Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions

Neuron

Volumn 47, Issue 3, 2005, Pages 365-378

  Verstreken, Patrik ^a   Ly, Cindy V ^a   Venken, Koen J T ^a   Koh, Tong Wey ^a   Zhou, Yi ^a   Bellen, Hugo J ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM; CYCLIC AMP DEPENDENT PROTEIN KINASE; DYNAMIN I;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA; ENDOCYTOBIOSIS; EXOCYTOSIS; MITOCHONDRION; MOBILIZATION; MUTATION; NERVE STIMULATION; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; REFLEX RECRUITMENT; SYNAPSE; SYNAPSE VESICLE;

ANIMALS; CALCIUM; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOSKELETAL PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; ELECTRIC STIMULATION; ENDOCYTOSIS; GTP PHOSPHOHYDROLASES; GTP-BINDING PROTEINS; LARVA; MEMBRANE PROTEINS; MITOCHONDRIA; MUTATION; MYOSIN LIGHT CHAINS; MYOSINS; NEUROMUSCULAR JUNCTION; NEUROPEPTIDES; NEUROTRANSMITTER AGENTS; PRESYNAPTIC TERMINALS; SYNAPSES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; TISSUE DISTRIBUTION; VESICULAR TRANSPORT PROTEINS;

EID: 23044506102     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2005.06.018     Document Type: Article

References (73)

1. T. Aiuchi, M. Matsunaga, K. Nakaya, and Y. Nakamura Effects of probes of membrane potential on metabolism in synaptosomes Biochim. Biophys. Acta 843 1985 20 24
2. E. Alnaes, and R. Rahamimoff On the role of mitochondria in transmitter release from motor nerve terminals J. Physiol. 248 1975 285 306
3. H.J. Bellen, and V. Budnik The neuromuscular junction W. Sullivan M. Ashburner R.S. Hawley Drosophila Protocols 2000 CSHL Press Cold Spring Harbor, NY 175 199
4. H.J. Bellen, R.W. Levis, G. Liao, Y. He, J.W. Carlson, G. Tsang, M. Evans-Holm, P.R. Hiesinger, K.L. Schulze, and G.M. Rubin The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes Genetics 167 2004 761 781
5. B. Billups, and I.D. Forsythe Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses J. Neurosci. 22 2002 5840 5847
6. R. Bouchard, R. Pattarini, and J.D. Geiger Presence and functional significance of presynaptic ryanodine receptors Prog. Neurobiol. 69 2003 391 418
7. A.R. Bresnick Molecular mechanisms of nonmuscle myosin-II regulation Curr. Opin. Cell Biol. 11 1999 26 33
8. S.L. Budd, and D.G. Nicholls Mitochondria, calcium regulation, and acute glutamate excitotoxicity in cultured cerebellar granule cells J. Neurochem. 67 1996 2282 2291
9. M.A. Calupca, C. Prior, L.A. Merriam, G.M. Hendricks, and R.L. Parsons Presynaptic function is altered in snake K+-depolarized motor nerve terminals containing compromised mitochondria J. Physiol. 532 2001 217 227
10. J.F. Collard, F. Cote, and J.P. Julien Defective axonal transport in a transgenic mouse model of amyotrophic lateral sclerosis Nature 375 1995 61 64
11. D.L. Court, S. Swaminathan, D. Yu, H. Wilson, T. Baker, M. Bubunenko, J. Sawitzke, and S.K. Sharan Mini-lambda: a tractable system for chromosome and BAC engineering Gene 315 2003 63 69
12. G. David, and E.F. Barrett Mitochondrial Ca2+ uptake prevents desynchronization of quantal release and minimizes depletion during repetitive stimulation of mouse motor nerve terminals J. Physiol. 548 2003 425 438
13. R. Delgado, C. Maureira, C. Oliva, Y. Kidokoro, and P. Labarca Size of vesicle pools, rates of mobilization, and recycling at neuromuscular synapses of a Drosophila mutant, shibire Neuron 28 2000 941 953
14. J. Finsterer Mitochondriopathies Eur. J. Neurol. 11 2004 163 186
15. D.D. Friel, and R.W. Tsien An FCCP-sensitive Ca2+ store in bullfrog sympathetic neurons and its participation in stimulus-evoked changes in [Ca2+]i J. Neurosci. 14 1994 4007 4024
16. D. Gitler, Y. Takagishi, J. Feng, Y. Ren, R.M. Rodriguiz, W.C. Wetsel, P. Greengard, and G.J. Augustine Different presynaptic roles of synapsins at excitatory and inhibitory synapses J. Neurosci. 24 2004 11368 11380
17. D.R. Green, and G. Kroemer The pathophysiology of mitochondrial cell death Science 305 2004 626 629
18. X. Guo, G.T. Macleod, A. Wellington, F. Hu, S. Panchumarthi, M. Schoenfield, L. Marin, M.P. Charlton, H.L. Atwood, and K.E. Zinsmaier The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses this issue Neuron 47 2005 379 393
19. J. Herrington, Y.B. Park, D.F. Babcock, and B. Hille Dominant role of mitochondria in clearance of large Ca2+ loads from rat adrenal chromaffin cells Neuron 16 1996 219 228
20. D.D. Hurd, and W.M. Saxton Kinesin mutations cause motor neuron disease phenotypes by disrupting fast axonal transport in Drosophila Genetics 144 1996 1075 1085
21. J.R. Jensen, and V. Rehder FCCP releases Ca2+ from a non-mitochondrial store in an identified Helisoma neuron Brain Res. 551 1991 311 314
22. L.V. Johnson, M.L. Walsh, and L.B. Chen Localization of mitochondria in living cells with rhodamine 123 Proc. Natl. Acad. Sci. USA 77 1980 990 994
23. K.E. Kamm, and J.T. Stull Dedicated myosin light chain kinases with diverse cellular functions J. Biol. Chem. 276 2001 4527 4530
24. O. Kann, R. Kovacs, and U. Heinemann Metabotropic receptor-mediated Ca2+ signaling elevates mitochondrial Ca2+ and stimulates oxidative metabolism in hippocampal slice cultures J. Neurophysiol. 90 2003 613 621
25. Y. Kidokoro, H. Kuromi, R. Delgado, C. Maureira, C. Oliva, and P. Labarca Synaptic vesicle pools and plasticity of synaptic transmission at the Drosophila synapse Brain Res. Brain Res. Rev. 47 2004 18 32
26. T.W. Koh, P. Verstreken, and H.J. Bellen Dap160/intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis Neuron 43 2004 193 205
27. H. Kuromi, and Y. Kidokoro Two distinct pools of synaptic vesicles in single presynaptic boutons in a temperature-sensitive Drosophila mutant, shibire Neuron 20 1998 917 925
28. H. Kuromi, and Y. Kidokoro Tetanic stimulation recruits vesicles from reserve pool via a cAMP-mediated process in Drosophila synapses Neuron 27 2000 133 143
29. H. Kuromi, and Y. Kidokoro Selective replenishment of two vesicle pools depends on the source of Ca2+ at the Drosophila synapse Neuron 35 2002 333 343
30. A.M. Labrousse, M.D. Zappaterra, D.A. Rube, and A.M. van der Bliek C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane Mol. Cell 4 1999 815 826
31. Z. Li, K. Okamoto, Y. Hayashi, and M. Sheng The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses Cell 119 2004 873 887
32. J.T. Littleton, and H.J. Bellen Genetic and phenotypic analysis of thirteen essential genes in cytological interval 22F1-2; 23B1-2 reveals novel genes required for neural development in Drosophila Genetics 138 1994 111 123
33. J.T. Littleton, M. Stern, K. Schulze, M. Perin, and H.J. Bellen Mutational analysis of Drosophila synaptotagmin demonstrates its essential role in Ca(2+)-activated neurotransmitter release Cell 74 1993 1125 1134
34. P. Liu, N.A. Jenkins, and N.G. Copeland A highly efficient recombineering-based method for generating conditional knockout mutations Genome Res. 13 2003 476 484
35. G.T. Macleod, M. Hegstrom-Wojtowicz, M.P. Charlton, and H.L. Atwood Fast calcium signals in Drosophila motor neuron terminals J. Neurophysiol. 88 2002 2659 2663
36. M. Makishima, Y. Honma, M. Hozumi, K. Sampi, M. Hattori, and K. Motoyoshi Induction of differentiation of human leukemia cells by inhibitors of myosin light chain kinase FEBS Lett. 287 1991 175 177
37. C.K. Mathews, and K.E. Van Holde Biochemistry Second Edition 1996 The Benjamin/Cummings Publishing Company Menlo Park, CA
38. K. Medler, and E.L. Gleason Mitochondrial Ca(2+) buffering regulates synaptic transmission between retinal amacrine cells J. Neurophysiol. 87 2002 1426 1439
39. S. Mochida, H. Kobayashi, Y. Matsuda, Y. Yuda, K. Muramoto, and Y. Nonomura Myosin II is involved in transmitter release at synapses formed between rat sympathetic neurons in culture Neuron 13 1994 1131 1142
40. J. Molgo, and M. Pecot-Dechavassine Effects of carbonyl cyanide m-chlorophenylhydrazone on quantal transmitter release and ultrastructure of frog motor nerve terminals Neuroscience 24 1988 695 708
41. M.G. Mozhayeva, M.F. Matos, X. Liu, and E.T. Kavalali Minimum essential factors required for vesicle mobilization at hippocampal synapses J. Neurosci. 24 2004 1680 1688
42. V.N. Murthy, and P. De Camilli Cell biology of the presynaptic terminal Annu. Rev. Neurosci. 26 2003 701 728
43. T.P. Newsome, B. Asling, and B.J. Dickson Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics Development 127 2000 851 860
44. P.V. Nguyen, L. Marin, and H.L. Atwood Synaptic physiology and mitochondrial function in crayfish tonic and phasic motor neurons J. Neurophysiol. 78 1997 281 294
45. D.G. Nicholls, and S.L. Budd Mitochondria and neuronal survival Physiol. Rev. 80 2000 315 360
46. D. Otsuga, B.R. Keegan, E. Brisch, J.W. Thatcher, G.J. Hermann, W. Bleazard, and J.M. Shaw The dynamin-related GTPase, Dnm1p, controls mitochondrial morphology in yeast J. Cell Biol. 143 1998 333 349
47. A.B. Parekh Mitochondrial regulation of intracellular Ca2+ signaling: more than just simple Ca2+ buffers News Physiol. Sci. 18 2003 252 256
48. A.L. Parks, K.R. Cook, M. Belvin, N.A. Dompe, R. Fawcett, K. Huppert, L.R. Tan, C.G. Winter, K.P. Bogart, and J.E. Deal Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome Nat. Genet. 36 2004 288 292
49. L. Polo-Parada, C.M. Bose, and L.T. Landmesser Alterations in transmission, vesicle dynamics, and transmitter release machinery at NCAM-deficient neuromuscular junctions Neuron 32 2001 815 828
50. L. Polo-Parada, F. Plattner, C. Bose, and L.T. Landmesser NCAM 180 acting via a conserved C-terminal domain and MLCK is essential for effective transmission with repetitive stimulation Neuron 46 2005 917 931
51. G.J. Praefcke, and H.T. McMahon The dynamin superfamily: universal membrane tubulation and fission molecules? Nat. Rev. Mol. Cell Biol. 5 2004 133 147
52. R. Prekeris, and D.M. Terrian Brain myosin V is a synaptic vesicle-associated motor protein: evidence for a Ca2+-dependent interaction with the synaptobrevin-synaptophysin complex J. Cell Biol. 137 1997 1589 1601
53. M. Reers, T.W. Smith, and L.B. Chen J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential Biochemistry 30 1991 4480 4486
54. R. Rikhy, M. Ramaswami, and K.S. Krishnan A temperature-sensitive allele of Drosophila sesB reveals acute functions for the mitochondrial adenine nucleotide translocase in synaptic transmission and dynamin regulation Genetics 165 2003 1243 1253
55. S.O. Rizzoli, and W.J. Betz Synaptic vesicle pools Nat. Rev. Neurosci. 6 2005 57 69
56. R. Rizzuto, P. Pinton, W. Carrington, F.S. Fay, K.E. Fogarty, L.M. Lifshitz, R.A. Tuft, and T. Pozzan Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses Science 280 1998 1763 1766
57. D.A. Rube, and A.M. van der Bliek Mitochondrial morphology is dynamic and varied Mol. Cell. Biochem. 256-257 2004 331 339
58. T.A. Ryan Inhibitors of myosin light chain kinase block synaptic vesicle pool mobilization during action potential firing J. Neurosci. 19 1999 1317 1323
59. M. Saitoh, T. Ishikawa, S. Matsushima, M. Naka, and H. Hidaka Selective inhibition of catalytic activity of smooth muscle myosin light chain kinase J. Biol. Chem. 262 1987 7796 7801
60. M. Sandberg, E. Butt, C. Nolte, L. Fischer, M. Halbrugge, J. Beltman, T. Jahnsen, H.G. Genieser, B. Jastorff, and U. Walter Characterization of Sp-5,6-dichloro-1-beta-D-ribofuranosylbenzimidazole-3′, 5′-monophosphorothioate (Sp-5,6-DCl-cBiMPS) as a potent and specific activator of cyclic-AMP-dependent protein kinase in cell extracts and intact cells Biochem. J. 279 1991 521 527
61. S. Sanyal, C. Consoulas, H. Kuromi, A. Basole, L. Mukai, Y. Kidokoro, K.S. Krishnan, and M. Ramaswami Analysis of conditional paralytic mutants in Drosophila SERCA reveals novel mechanisms for regulating membrane excitability Genetics 24 2004 4518 4529
62. E. Smirnova, L. Griparic, D.L. Shurland, and A.M. van der Bliek Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells Mol. Biol. Cell 12 2001 2245 2256
63. R.S. Stowers, L.J. Megeath, J. Gorska-Andrzejak, I.A. Meinertzhagen, and T.L. Schwarz Axonal transport of mitochondria to synapses depends on milton, a novel Drosophila protein Neuron 36 2002 1063 1077
64. J.D. Talbot, G. David, and E.F. Barrett Inhibition of mitochondrial Ca2+ uptake affects phasic release from motor terminals differently depending on external [Ca2+] J. Neurophysiol. 90 2003 491 502
65. Y. Tang, and R.S. Zucker Mitochondrial involvement in post-tetanic potentiation of synaptic transmission Neuron 18 1997 483 491
66. N. Trotta, C.K. Rodesch, T. Fergestad, and K. Broadie Cellular bases of activity-dependent paralysis in Drosophila stress-sensitive mutants J. Neurobiol. 60 2004 328 347
67. P. Verstreken, O. Kjaerulff, T.E. Lloyd, R. Atkinson, Y. Zhou, I.A. Meinertzhagen, and H.J. Bellen Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release Cell 109 2002 101 112
68. P. Verstreken, T.W. Koh, K.L. Schulze, R.G. Zhai, P.R. Hiesinger, Y. Zhou, S.Q. Mehta, Y. Cao, J. Roos, and H.J. Bellen Synaptojanin is recruited by endophilin to promote synaptic vesicle uncoating Neuron 40 2003 733 748
69. J.L. Werth, and S.A. Thayer Mitochondria buffer physiological calcium loads in cultured rat dorsal root ganglion neurons J. Neurosci. 14 1994 348 356
70. E. Yeh, K. Gustafson, and G.L. Boulianne Green fluorescent protein as a vital marker and reporter of gene expression in Drosophila Proc. Natl. Acad. Sci. USA. 92 1995 7036 7040
71. M. Yi, D. Weaver, and G. Hajnoczky Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit J. Cell Biol. 167 2004 661 672
72. J.E. Zengel, M.A. Sosa, R.E. Poage, and D.R. Mosier Role of intracellular Ca2+ in stimulation-induced increases in transmitter release at the frog neuromuscular junction J. Gen. Physiol. 104 1994 337 355
73. D. Zenisek, and G. Matthews The role of mitochondria in presynaptic calcium handling at a ribbon synapse Neuron 25 2000 229 237