Cysteine-string protein: The chaperone at the synapse

Journal of Neurochemistry

Volumn 74, Issue 5, 2000, Pages 1781-1789

  Chamberlain, Luke H ^a   Burgoyne, Robert D ^b  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Exocytosis; Neurotransmission; Secretion; Secretory granule; SNAREs; Synaptic vesicle

Indexed keywords

CALCIUM CHANNEL; CHAPERONE; CYSTEINE STRING PROTEIN; HEAT SHOCK PROTEIN 70; SYNAPTOBREVIN; SYNTAXIN;

EXOCYTOSIS; NEUROSECRETORY CELL; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN TARGETING; REVIEW; SYNAPSE;

AMINO ACID SEQUENCE; ANIMALS; DROSOPHILA; HSP40 HEAT-SHOCK PROTEINS; MEMBRANE PROTEINS; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; SYNAPSES; TISSUE DISTRIBUTION;

CAENORHABDITIS ELEGANS; MAMMALIA;

EID: 0034051803     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2000.0741781.x     Document Type: Review

References (81)

1. Bennett M. K. and Scheller R. H. (1993) The molecular machinery for secretion is conserved from yeast to neurons. Proc. Natl. Acad. Sci. USA 90, 2559-2563.
2. Bezprozvanny L., Scheller R. H., and Tsien R. W. (1995) Functional impact of syntaxin on gating of N-type and Q-type calcium channels. Nature 378, 623-626.
3. Braun J. E. A. and Scheller R. H. (1995) Cysteine string protein, a DnaJ family member, is present on diverse secretory vesicles. Neuropharmacology 34, 1361-1369.
4. Braun J. E. A., Wilbanks S. M., and Scheller R. H. (1996) The cysteine string secretory vesicle protein activates Hsc70 ATPase. J. Biol. Chem. 271, 25989-25993.
5. Broadie K., Prokop A., Bellen H. J., O'Kane C. J., Schulze K. L., and Sweeney S. T. (1995) Syntaxin and synaptobrevin function downstream of vesicle docking in Drosophila. Neuron 15, 663-673.
6. Brown H., Larsson O., Branstrom R., Yang S.-N., Leibiger B., Leibiger I., Fried G., Moede T., Deeney J. T., Brown G. R., Jacobsson G., Rhodes C. J., Braun J. E. A., Scheller R. H., Corkey B. E., Berggren P.-O., and Meister B. (1998) Cysteine string protein (CSP) is an insulin secretory granule-associated protein regulating β-cell exocytosis. EMBO J. 17, 5048-5058.
7. Bukau B. and Horwich A. L. (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92, 351-366.
8. 2+ and secretory vesicle dynamics. Trends Neurosci. 18, 191-196.
9. Burgoyne R. D. and Morgan A. (1998) Analysis of regulated exocytosis in adrenal chromaffin cells: insights into NSF/SNAP/SNARE function. Bioessays 20, 328-335.
10. Calakos N. and Scheller R. H. (1996) Synaptic vesicle biogenesis, docking and fusion, a molecular description. Physiol. Rev. 76, 1-29.
11. Caplan A. J., Cyr D. M., and Douglas M. G. (1993) Eukaryotic homologues of Escherichia coli dnaj: a diverse protein family that functions with hsp70 stress proteins. Mol. Biol. Cell 4, 555-563.
12. Chamberlain L. H. and Burgoyne R. D. (1996) Identification of a novel cysteine string protein variant and expression of cysteine string proteins in non-neuronal cells. J. Biol. Chem. 271, 7320-7323.
13. Chamberlain L. H. and Burgoyne R. D. (1997a) Activation of the ATPase activity of heat-shock proteins Hsc70/Hsp70 by cysteine string protein. Biochem. J. 322, 853-858.
14. Chamberlain L. H. and Burgoyne R. D. (1997b) The molecular chaperone function of the secretory vesicle cysteine string proteins. J. Biol. Chem. 272, 31420-31426.
15. Chamberlain L. H. and Burgoyne R. D. (1998a) Cysteine string protein functions directly in regulated exocytosis. Mol. Biol. Cell 9, 2259-2267.
16. Chamberlain L. H. and Burgoyne R. D. (1998b) The cysteine-string domain of the secretory vesicle cysteine-string protein is required for membrane targeting. Biochem. J. 335, 205-209.
17. Chamberlain L. H., Henry J., and Burgoyne R. D. (1996) Cysteine string proteins are associated with chromaffin granules. J. Biol. Chem. 271, 19514-19517.
18. Chappell T. G., Welch W. J., Schlossman D. M., Palter K. B., Schlesinger M. J., and Rothman J. E. (1986) Uncoating ATPase is a member of the 70 kilodalton family of stress proteins. Cell 45, 3-13.
19. Cheetham M. E. and Caplan A. V. (1998) Structure, function and evolution of DnaJ: conservation and adaptation of chaperone function. Cell Stress Chaperones 3, 28-36.
20. 2+ triggers massive exocytosis in Chinese hamster ovary cells. EMBO J. 15, 3787-3791.
21. Coppola T. and Gundersen C. B. (1996) Widespread expression of human cysteine string proteins. FEBS Lett. 391, 269-272.
22. Deitcher D. L., Ueda A., Stewart B. A., Burgess R. W., Kidokoro Y., and Schwarz T. L. (1998) Distinct requirements for evoked and spontaneous release of neurotransmitter are revealed by mutations in the Drosophila gene neuronal-synaptobrevin. J. Neurosci. 18, 2028-2039.
23. Eberle K. K., Zinsmaier K. E., Buchner S., Gruhn M., Jenni M., Arnold C., Leibold C., Reisch D., Walter N., Hafen E., Hofbauer A., Pflugfelder G. O., and Buchner E. (1998) Wide distribution of the cysteine string proteins in Drosophila tissues revealed by targeted mutagenesis. Cell Tissue Res. 294, 203-217.
24. Fasshauer D., Otto H., Eliason W. K., Jahn R., and Brunger A. T. (1997) Structural changes are associated with soluble N-ethylmaleimide-sensitive fusion protein attachment protein receptor complex formation. J. Biol. Chem. 272, 28036-28041.
25. Fernandez-Chacon R. and Südhof T. C. (1999) Genetics of synaptic vesicle function: toward the complete functional anatomy of an organelle. Annu. Rev. Physiol. 61, 753-776.
26. Gonzalo S. and Linder M. E. (1998) SNAP-25 palmitoylation and plasma membrane targeting require a functional secretory pathway. Mol. Biol. Cell 9, 585-597.
27. Graham M.E. and Burgoyne R. D. (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.
28. Gundersen C. B. and Umbach J. A. (1992) Suppression cloning of the cDNA for a candidate subunit of a presynaptic calcium channel. Neuron 9, 527-537.
29. Gundersen C. B., Mastrogiacomo A., Faull K., and Umbach J. A. (1994) Extensive lipidation of a Torpedo cysteine string protein. J. Biol. Chem. 269, 19197-19199.
30. Gundersen C. B., Mastrogiacomo A., and Umbach J. A. (1995) Cysteine-string proteins as templates for membrane fusion: models of synaptic vesicle exocytosis. J. Theor. Biol. 172, 269-277.
31. Hanson P. I., Heuser J. E., and Jahn R. (1997) Neurotransmitter release - four years of SNARE complexes. Curr. Opin. Neurobiol. 7, 310-315.
32. Hartl F.-U. (1996) Molecular chaperones in cellular protein folding. Nature 381, 571-580.
33. Hayashi T., McMahon H., Yamasaki S., Binz T., Hata Y., Südhof T. C., and Niemann H. (1994) Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly. EMBO J. 13, 5051-5061.
34. Heckmann M., Adelsberger H., and 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.
35. Kelley W. L. (1998) The J-domain family and the recruitment of chaperone power. Trends Biochem. Sci. 23, 222-227.
36. Kohan S. A., Pescatori M., Brecha N. C., Mastrogiacomo A., Umbach J. A., and Gundersen C. B. (1995) Cysteine string protein immunoreactivity in the nervous system and adrenal gland of the rat. J. Neurosci. 15, 6230-6238.
37. Kwon O. J., Kim C. M., Kim H., and Chin H. M. (1996) Differential expression of the alternatively spliced variants of the rat cysteine string protein. Mol. Biol. Cell 7, 2599.
38. Lang J. (1999) Molecular mechanisms and regulation of insulin exocytosis as a paradigm of endocrine secretion. Eur. J. Biochem. 259, 3-17.
39. 1A subunit of the P/Q-type calcium channel. J. Biol. Chem. 273, 13488-13492.
40. Littleton J. T., Chapman E. R., Kreber R., Garment M. B., Carbon S. D., and Ganetzky B. (1998) Temperature-sensitive paralytic mutations demonstrate that synaptic exocytosis requires SNARE complex assembly and disassembly. Neuron 21, 401-413.
41. Mastrogiacomo A. and Gundersen C. B. (1995) The nucleotide and deduced amino acid sequence of a rat cysteine string protein. Mol. Brain Res. 28, 12-18.
42. Mastrogiacomo A., Evans C. J., and Gundersen C. B. (1994a) Anti-peptide antibodies against a Torpedo cysteine-string protein. J. Neurochem. 62, 873-880.
43. 2+ channels. Science 263, 981-982.
44. Mastrogiacomo A., Kohan S. A., Whitelegge J. P., and Gundersen C. B. (1998a) Intrinsic membrane association of Drosophila cysteine string proteins. FEBS Lett 436, 85-91.
45. Mastrogiacomo A., Kornblum H. I., Umbach J. A., and Gundersen C. B. (1998b) A Xenopus cysteine string protein with a cysteine residue in the J domain. Biochim. Biophys. Acta 1401, 239-241.
46. Morales M., Ferrus A., and Martinez-Padron M. (1999) Presynaptic calcium-currents in normal and csp mutant Drosophila peptidergic terminals. Eur. J. Neurosci. 11, 1818-1826.
47. Nie Z., Ranjan R., Wenninger J. J., Hong S. N., Bronk P., and Zinsmaier K. E. (1999) Overexpression of cysteine-string proteins in Drosophila reveals interactions with syntaxin. J. Neurosci. 19, 10270-10279.
48. 2+ compound. J. Biol. Chem. 271, 17751-17754.
49. Ohki R., Kawamata T., Katoh Y., Hosoda F., and Ohki M. (1992) Excherichia coli dnaJ deletion mutation results in loss of stability of a positive regulator, CRP*. J. Biol. Chem. 267, 13180-13184.
50. Poage R. E., Meriney S. D., Gundersen C. B., and Umbach J. A. (1999) Antibodies against cysteine string proteins inhibit evoked neurotransmitter release at Xenopus neuromuscular junctions. J. Neuro-Physiol. 82, 50-59.
51. Pupier S., Leveque C., Marqueze B., Kataoka M., Takahashi M., and Saegar M. (1997) Cysteine string proteins are associated with secretory granules of the rat neurohypophysis. J. Neurosci. 17, 2722-2727.
52. Ranjan R., Bronk P., and Zinsmaier K. E. (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.
53. 2+ regulated exocytic vesicles in fibroblasts and epithelial cells. J. Cell Biol. 137, 93-104.
54. Rudiger S., Germeroth L., Schneider-Mergener J., and Bukau B. (1997) Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J. 16, 1501-1507.
55. Schiavo G., Benfenati F., Poulain B., Rossetto O., Polverino de Laureto P., DasGupta B. R., and Montecucco C. (1992) Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359, 832-835.
56. Sheng Z. H., Rettig J., Cook T., and Catterall W. A. (1996) Calcium-dependent interaction of N-type calcium channels with the synaptic core complex. Nature 379, 451-454.
57. Silver P. A. and Way J. C. (1993) Eukaryotic DnaJ homologues and the specificity of Hsp70 activity. Cell 74, 5-6.
58. Sollner T., Whiteheart S. W., Brunner M., Erdjument-Bromage H., Geromanos S., Tempst P., and Rothman J. E. (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318-323.
59. Stahl B., Tobaben S., and Südhof T. C. (1999) Two distinct domains in hsc70 are essential for the interaction with the synaptic vesicle cysteine string protein. Eur. J. Cell Biol. 78, 375-381.
60. Südhof T. C. (1995) The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375, 645-653.
61. Südhof T. C. and Rizo J. (1996) Synaptotagmins: C2 domain proteins that regulate membrane traffic. Neuron 17, 379-388.
62. Sutton R. B., Fasshauer D., Jahn R., and Brunger A. T. (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2,4A resolution. Nature 395, 347-353.
63. Sweeney S. T., Broadie K., Keane J., Niemann H., and O'Kane C. J. (1995) Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioural defects. Neuron 14, 341-351.
64. Terada K., Kanazawa M., Bukau B., and Mori M. (1997) The human DnaJ homologue dj2 facilitates mitochondrial protein import and luciferase refolding. J. Cell Biol. 139, 1089-1095.
65. Umbach J. A. and Gundersen C. B. (1991) Suppression cloning of a cDNA fragment for a candidate presynaptic calcium channel. Ann. NY Acad. Sci. 635, 443-446.
66. 2+ -dependent secretion of neurotransmitter at Drosophila neuromuscular junctions. J. Neurosci. 17, 7203-7209.
67. Umbach J. A., Zinsmaier K. E., Eberle K. K., Buchner E., Benzer S., and Gundersen C. B. (1994) Presynaptic dysfunction in Drosophila csp null mutants. Neuron 13, 899-907.
68. Umbach J. A., Saitoe M., Kidokoro Y., and Gundersen C. B. (1998) Attenuated influx of calcium ions at nerve endings of csp and shibire mutant Drosophila. J. Neurosci. 18, 3233-3340.
69. Ungewickell E., Ungewickell H., Holstein S. H., Lindner R., Prasad K., Barouch W., Martin B., Greene L. E., and Eisenberg E. (1995) Role of auxilin in uncoating clathrin-coated vesicles. Nature 378, 632-635.
70. Van de Goor J. and Kelly R. B. (1996) Association of Drosophila cysteine string proteins with membranes. FEBS Lett. 380, 251-256.
71. csl mutant Drosophila. Proc. Natl. Acad. Sci. USA 92, 5739-5743.
72. Walch-Solimena C., Blasi J., Edelmann L., Chapman E. R., Fischer von Mollard G., and Jahn R. (1995) The t-SNAREs syntaxin 1 and SNAP-25 are present on organelles that participate in vesicle recycling. J. Cell Biol. 128, 637-645.
73. Weber T., Zemelman B. V., McNew J. A., Westermann B., Gmachl M., Parfiati F., Sollner T. H., and Rothman J. E. (1998) SNARE pins: minimal machinery for membrane fusion. Cell 92, 759-772.
74. 2+ channels. EMBO J. 15, 4100-4110.
75. Wu M. N., Littleton J. T., Bhat M. A., Prokop A., and Bellen H. J. (1998) ROP, the Drosophila Sec1 homolog, interacts with syntaxin and regulates neurotransmitter release in a dosage-dependent manner. EMBO J. 17, 127-139.
76. Wu M. N., Fergestad T., Lloyd T. E., He Y., Broadie K., and Bellen H. J. (1999) Syntaxin 1A interacts with multiple exocytotic proteins to regulate neurotransmitter release in vivo. Neuron 23, 593-605.
77. 2+ increases and by cAMP. J. Neurosci. 19, 2432-2441.
78. Zhang H., Kelley W. L., Chamberlain L. H., Burgoyne R. D., Wollheim C. B., and Lang J. (1998) Cysteine-string proteins regulate exocytosis of insulin independent from transmembrane ion fluxes. FEBS Lett. 437, 267-272.
79. Zhang H., Kelley W. L., Chamberlain L. H., Burgoyne R. D., Wollheim C. B., and Lang J. (1999) Mutational analysis of cysteine-string protein function in insulin exocytosis. J. Cell Sci. 112, 1345-1351.
80. Zinsmaier K. E., Hofbauer A., Heimbeck G., Pflugfelder G. O., Buchner S., and Buchner E. (1990) A cysteine string protein is expressed in retina and brain of Drosophila. J. Neurogenet. 7, 15-29.
81. Zinsmaier K. E., Eberle K. K., Buchner E., Walter N., and Benzer S. (1994) Paralysis and early death in cysteine string protein mutants in Drosophila. Science 263, 977-980.