Myosin VI contributes to synaptic transmission and development at the Drosophila neuromuscular junction

BMC Neuroscience

Volumn 12, Issue , 2011, Pages

  Kisiel, Marta ^a   Majumdar, Debolina ^a   Campbell, Shelagh ^a   Stewart, Bryan A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN VI; MYOSIN HEAVY CHAIN;

ALLELE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; GENETIC ANALYSIS; GENOTYPE; LOCOMOTION; LOSS OF FUNCTION MUTATION; MALE; NERVE CELL PLASTICITY; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROMUSCULAR SYNAPSE; NONHUMAN; PROTEIN EXPRESSION; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; ANIMAL; METABOLISM; PHYSIOLOGY;

ANIMALS; DROSOPHILA MELANOGASTER; MYOSIN HEAVY CHAINS; NEUROMUSCULAR JUNCTION; SYNAPTIC TRANSMISSION;

EID: 79960069097     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-12-65     Document Type: Article

References (59)

1. Nunes P, Haines N, Kuppuswamy V, Fleet DJ, Stewart BA. Synaptic vesicle mobility and presynaptic F-actin are disrupted in a N-ethylmaleimide-sensitive factor allele of Drosophila. Mol Biol Cell 2006, 17(11):4709-4719. 10.1091/mbc.E06-03-0253, 1635382, 16914524.
2. Seabrooke S, Qiu X, Stewart B. Nonmuscle Myosin II helps regulate synaptic vesicle mobility at the Drosophila neuromuscular junction. BMC Neuroscience 2010, 11(1):37. 10.1186/1471-2202-11-37, 2853426, 20233422.
3. Gaffield MA, Betz WJ. Synaptic vesicle mobility in mouse motor nerve terminals with and without synapsin. J Neurosci 2007, 27(50):13691-13700. 10.1523/JNEUROSCI.3910-07.2007, 18077680.
4. Gaffield MA, Rizzoli SO, Betz WJ. Mobility of Synaptic Vesicles in Different Pools in Resting and Stimulated Frog Motor Nerve Terminals. Neuron 2006, 51(3):317-325. 10.1016/j.neuron.2006.06.031, 16880126.
5. Jordan R, Lemke EA, Klingauf J. Visualization of synaptic vesicle movement in intact synaptic boutons using fluorescence fluctuation spectroscopy. Biophys J 2005, 89(3):2091-2102. 10.1529/biophysj.105.061663, 1366711, 15980175.
6. Ryan TA. Inhibitors of myosin light chain kinase block synaptic vesicle pool mobilization during action potential firing. J Neurosci 1999, 19(4):1317-1323.
7. Tokuoka H, Goda Y. Myosin light chain kinase is not a regulator of synaptic vesicle trafficking during repetitive exocytosis in cultured hippocampal neurons. J Neurosci 2006, 26(45):11606-11614. 10.1523/JNEUROSCI.3400-06.2006, 17093082.
8. Menetrey J, Llinas P, Mukherjea M, Sweeney HL, Houdusse A. The structural basis for the large powerstroke of myosin VI. Cell 2007, 131(2):300-308. 10.1016/j.cell.2007.08.027, 17956731.
9. Iwaki M, Tanaka H, Iwane AH, Katayama E, Ikebe M, Yanagida T. Cargo-binding makes a wild-type single-headed myosin-VI move processively. Biophys J 2006, 90(10):3643-3652. 10.1529/biophysj.105.075721, 1440745, 16500969.
10. Naccache SN, Hasson T. Myosin VI altered at threonine 406 stabilizes actin filaments in vivo. Cell Motil Cytoskeleton 2006, 63(10):633-645. 10.1002/cm.20150, 16917816.
11. Petritsch C, Tavosanis G, Turck CW, Jan LY, Jan YN. The Drosophila myosin VI Jaguar is required for basal protein targeting and correct spindle orientation in mitotic neuroblasts. Dev Cell 2003, 4(2):273-281. 10.1016/S1534-5807(03)00020-0, 12586070.
12. Rock RS, Rice SE, Wells AL, Purcell TJ, Spudich JA, Sweeney HL. Myosin VI is a processive motor with a large step size. Proc Natl Acad Sci USA 2001, 98(24):13655-13659. 10.1073/pnas.191512398, 61096, 11707568.
13. Hertzano R, Shalit E, Rzadzinska AK, Dror AA, Song L, Ron U, Tan JT, Shitrit AS, Fuchs H, Hasson T, Ben-Tal N, Sweeney HL, de Angelis MH, Steel KP, Avraham KB. A Myo6 mutation destroys coordination between the myosin heads, revealing new functions of myosin VI in the stereocilia of mammalian inner ear hair cells. PLoS Genet 2008, 4(10):e1000207. 10.1371/journal.pgen.1000207, 2543112, 18833301.
14. Hicks JL, Deng WM, Rogat AD, Miller KG, Bownes M. Class VI unconventional myosin is required for spermatogenesis in Drosophila. Mol Biol Cell 1999, 10(12):4341-4353. 25762, 10588662.
15. Noguchi T, Lenartowska M, Miller KG. Myosin VI stabilizes an actin network during Drosophila spermatid individualization. Mol Biol Cell 2006, 17(6):2559-2571. 10.1091/mbc.E06-01-0031, 1474903, 16571671.
16. Noguchi T, Frank DJ, Isaji M, Miller KG. Coiled-coil-mediated dimerization is not required for myosin VI to stabilize actin during spermatid individualization in Drosophila melanogaster. Mol Biol Cell 2009, 20(1):358-367. 10.1091/mbc.E08-07-0776, 2613128, 19005209.
17. Geisbrecht ER, Montell DJ. Myosin VI is required for E-cadherin-mediated border cell migration. Nat Cell Biol 2002, 4(8):616-620.
18. Yoshida H, Cheng W, Hung J, Montell D, Geisbrecht E, Rosen D, Liu J, Naora H. Lessons from border cell migration in the Drosophila ovary: A role for myosin VI in dissemination of human ovarian cancer. Proc Natl Acad Sci USA 2004, 101(21):8144-8149. 10.1073/pnas.0400400101, 419571, 15146066.
19. Vreugde S, Ferrai C, Miluzio A, Hauben E, Marchisio PC, Crippa MP, Bussi M, Biffo S. Nuclear myosin VI enhances RNA polymerase II-dependent transcription. Mol Cell 2006, 23(5):749-755. 10.1016/j.molcel.2006.07.005, 16949370.
20. Millo H, Leaper K, Lazou V, Bownes M. Myosin VI plays a role in cell-cell adhesion during epithelial morphogenesis. Mech Dev 2004, 121(11):1335-1351. 10.1016/j.mod.2004.06.007, 15454264.
21. Maddugoda MP, Crampton MS, Shewan AM, Yap AS. Myosin VI and vinculin cooperate during the morphogenesis of cadherin cell cell contacts in mammalian epithelial cells. J Cell Biol 2007, 178(3):529-540. 10.1083/jcb.200612042, 2064848, 17664339.
22. Sahlender DA, Roberts RC, Arden SD, Spudich G, Taylor MJ, Luzio JP, Kendrick-Jones J, Buss F. Optineurin links myosin VI to the Golgi complex and is involved in Golgi organization and exocytosis. J Cell Biol 2005, 169(2):285-295. 10.1083/jcb.200501162, 2171882, 15837803.
23. Bond LM, Peden AA, Kendrick-Jones J, Sellers JR, Buss F. Myosin VI and its binding partner optineurin are involved in secretory vesicle fusion at the plasma membrane. Mol Biol Cell 2011, 22(1):54-65. 10.1091/mbc.E10-06-0553, 3016977, 21148290.
24. Buss F, Arden SD, Lindsay M, Luzio JP, Kendrick-Jones J. Myosin VI isoform localized to clathrin-coated vesicles with a role in clathrin-mediated endocytosis. EMBO J 2001, 20(14):3676-3684. 10.1093/emboj/20.14.3676, 125554, 11447109.
25. Aschenbrenner L, Naccache SN, Hasson T. Uncoated endocytic vesicles require the unconventional myosin, Myo6, for rapid transport through actin barriers. Mol Biol Cell 2004, 15(5):2253-2263. 10.1091/mbc.E04-01-0002, 404020, 15004223.
26. Puri C. Loss of myosin VI no insert isoform (NoI) induces a defect in clathrin-mediated endocytosis and leads to caveolar endocytosis of transferrin receptor. J Biol Chem 2009, 284(50):34998-35014. 10.1074/jbc.M109.012328, 2787362, 19840950.
27. Park H, Ramamurthy B, Travaglia M, Safer D, Chen LQ, Franzini-Armstrong C, Selvin PR, Sweeney HL. Full-length myosin VI dimerizes and moves processively along actin filaments upon monomer clustering. Mol Cell 2006, 21(3):331-336. 10.1016/j.molcel.2005.12.015, 16455488.
28. Osterweil E, Wells DG, Mooseker MS. A role for myosin VI in postsynaptic structure and glutamate receptor endocytosis. J Cell Biol 2005, 168(2):329-338. 10.1083/jcb.200410091, 2171578, 15657400.
29. Yano H, Ninan I, Zhang H, Milner TA, Arancio O, Chao MV. BDNF-mediated neurotransmission relies upon a myosin VI motor complex. Nat Neurosci 2006, 9(8):1009-1018. 10.1038/nn1730, 16819522.
30. Erben V, Waldhuber M, Langer D, Fetka I, Jansen RP, Petritsch C. Asymmetric localization of the adaptor protein Miranda in neuroblasts is achieved by diffusion and sequential interaction of Myosin II and VI. J Cell Sci 2008, 121(Pt 9):1403-1414.
31. Peyre JB, Seabrooke S, Randlett O, Kisiel M, Aigaki T, Stewart BA. Interaction of cytoskeleton genes with NSF2-induced neuromuscular junction overgrowth. Genesis 2006, 44(12):595-600. 10.1002/dvg.20254, 17139674.
32. Morrison JK, Miller KG. Genetic characterization of the Drosophila jaguar322 mutant reveals that complete myosin VI loss of function is not lethal. Genetics 2008, 179(1):711-716. 10.1534/genetics.107.085969, 2390649, 18493084.
33. Sokolowski MB, Hansell KP. The foraging locus: behavioral tests for normal muscle movement in rover and sitter Drosophila melanogaster larvae. Genetica 1992, 85(3):205-209. 10.1007/BF00132272, 1521800.
34. Millo H, Bownes M. The expression pattern and cellular localisation of Myosin VI during the Drosophila melanogaster life cycle. Gene Expr Patterns 2007, 7(4):501-510. 10.1016/j.modgep.2006.10.008, 17185045.
35. Atwood HL, Govind CK, Wu CF. Differential ultrastructure of synaptic terminals on ventral longitudinal abdominal muscles in Drosophila larvae. J Neurobiol 1993, 24(8):1008-1024. 10.1002/neu.480240803, 8409966.
36. Stimson DT, Estes PS, Rao S, Krishnan KS, Kelly LE, Ramaswami M. Drosophila stoned proteins regulate the rate and fidelity of synaptic vesicle internalization. J Neurosci 2001, 21(9):3034-3044.
37. Rodesch CK, Broadie K. Genetic studies in Drosophila: vesicle pools and cytoskeleton-based regulation of synaptic transmission. Neuroreport 2000, 11(18):R45-53. 10.1097/00001756-200012180-00002, 11192639.
38. Zucker RS. Calcium- and activity-dependent synaptic plasticity. Curr Opin Neurobiol 1999, 9(3):305-313. 10.1016/S0959-4388(99)80045-2, 10395573.
39. Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Physiol 2002, 64:355-405. 10.1146/annurev.physiol.64.092501.114547, 11826273.
40. Zucker RS, Delaney KR, Mulkey R, Tank DW. Presynaptic calcium in transmitter release and posttetanic potentiation. Ann N Y Acad Sci 1991, 635:191-207. 10.1111/j.1749-6632.1991.tb36492.x, 1683751.
41. Hoang B, Chiba A. Single-cell analysis of Drosophila larval neuromuscular synapses. Dev Biol 2001, 229(1):55-70. 10.1006/dbio.2000.9983, 11133154.
42. Zhang B. Genetic and molecular analysis of synaptic vesicle recycling in Drosophila. J Neurocytol 2003, 32(5-8):567-589.
43. Akbergenova Y, Bykhovskaia M. Synapsin maintains the reserve vesicle pool and spatial segregation of the recycling pool in Drosophila presynaptic boutons. Brain Res 2007, 1178:52-64.
44. Akbergenova Y, Bykhovskaia M. Synapsin regulates vesicle organization and activity-dependent recycling at Drosophila motor boutons. Neuroscience 2010, 170(2):441-452. 10.1016/j.neuroscience.2010.07.021, 20638447.
45. Pawson C, Eaton BA, Davis GW. Formin-dependent synaptic growth: evidence that Dlar signals via Diaphanous to modulate synaptic actin and dynamic pioneer microtubules. J Neurosci 2008, 28(44):11111-11123. 10.1523/JNEUROSCI.0833-08.2008, 2654187, 18971454.
46. Mermall V, Miller KG. The 95F unconventional myosin is required for proper organization of the Drosophila syncytial blastoderm. J Cell Biol 1995, 129(6):1575-1588. 10.1083/jcb.129.6.1575, 2291172, 7790355.
47. Kuromi H, Kidokoro Y. Two distinct pools of synaptic vesicles in single presynaptic boutons in a temperature-sensitive Drosophila mutant, shibire. Neuron 1998, 20(5):917-925. 10.1016/S0896-6273(00)80473-0, 9620696.
48. Rizzoli SO, Betz WJ. Synaptic vesicle pools. Nat Rev Neurosci 2005, 6(1):57-69. 10.1038/nrn1583, 15611727.
49. Delgado R, Maureira C, Oliva C, Kidokoro Y, Labarca P. Size of vesicle pools, rates of mobilization, and recycling at neuromuscular synapses of a Drosophila mutant, shibire. Neuron 2000, 28(3):941-953. 10.1016/S0896-6273(00)00165-3, 11163278.
50. Kuromi H, Kidokoro Y. Tetanic stimulation recruits vesicles from reserve pool via a cAMP-mediated process in Drosophila synapses. Neuron 2000, 27(1):133-143. 10.1016/S0896-6273(00)00015-5, 10939337.
51. Stewart BA, McLean JR. Population density regulates Drosophila synaptic morphology in a Fasciclin-II-dependent manner. J Neurobiol 2004, 61(3):392-399. 10.1002/neu.20096, 15490479.
52. Dickman DK, Horne JA, Meinertzhagen IA, Schwarz TL. A slowed classical pathway rather than kiss-and-run mediates endocytosis at synapses lacking synaptojanin and endophilin. Cell 2005, 123(3):521-533. 10.1016/j.cell.2005.09.026, 16269341.
53. 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. Eps15 and Dap160 control synaptic vesicle membrane retrieval and synapse development. J Cell Biol 2007, 178(2):309-322. 10.1083/jcb.200701030, 2064449, 17620409.
54. Sambrook J. Molecular cloning: a laboratory manual 2001, Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press, 3.
55. Pereira HS, MacDonald DE, Hilliker AJ, Sokolowski MB. Chaser (Csr), a new gene affecting larval foraging behavior in Drosophila melanogaster. Genetics 1995, 141(1):263-270. 1206725, 8536975.
56. Stewart BA, Mohtashami M, Rivlin P, Deitcher DL, Trimble WS, Boulianne GL. Dominant-negative NSF2 disrupts the structure and function of Drosophila neuromuscular synapses. J Neurobiol 2002, 51(4):261-271. 10.1002/neu.10059, 12150502.
57. Stewart BA, Atwood HL, Renger JJ, Wang J, Wu CF. Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J Comp Physiol A 1994, 175(2):179-191. 10.1007/BF00215114, 8071894.
58. Seabrooke S, Stewart BA. Moesin helps to restrain synaptic growth at the Drosophila neuromuscular junction. Dev Neurobiol 2008, 68(3):379-391. 10.1002/dneu.20595, 18161855.
59. Sullivan W, Ashburner M, Hawley RS. Drosophila protocols 2000, Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press.