Mutational analysis of cysteine-string protein function in insulin exocytosis

Journal of Cell Science

Volumn 112, Issue 9, 1999, Pages 1345-1351

  Zhang, Hui ^a   Kelley, William L ^a   Chamberlain, Luke H ^b   Burgoyne, Robert D ^b   Lang, Jochen ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Calcium; DnaJ; Exocytosis; Insulin

Indexed keywords

CHAPERONE; CYSTEINE; INSULIN; PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; EXOCYTOSIS; HUMAN; INSULIN RELEASE; ION TRANSPORT; MUTATION; NEUROTRANSMITTER RELEASE; NUCLEOTIDE SEQUENCE; POINT MUTATION; PRIORITY JOURNAL;

CELLS, CULTURED; EXOCYTOSIS; HSP40 HEAT-SHOCK PROTEINS; HUMANS; INSULIN; MEMBRANE PROTEINS; MUTAGENESIS, SITE-DIRECTED; NERVE TISSUE PROTEINS; POINT MUTATION; SUBCELLULAR FRACTIONS;

EID: 0033055960     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (52)

1. Augustine, G. J., Burns, M. E., Debello, W. M., Pettit, D. L. and Schweizer, F. E. (1996). Exocytosis: proteins and perturbations. Annu. Rev. Pharmacol. Toxicol. 36, 659-701.
2. 2+ channels and insulin-containing secretory granules and its significance for the initiation of exocytosis in mouse pancreatic B-cells. EMBO J. 14, 50-57.
3. 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.
4. Brown, H., Larsson, O., Bränström, R., Yang, S. N., Leibiger, B., Leibiger, I., Fried, G., Moede, T., Deeney, J. T., Brown, G. R., et al. (1998). Cysteine string protein (CSP) is an insulin secretory granule-associated protein regulating beta-cell exocytosis. EMBO J. 17, 5048-5058.
5. 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.
6. 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.
7. 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.
8. 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.
9. Chamberlain, L. H. and Burgoyne, R. D. (1998). Cysteine string protein functions directly in regulated exocytosis. Mol. Biol. Cell 9, 2259-2267.
10. Coppola, T. and Gundersen, C. (1996). Widespread expression of human cysteine string proteins. FEBS Lett. 391, 269-272.
11. Eberle, K. K., Zinsmaier, K. E., Buchner, S., Gruhn, M., Jenni, M., Arnold, C., Leibold, C., Reisch, D., Walter, N., Hafen, E., et al. (1998). Wide distribution of the cysteine string proteins in Drosophila tissues revealed by targeted mutagenesis. Cell Tissue Res. 294, 203-217.
12. Gengyoando, K., Kitayama, H., Mukaida, M. and Ikawa, Y. (1996). A murine neural-specific homolog corrects cholinergic defects in Caenorhabditis elegans unc-18 mutants. J. Neurosci. 16, 6695-6702.
13. 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.
14. 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.
15. Hanson, P. I., Heuser, J. E. and Jahn, R. (1997). Neurotransmitter release -four years of SNARE complexes. Curr. Opin. Neumbiol. 7, 310-315.
16. Holstein, S. E., Ungewickell, H. and Ungewickell, E. (1996). Mechanism of clathrin basket dissociation: separate functions of protein domains of the DnaJ homologue auxilin. J. Cell Biol. 135, 925-937.
17. Kelley, W. L. (1998). The J-domain family and the recruitment of chaperone power. Trends Biochem. Sci. 23, 222-227.
18. 2+ stimulated exocytosis of insulin. Biochem. J. 314, 199-203.
19. Kunkel, T. A. (1985). Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Nat. Acad. Sci. USA 82, 477-492.
20. o or by the expression of their active Gα subunits. EMBO J. 14, 3635-3644.
21. Lang, J., Fukuda, M., Zhang, H., Mikoshiba, K. and Wollheim, C. B. (1997a). The first C2 domain of synaptotagmin is required for exocytosis of insulin from pancreatic β-cells: Action of synaptotagmin at low micromolar calcium. EMBO J. 16, 5837-5846.
22. Lang, J., Regazzi, R. and Wollheim, C. B. (1997b). Clostridial toxins and endocrine secretion: Their use in insulin-secreting cells. In Bacterial Toxins: Tools in Cell Biology (ed. K. Aktories), pp. 217-240. Weinheim: Chapman & Hall.
23. Lang, J., Zhang, H., Vaidyanathan, V. V., Sadoul, K., Niemann, H. and Wollheim., C. B. (1997c). Transient expression of botulinum neurotoxin C1 light chain differentially inhibits calcium and glucose induced insulin secretion in clonal β-cells. FEES Lett. 419, 13-17.
24. Lang, J. (1999). Molecular mechanisms and regulation of insulin exocytosis as a paradigm of endocrine secretion. Eur. J. Biochem. 259, 1-16.
25. 1A subunit of the P/Q-type calcium channel. J. Biol. Chem. 273, 13488-13492.
26. Li, G., Regazzi, R., Balch, W. E. and Wollheim, C. B. (1993). Stimulation of insulin release from permeabilized HIT-T15 cells by a synthetic peptide corresponding to the effector domain of the small GTP-binding protein rab3. FEBS Lett. 327, 145-149.
27. Ligon, B., Boyd, A. E. and Dunlap, K. (1998). Class A calcium channel variants in pancreatic islets and their role in insulin secretion. J. Biol. Chem. 273, 13905-13911.
28. Lin, R. C. and Scheller, R. H. ( 1997). Structural organization of the synaptic exocytosis core complex. Neuron 19, 1087-1094.
29. Lupas, A. (1996). Prediction and analysis of coiled-coiled structures. Meth. Enzymol. 266, 513-525.
30. Martin, T. F. J. (1997). Stages of regulated exocytosis. Trends Cell Biol. 7, 271-276.
31. 2+ channels. Science 263, 981-982.
32. Mastrogiacomo, A. and Gundersen, C. B. (1995). The nucleotide and deduced amino acid sequence of a rat cysteine string protein. Brain Res. Mol. Brain Res. 28, 1218.
33. 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.
34. 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.
35. Morgan, A. and Burgoyne, R. D. (1995). Is NSF a fusion protein? Trends Cell Biol. 5, 335-339.
36. 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.
37. Regazzi, R., Ravazzola, R., Iezzi, M., Lang, J., Zahraoui, A. andereggen, E., Morel, P., Takai, Y. and Wollheim, C. B. (1996). Expression, localization and functional role of small GTPases of the Rab3 family in insulin-secreting cells. J. Cell Sci. 109, 2265-2273.
38. Schlossman, D. M., Schmid, S. L., Braell, W. A. and Rothman, J. R. (1984). An enzyme that remove clathrin coats: purification of an uncoating ATPase. J. Cell Biol. 99, 723-733.
39. Schulze, K. L., Littleton, J. T., Salzberg, A., Halachmi, N., Stern, M., Lev, Z. and Bellen, H. J. (1994). rop, a Drosophila homolog of yeast Sec 1 and vertebrate n-Sec 1/Munc-18 proteins, is a negative regulator of neurotransmitter release in vivo. Neuron 13, 1099-1108.
40. Stanley, E. F. (1997). The calcium channel and the organization of the presynaptic transmitter release face. Trends Neurosci. 20, 404-409.
41. Umbach, J. A., Zinsmaier, K. E., Eberle, K. K., Buchner, E., Benzer, S. and Gundersen, C. B. (1994). Presynaptic dysfunction in Drosophila csp mutants. Neuron 13, 899-907.
42. 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, 3233-3240.
43. van de Goor, J. and Kelly, R. B. (1996). Association of Drosophila cysteine string proteins with membranes. FEBS Lett. 380, 251-256.
44. Wall, D., Zylicz, M. and Georgopoulos, C. (1995). The conserved G/F motif of the DnaJ chaperone is necessary for the activation of the substrate binding properties of the DnaK chaperone. J. Biol. Chem. 270, 2139-2144.
45. Wang, C. and Lee, M. R. (1993). High-level expression of soluble rat hsc70 in Escherichia coli: purification and characterization of the cloned enzyme. Biochem. J. 294, 69-77.
46. Weller, U., Muller, L., Messner, M., Palmer, M., Valeva, A., Tranum Jensen, J., Agrawal, P., Biermann, C., Dobereiner, A., Kehoe, M. A., et al. (1996). Expression of active streptolysin O in Escherichia coli as a maltose-binding-protein-streptolysin-O fusion protein. The N-terminal 70 amino acids are not required for hemolytic activity. Eur. J. Biochem. 236, 34-39.
47. Wilson, R., Ainscough, R. anderson, K., Baynes, C., Berks, M., Bonfield, J., Burton, J., Connell, M., Copsey, T., Cooper, J., et al. (1994). 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature 368, 32-38.
48. Wollheim, C. B., Lang, J. and Regazzi, R. (1996). Regulation of exocytosis by calcium and G-proteins. Diabetes Rev. 4, 277-297.
49. Zhang, H., Kelley, W., Chamberlain, L., Bourgoyne, R., Wollheim, C. B. and Lang, J. (1997). Role of the cysteine string protein in insulin secretion from pancreatic β-cells. Diabetologia 40 Suppl. 1, A1 13:439.
50. 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.
51. 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.
52. Zinsmaier, K. E., Eberle, K. K., Buchner, E., Walter, N. and Benzer, S. (1994). Paralysis and early death in cysteine string protein mutants of Drosophila. Science 263, 977-980.