Abnormal synaptic vesicle biogenesis in Drosophila synaptogyrin mutants

Journal of Neuroscience

Volumn 32, Issue 50, 2012, Pages 18054-18067

  Stevens, Robin J ^a   Akbergenova, Yulia ^a   Jorquera, Ramon A ^a,b   Troy Littleton, J ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b SCHOOL OF MEDICINE   (Puerto Rico)

Author keywords

[No Author keywords available]

Indexed keywords

SYNAPTOGYRIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CONTROLLED STUDY; DELETION MUTANT; DROSOPHILA; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; NERVE CELL STIMULATION; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROMODULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; STRUCTURAL HOMOLOGY; SYNAPSE VESICLE; TRANSGENICS; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOTTING, WESTERN; DROSOPHILA; IMMUNOHISTOCHEMISTRY; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; MUTATION; NEUROMUSCULAR JUNCTION; PATCH-CLAMP TECHNIQUES; SYNAPTIC VESICLES; SYNAPTOGYRINS;

EID: 84870996732     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2668-12.2012     Document Type: Article

References (77)

1. Abraham C, Hutter H, Palfreyman MT, Spatkowski G, Weimer RM, Windoffer R, Jorgensen EM, Leube RE (2006) Synaptic tetraspan vesicle membrane proteins are conserved but not needed for synaptogenesis and neuronal function in Caenorhabditis elegans. Proc Natl Acad Sci U S A 103:8227-8232. CrossRef Medline
2. Abraham C, Bai L, Leube RE (2011) Synaptogyrin-dependent modulation of synaptic neurotransmission in Caenorhabditis elegans. Neuroscience 190:75-88. CrossRef Medline
3. Akbergenova Y, Bykhovskaia M (2009) Enhancement of the endosomal endocytic pathway increases quantal size. Mol Cell Neurosci 40:199-206. CrossRef Medline
4. Arthur CP, Stowell MH (2007) Structure of synaptophysin: a hexameric MARVEL-domain channel protein. Structure 15:707-714. CrossRef Medline
5. Barber CF, Jorquera RA, Melom JE, Littleton JT (2009) Postsynaptic regulation of synaptic plasticity by synaptotagmin 4 requires both C2 domains. J Cell Biol 187:295-310. CrossRef Medline
6. Belfort GM, Bakirtzi K, Kandror KV (2005) Cellugyrin induces biogenesis of synaptic-like microvesicles in PC12 cells. J Biol Chem 280:7262-7272. CrossRef Medline
7. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415. Medline
8. Brand SH, Laurie SM, Mixon MB, Castle JD (1991) Secretory carrier membrane proteins 31-35 define a common protein composition among secretory carrier membranes. J Biol Chem 266:18949-18957. Medline
9. Budnik V, Zhong Y, Wu CF (1990) Morphological plasticity of motor axons in Drosophila mutants with altered excitability. J Neurosci 10:3754-3768. Medline
10. Calakos N, Scheller RH (1994) Vesicle-associated membrane protein and synaptophysin are associated on the synaptic vesicle. J Biol Chem 269: 24534-24537. Medline
11. Cheng MC, Chen CH (2007) Identification of rare mutations of synaptogyrin 1 gene in patients with schizophrenia. J Psychiatr Res 41:1027-1031. CrossRef Medline
12. Cho RW, Song Y, Littleton JT (2010) Comparative analysis of Drosophila and mammalian complexins as fusion clamps and facilitators of neurotransmitter release. Mol Cell Neurosci 45:389-397. CrossRef Medline
13. Cochilla AJ, Angleson JK, Betz WJ (1999) Monitoring secretory membrane with FM1-43 fluorescence. Annu Rev Neurosci 22:1-10. CrossRef Medline
14. Collins CA, DiAntonio A (2007) Synaptic development: insights from Drosophila. Curr Opin Neurobiol 17:35-42. CrossRef Medline
15. Daly C, Ziff EB (2002) Ca2+-dependent formation of a dynaminsynaptophysin complex: potential role in synaptic vesicle endocytosis. J Biol Chem 277:9010-9015. CrossRef Medline
16. Daly C, Sugimori M, Moreira JE, Ziff EB, Llinás R (2000) Synaptophysin regulates clathrin-independent endocytosis of synaptic vesicles. Proc Natl Acad Sci U S A 97:6120-6125. CrossRef Medline
17. De Camilli P, Takei K (1996) Molecular mechanisms in synaptic vesicle endocytosis and recycling. Neuron 16:481-486. CrossRef Medline
18. de Lange RP, de Roos AD, Borst JG (2003) Two modes of vesicle recycling in the rat calyx of Held. J Neurosci 23:10164-10173. Medline
19. Dickman DK, Horne JA, Meinertzhagen IA, Schwarz TL (2005) A slowed classical pathway rather than kiss-and-run mediates endocytosis at synapses lacking synaptojanin and endophilin. Cell 123:521-533. CrossRef Medline
20. Dickman DK, Lu Z, Meinertzhagen IA, Schwarz TL (2006) Altered synaptic development and active zone spacing in endocytosis mutants. Curr Biol 16:591-598. CrossRef Medline
21. Di Tommaso P, Moretti S, Xenarios I, Orobitg M, Montanyola A, Chang JM, Taly JF, Notredame C (2011) T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res 39:W13-W17. CrossRef Medline
22. Edelmann L, Hanson PI, Chapman ER, Jahn R (1995) Synaptobrevin binding to synaptophysin: a potential mechanism for controlling the exocytotic fusion machine. EMBO J 14:224-231. Medline
23. Estrada B, Maeland AD, Gisselbrecht SS, Bloor JW, Brown NH, Michelson AM (2007) The MARVEL domain protein, Singles Bar, is required for progression past the pre-fusion complex stage of myoblast fusion. Dev Biol 307:328-339. CrossRef Medline
24. Evans GJ, Cousin MA (2007) Activity-dependent control of slow synaptic vesicle endocytosis by cyclin-dependent kinase 5. J Neurosci 27:401-411. CrossRef Medline
25. Fernández-Chacón R, Südhof TC (2000) Novel SCAMPs lacking NPF repeats: ubiquitous and synaptic vesicle-specific forms implicate SCAMPs in multiple membrane-trafficking functions. J Neurosci 20:7941-7950. Medline
26. Furuse M, Tsukita S (2006) Claudins in occluding junctions of humans and flies. Trends Cell Biol 16:181-188. CrossRef Medline
27. Gincel D, Shoshan-Barmatz V (2002) The synaptic vesicle protein synapto physin: purification and characterization of its channel activity. Biophys J 83:3223-3229. CrossRef Medline
28. Granseth B, Odermatt B, Royle SJ, Lagnado L (2006) Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 51:773-786. CrossRef Medline
29. Guan Z, Saraswati S, Adolfsen B, Littleton JT (2005) Genome-wide transcriptional changes associated with enhanced activity in the Drosophila nervous system. Neuron 48:91-107. CrossRef Medline
30. Guerrero G, Rieff DF, Agarwal G, Ball RW, Borst A, Goodman CS, Isacoff EY (2005) Heterogeneity in synaptic transmission along a Drosophila larval motor axon. Nat Neurosci 8:1188-1196. CrossRef Medline
31. Hartline DK, Colman DR (2007) Rapid conduction and the evolution of giant axons and myelinated fibers. Curr Biol 17:R29-R35. CrossRef Medline
32. Hayashi M, Raimondi A, O'Toole E, Paradise S, Collesi C, Cremona O, Ferguson SM, De Camilli P (2008) Cell-and stimulus-dependent heterogeneity of synaptic vesicle endocytic recycling mechanisms revealed by studies of dynamin 1-null neurons. Proc Natl Acad Sci U S A 105:2175-2180. CrossRef Medline
33. He L, Wu LG (2007) The debate on the kiss-and-run fusion at synapses. Trends Neurosci 30:447-455. CrossRef Medline
34. Heuser JE, Reese TS (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 57:315-344. CrossRef Medline
35. Hubbard C, Singleton D, Rauch M, Jayasinghe S, Cafiso D, Castle D (2000) The secretory carrier membrane protein family: structure and membrane topology. Mol Biol Cell 11:2933-2947. Medline
36. Hübner K, Windoffer R, Hutter H, Leube RE (2002) Tetraspan vesicle membrane proteins: synthesis, subcellular localization, and functional properties. Int Rev Cytol 214:103-159. CrossRef Medline
37. Huntwork S, Littleton JT (2007) A complexin fusion clamp regulates spontaneous neurotransmitter release and synaptic growth. Nat Neurosci 10: 1235-1237. CrossRef Medline
38. Iatropoulos P, Gardella R, Valsecchi P, Magri C, Ratti C, Podavini D, Rossi G, Gennarelli M, Sacchetti E, Barlati S (2009) Association study and mutational screening of SYNGR1 as a candidate susceptibility gene for schizophrenia. Psychiatr Genet 19:237-243. CrossRef Medline
39. Jan LY, Jan YN (1976) L-glutamate as an excitatory transmitter at the Drosophila larval neuromuscular junction. J Physiol 262:215-236. Medline
40. Janz R, Südhof TC, Hammer RE, Unni V, Siegelbaum SA, Bolshakov VY (1999) Essential roles in synaptic plasticity for synaptogyrin I and synaptophysin I. Neuron 24:687-700. CrossRef Medline
41. Kay AR, Alfonso A, Alford S, Cline HT, Holgado AM, Sakmann B, Snitsarev VA, Stricker TP, Takahashi M, Wu LG (1999) Imaging synaptic activity in intact brain and slices with FM1-43 in C. elegans, lamprey, and rat. Neuron 24:809-817. CrossRef Medline
42. Khodosh R, Augsburger A, Schwarz TL, Garrity PA (2006) Bchs, a BEACH domain protein, antagonizes Rab11 in synapse morphogenesis and other developmental events. Development 133:4655-4665. CrossRef Medline
43. King N, et al. (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451:783-788. CrossRef Medline
44. Koenig JH, Ikeda K (1996) Synaptic vesicles have two distinct recycling pathways. J Cell Biol 135:797-808. CrossRef Medline
45. Koh TW, Verstreken P, Bellen HJ (2004) Dap160/intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis. Neuron 43:193-205. CrossRef Medline
46. Koh TW, Korolchuk VI, Wairkar YP, Jiao W, Evergren E, Pan H, Zhou Y, Venken KJ, Shupliakov O, Robinson IM, O'Kane CJ, Bellen HJ (2007) Eps15 and Dap160 control synaptic vesicle membrane retrieval and synapse development. J Cell Biol 178:309-322. CrossRef Medline
47. Kwon SE, Chapman ER (2011) Synaptophysin regulates the kinetics of synaptic vesicle endocytosis in central neurons. Neuron 70:847-854. CrossRef Medline
48. Lnenicka GA, Keshishian H (2000) Identified motor terminals in Drosophila larvae show distinct differences in morphology and physiology. J Neurobiol 43:186-197. CrossRef Medline
49. Markstein M, Pitsouli C, Villalta C, Celniker SE, Perrimon N (2008) Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes. Nat Genet 40:476-483. CrossRef Medline
50. Marxen M, Volknandt W, Zimmermann H (1999) Endocytic vacuoles formed following a short pulse of K+-stimulation contain a plethora of presynaptic membrane proteins. Neuroscience 94:985-996. CrossRef Medline
51. McMahon HT, Bolshakov VY, Janz R, Hammer RE, Siegelbaum SA, Südhof TC (1996) Synaptophysin, a major synaptic vesicle protein, is not essential for neurotransmitter release. Proc Natl Acad Sci U S A 93:4760-4764. CrossRef Medline
52. Miller TM, Heuser JE (1984) Endocytosis of synaptic vesicle membrane at the frog neuromuscular junction. J Cell Biol 98:685-698. CrossRef Medline
53. Ni JQ, Markstein M, Binari R, Pfeiffer B, Liu LP, Villalta C, Booker M, Perkins L, Perrimon N (2008) Vector and parameters for targeted transgenic RNA interference in Drosophila melanogaster. Nat Methods 5:49-51. CrossRef Medline
54. Nonet ML (1999) Visualization of synaptic specializations in live C. elegans with synaptic vesicle protein-GFP fusions. J Neurosci Methods 89:33-40. CrossRef Medline
55. Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205-217. CrossRef Medline
56. Peled ES, Isacoff EY (2011) Optical quantal analysis of synaptic transmission in wild-type and rab3-mutant Drosophila motor axons. Nat Neurosci 14:519-526. CrossRef Medline
57. Plate M, Li T, Wang Y, Mo X, Zhang Y, Ma D, Han W (2010) Identification and characterization of CMTM4, a novel gene with inhibitory effects on HeLa cell growth through Inducing G2/M phase accumulation. Mol Cells 29:355-361. CrossRef Medline
58. Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov VV, Jurka J, Genikhovich G, Grigoriev IV, Lucas SM, Steele RE, Finnerty JR, Technau U, Martindale MQ, Rokhsar DS (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86-94. CrossRef Medline
59. Rehm H, Wiedenmann B, Betz H (1986) Molecular characterization of synaptophysin, a major calcium-binding protein of the synaptic vesicle membrane. EMBO J 5:535-541. Medline
60. Richards DA, Guatimosim C, Betz WJ (2000) Two endocytic recycling routes selectively fill two vesicle pools in frog motor nerve terminals. Neuron 27:551-559. CrossRef Medline
61. Richards DA, Guatimosim C, Rizzoli SO, Betz WJ (2003) Synaptic vesicle pools at the frog neuromuscular junction. Neuron 39:529-541. CrossRef Medline
62. Sánchez-Pulido L, Martín-Belmonte F, Valencia A, Alonso MA (2002) MARVEL: a conserved domain involved in membrane apposition events. Trends Biochem Sci 27:599-601. CrossRef Medline
63. Spiwoks-Becker I, Vollrath L, Seeliger MW, Jaissle G, Eshkind LG, Leube RE (2001) Synaptic vesicle alterations in rod photoreceptors of synaptophysin-deficient mice. Neuroscience 107:127-142. CrossRef Medline
64. Srivastava M, et al. (2008) The Trichoplax genome and the nature of placozoans. Nature 454:955-960. CrossRef Medline
65. Srivastava M, et al. (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720-726. CrossRef Medline
66. Takamori S, et al. (2006) Molecular anatomy of a trafficking organelle. Cell 127:831-846. CrossRef Medline
67. Takei K, Mundigl O, Daniell L, De Camilli P (1996) The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J Cell Biol 133:1237-1250. CrossRef Medline
68. Thiele C, Hannah MJ, Fahrenholz F, Huttner WB (2000) Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat Cell Biol 2:42-49. CrossRef Medline
69. Thomas L, Hartung K, Langosch D, Rehm H, Bamberg E, Franke WW, Betz H (1988) Identification of synaptophysin as a hexameric channel protein of the synaptic vesicle membrane. Science 242:1050-1053. CrossRef Medline
70. Uytterhoeven V, Kuenen S, Kasprowicz J, Miskiewicz K, Verstreken P (2011) Loss of skywalker reveals synaptic endosomes as sorting stations for synaptic vesicle proteins. Cell 145:117-132. CrossRef Medline
71. Verma R, Chauhan C, Saleem Q, Gandhi C, Jain S, Brahmachari SK (2004) A nonsense mutation in the synaptogyrin 1 gene in a family with schizophrenia. Biol Psychiatry 55:196-199. CrossRef Medline
72. Verma R, Kubendran S, Das SK, Jain S, Brahmachari SK (2005) SYNGR1 is associated with schizophrenia and bipolar disorder in southern India. J Hum Genet 50:635-640. CrossRef Medline
73. Verstreken P, Kjaerulff O, Lloyd TE, Atkinson R, Zhou Y, Meinertzhagen IA, Bellen HJ (2002) Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell 109:101-112. CrossRef Medline
74. Verstreken P, Koh TW, Schulze KL, Zhai RG, Hiesinger PR, Zhou Y, Mehta SQ, Cao Y, Roos J, Bellen HJ (2003) Synaptojanin is recruited by endophilin to promote synaptic vesicle uncoating. Neuron 40:733-748. CrossRef Medline
75. Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, Dürrbeck H, Buchner S, Dabauvalle MC, Schmidt M, Qin G, Wichmann C, Kittel R, Sigrist SJ, Buchner E (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. CrossRef Medline
76. Washbourne P, Schiavo G, Montecucco C (1995) Vesicle-associated membrane protein-2 (synaptobrevin-2) forms a complex with synaptophysin. Biochem J 305:721-724. Medline
77. Wu W, Xu J, Wu XS, Wu LG (2005) Activity-dependent acceleration of endocytosis at a central synapse. J Neurosci 25:11676-11683. CrossRef Medline