UNC-41/stonin functions with AP2 to recycle synaptic vesicles in Caenorhabditis elegans

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Mullen, Gregory P ^a   Grundahl, Kiely M ^a   Gu, Mingyu ^b   Watanabe, Shigeki ^b   Hobson, Robert J ^b   Crowell, John A ^a   McManus, John R ^a   Mathews, Eleanor A ^a   Jorgensen, Erik M ^b   Rand, James B ^a  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CAENORHABDITIS ELEGANS PROTEIN; MU ADAPTIN; PROTEIN AP2; PROTEIN UNC 41; STONIN; SYNAPTOTAGMIN; UNCLASSIFIED DRUG;

ACETYLCHOLINE MOTOR NEURON; APM 2 GENE; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; ENDOCYTOSIS; GABA MOTOR NEURON; GENE; GENE EXPRESSION; GENE FUNCTION; MOTONEURON; MUTANT; NERVE CELL LESION; NONHUMAN; PHENOTYPE; PROTEIN FAMILY; PROTEIN FUNCTION; SNT 1 GENE; SYNAPSE VESICLE; UNC 41 GENE;

ADAPTOR PROTEIN COMPLEX 2; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CARRIER PROTEINS; CLONING, MOLECULAR; DROSOPHILA PROTEINS; ENDOCYTOSIS; GENE EXPRESSION REGULATION; GENES, HELMINTH; GENOME; MUTATION; NERVE TISSUE PROTEINS; NERVOUS SYSTEM; PHENOTYPE; PROTEIN TRANSPORT; SYNAPTIC VESICLES; SYNAPTOTAGMINS;

CAENORHABDITIS ELEGANS; MAMMALIA;

EID: 84863698848     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040095     Document Type: Article

References (55)

1. Dittman J, Ryan TA, (2009) Molecular circuitry of endocytosis at nerve terminals. Annu Rev Cell Dev Biol 25: 133-160.
2. Robinson MS, Bonifacino JS, (2001) Adaptor-related proteins. Curr Opin Cell Biol 13: 444-453.
3. Jackson LP, Kelly BT, McCoy AJ, Gaffry T, James LC, et al. (2010) A large-scale conformational change couples membrane recruitment to cargo binding in the AP2 clathrin adaptor complex. Cell 141: 1220-1229.
4. Zhang B, Koh YH, Beckstead RB, Budnik V, Ganetzky B, et al. (1998) Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron 21: 1465-1475.
5. Nonet ML, Holgado AM, Brewer F, Serpe CJ, Norbeck BA, et al. (1999) UNC-11, a Caenorhabditis elegans AP180 homologue, regulates the size and protein composition of synaptic vesicles. Mol Biol Cell 10: 2343-2360.
6. Bao H, Daniels RW, MacLeod GT, Charlton MP, Atwood HL, et al. (2005) AP180 Maintains the Distribution of Synaptic and Vesicle Proteins in the Nerve Terminal and Indirectly Regulates the Efficacy of Ca2+-Triggered Exocytosis. J Neurophysiol 94: 1888-1903.
7. Harel A, Wu F, Mattson MP, Morris CM, Yao PJ, (2008) Evidence for CALM in directing VAMP2 trafficking. Traffic 9: 417-429.
8. Koo SJ, Markovic S, Puchkov D, Mahrenholz CC, Beceren-Braun F, et al. (2011) SNARE motif-mediated sorting of synaptobrevin by the endocytic adaptors clathrin assembly lymphoid myeloid leukemia (CALM) and AP180 at synapses. Proceedings of the National Academy of Sciences 108: 13540-13545.
9. Schuske K, Palfreyman MT, Watanabe S, Jorgensen EM, (2007) UNC-46 is required for trafficking of the vesicular GABA transporter. Nat Neurosci 10: 846-853.
10. Maritzen T, Podufall J, Haucke V, (2010) Stonins-specialized adaptors for synaptic vesicle recycling and beyond? Traffic 11: 8-15.
11. Grigliatti TA, Hall L, Rosenbluth R, Suzuki DT, (1973) Temperature-sensitive mutations in Drosophila melanogaster. XIV. A selection for immobile adults. Mol Gen Genet 120: 107-114.
12. Fergestad T, Davis WS, Broadie K, (1999) The stoned proteins regulate synaptic vesicle recycling in the presynaptic terminal. J Neurosci 19: 5847-5860.
13. Kelly LE, Phillips AM, (2005) Molecular and genetic characterization of the interactions between the Drosophila stoned-B protein and DAP-160 (intersectin). Biochem J 388: 195-204.
14. Martina JA, Bonangelino CJ, Aguilar RC, Bonifacino JS, (2001) Stonin 2: An adaptor-like protein that interacts with components of the endocytic machinery. J Cell Biol 153: 1111-1120.
15. Walther K, Diril MK, Jung N, Haucke V, (2004) Functional dissection of the interactions of stonin 2 with the adaptor complex AP-2 and synaptotagmin. Proc Natl Acad Sci U S A 101: 964-969.
16. Diril MK, Wienisch M, Jung N, Klingauf J, Haucke V, (2006) Stonin 2 is an AP-2-dependent endocytic sorting adaptor for synaptotagmin internalization and recycling. Dev Cell 10: 233-244.
17. Phillips AM, Smith M, Ramaswami M, Kelly LE, (2000) The products of the Drosophila stoned locus interact with synaptic vesicles via synaptotagmin. J Neurosci 20: 8254-8261.
18. Phillips AM, Ramaswami M, Kelly LE, (2010) Stoned. Traffic 11: 16-24.
19. Jung N, Wienisch M, Gu M, Rand JB, Muller SL, et al. (2007) Molecular basis of synaptic vesicle cargo recognition by the endocytic sorting adaptor stonin 2. The Journal of Cell Biology 179: 1497-1510.
20. Fergestad T, Broadie K, (2001) Interaction of stoned and synaptotagmin in synaptic vesicle endocytosis. J Neurosci 21: 1218-1227.
21. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
22. Rand JB, Russell RL, (1985) Molecular basis of drug-resistance mutations in the nematode Caenorhabditis elegans. Psychopharm Bull 21: 623-630.
23. Harada S, Hori I, Yamamoto H, Hosono R, (1994) Mutations in the unc-41 gene cause elevation of acetylcholine levels. J Neurochem 63: 439-446.
24. Nguyen M, Alfonso A, Johnson CD, Rand JB, (1995) Caenorhabditis elegans mutants resistant to inhibitors of acetylcholinesterase. Genetics 140: 527-535.
25. McIntire SL, Jorgensen E, Horvitz HR, (1993) Genes required for GABA function in Caenorhabditis elegans. Nature 364: 334-337.
26. Miller KG, Alfonso A, Nguyen M, Crowell JA, Johnson CD, et al. (1996) A genetic selection for Caenorhabditis elegans synaptic transmission mutants. Proc Natl Acad Sci USA 93: 12593-12598.
27. Nonet ML, Grundahl K, Meyer BJ, Rand JB, (1993) Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 73: 1291-1305.
28. Brett TJ, Traub LM, Fremont DH, (2002) Accessory protein recruitment motifs in clathrin-mediated endocytosis. Structure 10: 797-809.
29. Jha A, Agostinelli NR, Mishra SK, Keyel PA, Hawryluk MJ, et al. (2004) A novel AP-2 adaptor interaction motif initially identified in the long-splice isoform of synaptojanin 1, SJ170. J Biol Chem 279: 2281-2290.
30. Ritter B, Denisov AY, Philie J, Deprez C, Tung EC, et al. (2004) Two WXXF-based motifs in NECAPs define the specificity of accessory protein binding to AP-1 and AP-2. EMBO Journal 23: 3701-3710.
31. Sheng M, Sala C, (2001) PDZ domains and the organization of supramolecular complexes. Annu Rev Neurosci 24: 1-29.
32. Gu M, Schuske K, Watanabe S, Liu Q, Baum P, et al. (2008) m2 adaptin facilitates but is not essential for synaptic vesicle recycling in Caenorhabditis elegans. J Cell Biol 183: 881-892.
33. Mathews EA, Mullen GP, Crowell JA, Duerr JS, McManus JR, et al. (2007) Differential expression and function of synaptotagmin 1 isoforms in Caenorhabditis elegans. Mol Cell Neurosci 34: 642-652.
34. Mohrmann R, Matthies HJ, Woodruff E III, Broadie K, (2008) Stoned B mediates sorting of integral synaptic vesicle proteins. Neuroscience 153: 1048-1063.
35. Hall DH, Hedgecock EM, (1991) Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans. Cell 65: 837-847.
36. Otsuka AJ, Jeyaprakash A, Garcia-Añoveros J, Tang LZ, Fisk G, et al. (1991) The C. elegans unc-104 gene encodes a putative kinesin heavy chain-like protein. Neuron 6: 113-122.
37. Estes PS, Jackson TC, Stiimson DT, Sanyal S, Kelly LE, et al. (2003) Functional dissection of a eukaryotic dicistronic gene: Transgenic stonedB, but not stonedA, restores normal synaptic properties to Drosophila stoned mutants. Genetics 165: 185-196.
38. Frøkjær-Jensen C, Davis MW, Hopkins CE, Newman BJ, Thummel JM, et al. (2008) Single-copy insertion of transgenes in Caenorhabditis elegans. Nat Genet 40: 1375-1383.
39. Harris TW, Hartwieg E, Horvitz HR, Jorgensen EM, (2000) Mutations in synaptojanin disrupt synaptic vesicle recycling. J Cell Biol 150: 589-599.
40. Stimson DT, Estes PS, Rao S, Krishnan KS, Kelly LE, et al. (2001) Drosophila Stoned Proteins Regulate the Rate and Fidelity of Synaptic Vesicle Internalization. J Neurosci 21: 3034-3044.
41. Petrovich TZ, Merakovsky J, Kelly LE, (1993) A genetic analysis of the stoned locus and its interaction with dunce, shibire, and Suppressor of stoned variants of Drosophila melanogaster. Genetics 133: 955-965.
42. Jorgensen EM, Hartwieg E, Schuske K, Nonet ML, Jin Y, et al. (1995) Defective recycling of synaptic vesicles in synaptotagmin mutants of Caenorhabditis elegans. Nature 378: 196-199.
43. Verstreken P, Kjaerulff O, Lloyd TE, Atkinson R, Zhou Y, et al. (2002) Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell 109: 101-112.
44. Poskanzer KE, Fetter RD, Davis GW, (2006) Discrete residues in the c(2)b domain of synaptotagmin I independently specify endocytic rate and synaptic vesicle size. Neuron 50: 49-62.
45. Yao J, Kwon SE, Gaffaney JD, Dunning FM, Chapman ER, (2012) Uncoupling the roles of synaptotagmin I during endo- and exocytosis of synaptic vesicles. Nat Neurosci 15: 243-249.
46. Moerman DG, Benian GM, Waterston RH, (1986) Molecular cloning of the muscle gene unc-22 in Caenorhabditis elegans by Tc1 transposon tagging. Proc Natl Acad Sci U S A 83: 2579-2583.
47. Kamikura DM, Cooper JA, (2003) Lipoprotein receptors and a Disabled family cytoplasmic adaptor protein regulate EGL-17/FGF export in C. elegans. Genes Dev 17: 2798-2811.
48. Liu Q, Sommer SS, (1995) Restriction endonuclease fingerprinting (REF): a sensitive method for screening mutations in long, contiguous segments of DNA. BioTechniques 18: 470-477.
49. Miller DM, Desai NS, Hardin DC, Piston DW, Patterson GH, et al. (1999) Two-color GFP expression system for C. elegans. BioTechniques 26: 914-921.
50. Duerr JS, Frisby DL, Gaskin J, Duke A, Asermely K, et al. (1999) The cat-1 gene of C. elegans encodes a vesicular monoamine transporter required for specific monoamine-dependent behaviors. J Neurosci 19: 72-84.
51. Duerr JS, Han H-P, Fields SD, Rand JB, (2008) Identification of major classes of cholinergic neurons in the nematode Caenorhabditis elegans. J Comp Neurol 506: 398-408.
52. Nonet ML, Saifee O, Zhao H, Rand JB, Wei L, (1998) Synaptic transmission deficits in Caenorhabditis elegans synaptobrevin mutants. J Neurosci 18: 70-80.
53. Deken SL, Vincent R, Hadwiger G, Liu Q, Wang ZW, et al. (2005) Redundant localization mechanisms of RIM and ELKS in Caenorhabditis elegans. J Neurosci 25: 5975-5983.
54. Mullen GP, Mathews EA, Saxena P, Fields SD, McManus JR, et al. (2006) The Caenorhabditis elegans snf-11 Gene Encodes a Sodium-dependent GABA Transporter Required for Clearance of Synaptic GABA. Mol Biol Cell 17: 3021-3030.
55. Mello CC, Kramer JM, Stinchcomb D, Ambros V, (1991) Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10: 3959-3970.