Morphological and functional effects of altered cysteine string protein at the Drosophila larval neuromuscular junction

Synapse

Volumn 61, Issue 1, 2007, Pages 1-16

  Dawson Scully, Ken ^a   Lin, Yongqi ^b   Imad, Mays ^b   Zhang, Jinhui ^b   Marin, Leo ^c   Horne, Jane A ^d   Meinertzhagen, Ian A ^d   Karunanithi, Shanker ^b   Zinsmaier, Konrad E ^b   Atwood, Harold L ^c  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF ARIZONA   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Active zone; CSP; Hsp70; Nerve terminal growth; Neurotransmitter release; Reserve pool; Synaptic growth; Synaptic vesicle; Vesicle trafficking

Indexed keywords

CYSTEINE STRING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTHROPOD LARVA; ARTICLE; CONTROLLED STUDY; CYTOPLASM VESICLE; DROSOPHILA; EVOKED RESPONSE; GENE CLUSTER; GENE MUTATION; MORPHOLOGY; MOTONEURON; NERVE DEGENERATION; NEUROMUSCULAR SYNAPSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; ROOM TEMPERATURE; SYNAPSE VESICLE; TEMPERATURE MEASUREMENT;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EVOKED POTENTIALS; LARVA; NERVE TISSUE PROTEINS; NEUROMUSCULAR JUNCTION; NEUROTRANSMITTER AGENTS; PRESYNAPTIC TERMINALS; SYNAPSES; SYNAPTIC VESICLES;

EID: 33845519197     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.20335     Document Type: Article

References (61)

1. Arnold C, Reisch N, Leibold C, Becker S, Pruefert K, Sautter K, Palm D, Jatzke S, Buchner S, Buchner E. 2004. Structure-function analysis of the cysteine string protein in Drosophila: Cysteine string, linker and C terminus. J Exp Biol 207:1323-1334.
2. Atwood HL, Karunanithi S, Georgiou J, Charlton MP. 1997. Strength of synaptic transmission at neuromuscular junctions of crustaceans and insects in relation to calcium entry. Invert Neurosci 3:81-87.
3. Atwood HL, Wojtowicz JM. 1999. Silent synapses in neural plasticity: Current evidence. Learn Mem 6:542-571.
4. Atwood HL, Govind CK, Wu CF. 1993. Differential ultrastructure of synaptic terminals on ventral longitudinal abdominal muscles in Drosophila larvae. J Neurobiol 24:1008-1024.
5. 2+-triggered exocytosis. J Neurophysiol 94:1888-1903.
6. Braun J, Wilbanks SM, Scheller RH. 1996. The cysteine string secretory vesicle protein activates Hsc70 ATPase. J Biol Chem 271:25989-25993.
7. Bronk P, Wenneger JJ, Dawson-Scully K, Guo X, Hong S, Atwood HL, Zinsmaier KE. 2001. Drosophila Hsc70-4 (Hsc4) is critical for neurotransmitter exocytosis. Neuron 30:475-488.
8. Bronk P, Nie Z, Klose MK, Dawson-Scully K, Zhang J, Robertson RM, Atwood HL, Zinsmaier KE. 2005. The multiple functions of cysteine-string protein analyzed at Drosophila nerve terminals. J Neurosci 25:2204-2214.
9. Brown H, Larsson O, Branstrom R, Yang SN, Leibiger B, Leibiger I, Fried G, Moede T, Deeney JT, Brown GR, Jacobsson G, Rhodes CJ, Braun JE, Scheller RH, Corkey BE, Berggren PO, Meister B. 1998. Cysteine string protein (CSP) is an insulin secretory granule-associated protein regulating β-cell exocytosis. EMBO J 17:5048-5058.
10. Buchner E, Gundersen CB. 1997. The DnaJ-like cysteine string protein and exocytotic neurotransmitter release. Trends Neurosci 20: 223-227.
11. Chamberlain LH, Burgoyne RD. 1997a. The molecular chaperone function of the secretory vesicle cysteine string proteins. J Biol Chem 272:31420-31426.
12. Chamberlain LH, Burgoyne RD. 1997b. Activation of the ATPase activity of heat-shock proteins Hsc70/Hsp70 by cysteine-string protein. Biochem J 322:853-858.
13. Chamberlain LH, Burgoyne RD. 1998. Cysteine string protein functions directly in regulated exocytosis. Mol Biol Cell 9:2259-2267.
14. Chamberlain LH, Burgoyne RD. 2000. Cysteine string protein: The chaperone at the synapse. J Neurochem 74:1781-1789.
15. Chang H, Ciani S, Kidokoro Y. 1994. Ion permeation properties of the glutamate receptor channel in cultured embryonic Drosophila myotubes. J Physiol 476:1-16.
16. Chen S, Zheng X, Schulze KL, Morris T, Bellen H, Stanley EF. 2002. Enhancement of presynaptic calcium current by cysteine string protein. J Physiol 538:383-389.
17. Choi JC, Park D, Griffith LC. 2004. Electrophysiological and morphologi-cal characterization of identified motor neurons in the Drosophila third instar larva central nervous system. J Neurophysiol 91:2353-2365.
18. Davis GW, Goodman CS. 1998. Genetic analysis of synaptic development and plasticity: Homeostatic regulation of synaptic efficacy. Curr Opin Neurobiol 8:149-156.
19. Davis GW, Schuster CM, Goodman CS. 1996. Genetic dissection of structural and functional components of synaptic plasticity. III. CREB is necessary for presynaptic functional plasticity. Neuron 17:669-679.
20. Davis GW, DiAntonio A, Petersen SA, Goodman CS. 1998. Postsynaptic PKA controls quantal size and reveals a retrograde signal that regulates presynaptic transmitter release in Drosophila. Neuron 20:305-315.
21. Dawson-Scully K, Bronk P, Atwood HL, Zinsmaier KE. 2000. Cysteinestring protein increases the calcium sensitivity of neurotransmitter exocytosis in Drosophila. J Neurosci 20:6039-6047.
22. del Castillo J, Katz B. 1954. Quantal components of the end-plate potential. J Physiol 411:179-194.
23. Eberle KK, Zinsmaier KE, Buchner S, Jenni M, Arnold C, Leibold C, Reisch D, Walter N, Hafen E, Hofbauer A, Pflugfelder GO, Büchner E. 1998. Wide distribution of cysteine string protein in Drosophila tissues revealed by targeted mutagenesis. Cell Tissue Res 294:203-217.
24. Evans GJ, Morgan A. 2002. Phosphorylation-dependent interaction of the synaptic vesicle proteins cysteine string protein and synaptotagmin I. Biochem J 364:343-347.
25. Evans GJ, Wilkinson MC, Graham ME, Turner KM, Chamberlain LH, Burgoyne RD, Morgan A. 2001. Phosphorylation of cysteine string protein by protein kinase A. Implications for the modulation of exocytosis. J Biol Chem 276:47877-47885.
26. Evans GJ, Morgan A, Burgoyne RD. 2003. Tying everything together: The multiple roles of cysteine string protein (CSP) in regulated exocytosis. Traffic 4:653-659.
27. Fernandez-Chacon R, Wolfel M, Nishimune H, Tabares L, Schmitz F, Castellano-Munoz M, Rosenmund C, Montesinos ML, Sanes JR, Schneggenburger R, Sudhof TC. 2004. The synaptic vesicle protein CSP áprevents presynaptic degeneration. Neuron 42:237-251.
28. Graham ME, Burgoyne RD. 2000. Comparison of cysteine string protein (Csp) and mutant α-SNAP overexpression reveals a role for csp in late steps of membrane fusion in dense-core granule exocytosis in adrenal chromaffin cells. J Neurosci 20:1281-1289.
29. Guerrero G, Reiff 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.
30. Gundersen CB, Umbach JA. 1992. Suppression cloning of the cDNA for a candidate subunit of a presynaptic calcium channel. Neuron 9:527-537.
31. Heckmann M, Adelsberger H, Dudel J. 1997. Evoked transmitter release at neuromuscular junctions in wild type and cysteine string protein null mutant larvae of Drosophila. Neurosci Lett 228:167-170.
32. Hoang B, Chiba A. 2001. Single-cell analysis of Drosophila larval neuromuscular synapses. Dev Biol 229:55-70.
33. Jia XX, Gorczyca M, Budnik V. 1993. Ultrastructure of neuromuscular junctions in Drosophila: Comparison of wild type and mutants with increased excitability. J Neurobiol 24:1025-1044.
34. Karunanithi S, Marin L, Wong K, Atwood HL. 2002. Quantal size and variation determined by vesicle size in normal and mutant Drosophila glutamatergic synapses. J Neurosci 22:10267-10276.
35. Kidokoro Y, Kuromi H, Delgado R, Maureira C, Oliva C, Labarca P. 2004. Synaptic vesicle pools and plasticity of synaptic transmission at the Drosophila synapse. Brain Res Rev 47:18-32.
36. Koenig JH, Yamaoka K, Ikeda K. 1993. Calcium-induced translocation of synaptic vesicles to the active site. J Neurosci 13:2313-2322.
37. Kurdyak P, Atwood HL, Stewart BA, Wu CF. 1994. Differential physiology and morphology of motor axons to ventral longitudinal muscles in larval Drosophila. J Comp Neurol 350:463-472.
38. Kuromi H, Kidokoro Y. 2003. Two synaptic vesicle pools, vesicle recruitment and replenishment of pools at the Drosophila neuromuscular junction. J Neurocytol 32:551-565.
39. Kuromi H, Kidokoro Y. 2005. Exocytosis and endocytosis of synaptic vesicles and functional roles of vesicle pools: Lessons from the Drosophila neuromuscular junction. Neuroscientist 11:138-147.
40. Lnenicka GA, Keshishian H. 2000. Identified motor terminals in Drosophila larvae show distinct differences in morphology and physiology. J Neurobiol 43:186-197.
41. Macleod GT, Hegström-Wojtowicz M, Charlton MP, Atwood HL. 2002. Fast calcium signals in Drosophila motor neuron terminals. J Neurophysiol 88:2659-2663.
42. Magga JM, Jarvis SE, Arnot MI, Zamponi GW, Braun JE. 2000. Cysteine string protein regulates G protein modulation of N-type calcium channels. Neuron 28:195-204.
43. Natochin M, Campbell TN, Barren B, Miller LC, Hameed S, Artemyev NO, Braun JE. 2005. Characterization of the G α(s) regulator cysteine string protein. J Biol Chem 280:30236-30241.
44. Nie Z, Ranjan R, Wenniger JJ, Hong SN, Bronk P, Zinsmaier KE. 1999. Overexpression of cysteine string protein in Drosophila reveals interactions with syntaxin. J Neurosci 19:10270-10279.
45. Ranjan R, Bronk P, Zinsmaier KE. 1998. Cysteine string protein is required for calcium secretion coupling of evoked neurotransmission in Drosophila but not for vesicle recycling. J Neurosci 18:956-964.
46. Sakisaka T, Meerlo T, Matteson J, Plutner H, Balch WE. 2002. Rab-α GDI activity is regulated by a Hsp90 chaperone complex. EMBO J 21: 6125-6135.
47. Schikorski T, Stevens CF. 2001. Morphological correlates of functionally defined synaptic vesicle populations. Nat Neurosci 4:391-395.
48. Song W, Ranjan R, Dawson-Scully K, Bronk P, Marin L, Seroude L, Yi-Jyun L, Nie Z, Atwood HL, Benzer S, Zinsmaier KE. 2002. Pre-synaptic Methuselah regulates synaptie vesicle trafficking at Drosophila neuromuscular junctions. Neuron 36:105-119.
49. Stewart BA, Atwood HL, Renger JJ, Wang J, Wu CF. 1994. Improved stability of Drosaphila larval neuromuscular preparations in haemolymph-like physiological solutions. J Comp Physiol 175:179-191.
50. Tobaben S, Thakur P, Fernandez-Chacon R, Sudhdf TC, Rettig J, Stahl B. 2001. A trimeric protein complex functions as a synaptie chaperone machine. Neuron 31:987-999.
51. Tobaben S, Varoqueaux F, Brose N, Stahl B, Meyer G. 2003. A brain-specific isoform of small glutamine-rich tetratricopeptide repeat-containing protein binds to Hsc70 and the cvsteine string protein. J Biol Chem 78:38376-38383.
52. 2+-dependent secretion of neurotransmitter at Drosophila neuromuscular junctions: J Neurosei 17: 7203-7209.
53. Umbach JA, Zinsmaier KE, Eberle KK, Buchner E, Benzer S, Gundersen CB. 1994. Presynaptic dysfunction in Drosophila csp mutants. Neuron 13:899-907.
54. Umbach JA, Saitoe M, Kidokoro Y, Gunderson CB. 1998. Attenuated influx of calcium ions at nerve endings of csp and shibire mutant Drosophila. J Neurosci 18:3233-3240.
55. Wu MN, Fergestad T, Lloyd TE, He Y, Broadie K, Bellen HJ. 1999. Syntaxin IA interacts with multiple exocytic proteins to regulate neurotransmitter release in vivo. Neuron 23:593-605.
56. Wucherpfennig T, Wilsch-Brauninger M, Gonzalez-Gaitan M. 2003. Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J Cell Biol 161:609-624.
57. Zhang H, Kelley WL, Chamberlain LH, Burgoyne RD, Wollheim CB, Lang J. 1998. Cysteine-string proteins regulate exocytosis of insulin independent from transmembrane ion fluxes. FEBS Lett 437: 267-272.
58. Zhang H, Kelley WL, Chamberlain LH, Burgoyne RD, Lang J. 1999. Mutational analysis of cysteine-string protein function in insulin exocytosis. J Cell Sci 112:1345-1351.
59. Zinsmaier KE. 1997. Cysteine string proteins. In: Gething MJ, editor. Guidebook to molecular chaperones and protein folding catalysts. Oxford University Press, p 115-117.
60. Zinsmaier KE, Bronk P. 2001. Molecular chaperones and the regulation of neurotransmitter exocytosis. Biochem Pharmacol 62:1-11.
61. Zinsmaier KE, Eberle KK, Buchner E, Walter N, Benzer S. 1994. Paralysis and early death in cysteine string protein mutants of Drosophila. Science 263:977-980.