007. Extracellular interactions between GluR2 and N-cadherin in spine regulation. Neuron 54: 461-477.
53. Sanes JR, Lichtman JW. 2001. Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci 2: 791-805.
54. Schmid A, Qin G, Wichmann C, Kittel RJ, Mertel S, Fouquet W, Schmidt M, Heckmann M, Sigrist SJ. 2006 Non-NMDAtype glutamate receptors are essential for maturation but not for initial assembly of synapses at Drosophila neuromuscular junctions. J. Neurosci 26: 11267-11277.
55. Schulze KL, Broadie K, Perin MS, Bellen HJ. 1995. Genetic and electrophysiological studies of Drosophila syntaxin-1A demonstrate its role in nonneuronal secretion and neurotransmission. Cell 80: 311-320.
56. Schwabe T, Bainton RJ, Fetter RD, Heberlein U, Gaul U. 2005. GPCR signaling is required for blood-brain barrier formation in Drosophila. Cell 123: 133-144.
57. Schwenk J, Harmel N, Zolles G, Bildl W, Kulik A, Heimrich B, Chisaka O, Jonas P, Schulte U, Fakler B, et al. 2009. Functional proteomics identify cornichon proteins as auxiliary subunits of AMPA receptors. Science. 323: 1313-1319.
58. Serpe M, O'Connor MB. 2006. The metalloprotease tolloidrelated and its TGF-ββ-like substrate Dawdle regulate Drosophila motoneuron axon guidance. Development 133: 4969-4979.
59. Shepherd JD, Huganir RL. 2007. The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol 23: 613-643.
60. Sia GM, Beique JC, Rumbaugh G, Cho R, Worley P., Huganir RL. 2007. Interaction of the N-terminal domain of the AMPA receptor GluR4 subunit with the neuronal pentraxin NP1 mediates GluR4 synaptic recruitment. Neuron 55: 87-102.
61. Stevens CF. 1976. A comment on Martin's relation. Biophys J16: 891-895.
62. Stewart BA, Atwood HL, Renger JJ, Wang J, Wu CF. 1994. Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J Comp Physiol A 175: 179-191.
63. Straub C, Hunt DL, Yamasaki M, Kim KS, Watanabe M, Castillo PE, Tomita S. 201la. Distinct functions of kainate receptors in the brain are determined by the auxiliary subunit Neto1. Nat Neurosci 14: 866-873.
64. Straub C, Zhang W, Howe JR. 2011b. Neto2 modulation of kainate receptors with different subunit compositions. J Neurosci 31: 8078-8082.
65. Tang M, Pelkey KA, Ng D, Ivakine E, McBain CJ, Salter MW, McInnes RR. 2011. Neto1 is an auxiliary subunit of native synaptic kainate receptors. J Neurosci 31: 10009-10018.
66. Tomita S, Chen L, Kawasaki Y, Petralia RS, Wenthold RJ, Nicoll RA, Bredt DS. 2003. Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins. J Cell Biol 161: 805-816.
67. Venken KJ, Popodi E, Holtzman SL, Schulze KL, Park S, Carlson JW, Hoskins RA, Bellen HJ, Kaufman TC. 2010. A molecularly defined duplication set for the X chromosome of Drosophila melanogaster. Genetics 186: 1111-1125.
68. von Engelhardt J, Mack V, Sprengel R, Kavenstock N, Li KW, Stern-Bach Y, Smit AB, Seeburg PH, Monyer H. 2010. CKAMP44: A brain-specific protein attenuating short-term synaptic plasticity in the dentate gyms. Science 327: 1518-1522.
69. Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, Durrbeck H, Buchner S, Dabauvalle MC, Schmidt M, Qin G, et al. 2006. Bruchpilot, a protein with homology to ELKS/ CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49: 833-844.
70. Walker CS, Francis MM, Brockie PJ, Madsen DM, Zheng Y, Maricq AV. 2006. Conserved SOL-1 proteins regulate ionotropic glutamate receptor desensitization. Proc Natl Acad Sci 103: 10787-10792.
71. Wu H, Xiong WC, Mei L. 2010. To build a synapse: Signaling pathways in neuromuscular junction assembly. Development 137: 1017-1033.
72. Zhang B, Koh YH, Beckstead RB, Budnik V, Ganetzky B, Bellen HJ. 1998. Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron 21: 1465-1475.
73. Zhang W, St-Gelais F, Grabner CP, Trinidad JC, Sumioka A, Morimoto-Tomita M, Kim KS, Straub C, Burlingame AL, Howe JR, et al. 2009. A transmembrane accessory subunit that modulates kainate-type glutamate receptors. Neuron 61: 385-396.
74. Zheng Y, Mellem JE, Brockie PJ, Madsen DM, Maricq AV. 2004. SOL-1 is a CUB-domain protein required for GLR-1 glutamate receptor function in C. elegans. Nature 427: 451-457.