Cysteine string protein (CSP) is an insulin secretory granule-associated protein regulating β-cell exocytosis

EMBO Journal

Volumn 17, Issue 17, 1998, Pages 5048-5058

  Brown, Hilary ^a   Larsson, Olof ^a   Bränström, Robert ^a   Yang, Shao Nian ^a   Leibiger, Barbara ^a   Leibiger, Ingo ^a   Fried, Gabriel ^b   Moede, Tilo ^a   Deeney, Jude T ^a   Brown, Graham R ^a   Jacobsson, Gunilla ^a   Rhodes, Christopher J ^c   Braun, Janice E A ^d   Scheller, Richard H ^d   Corkey, Barbara E ^e   Berggren, Per Olof ^a   Meister, Björn ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d STANFORD UNIVERSITY   (United States)

^e BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calcium; Chaperone; Heat shock protein; Pancreas; Secretion

Indexed keywords

CALCIUM; CALCIUM CHANNEL; CYSTEINE STRING PROTEIN; INSULIN; MESSENGER RNA; PROTEIN; UNCLASSIFIED DRUG;

ACINAR CELL; AMPEROMETRY; ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CELL LINE; CELL MEMBRANE; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; CYTOSOL; ENDOCRINE CELL; EXOCYTOSIS; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; INSULIN RELEASE; INSULINOMA; NERVE FIBER; NONHUMAN; PANCREAS; PANCREAS ISLET; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECRETORY GRANULE; SYNAPSE VESICLE;

ANIMALS; CALCIUM CHANNELS; CELL FRACTIONATION; CELLS, CULTURED; CYTOPLASMIC GRANULES; EXOCYTOSIS; FLUORESCENT ANTIBODY TECHNIQUE; HSP40 HEAT-SHOCK PROTEINS; INSULIN; ISLETS OF LANGERHANS; MALE; MEMBRANE PROTEINS; MICE; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; RNA, MESSENGER; SUBCELLULAR FRACTIONS;

ANIMALIA; EUKARYOTA;

EID: 0032167421     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.17.5048     Document Type: Article

References (53)

1. 2+ on insulin secretion in pancreatic beta cells. J. Biol. Chem., 272, 31308-31314.
2. 2+ and pancreatic β-cell function. Biochem. Soc. Trans., 22, 12-18.
3. Bohen, S.P. Kralli, A. and Yamamoto, K.R. (1995) Hold 'em and fold 'em: chaperones and signal transduction. Nature. 268, 1303-1304.
4. 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.
5. Braun, J.E.A., Wilbanks, S.M. and Scheller, R.H. (1996) The cysteine string protein secretory vesicle protein activates Hsc70 ATPase. J. Biol. Chem., 271, 25989-25993.
6. Buchan, A.M.J., Sikora, L.K.J., Levy, J.G., McIntosh, C.H.S., Dyck, J. and Brown, J.C. (1985) An immunocytochemical investigation with monoclonal antibodies to somatostatin. Histochemistry, 83, 175-180.
7. Buchner, E. and Gundersen, C.B. (1997) The DnaJ-like cysteine string protein and exocytotic neurotransmitter release. Trends Neurosci., 20, 223-227.
8. Caplan, A.J., Cyr, D.M. and Douglas, M.G. (1993) Eucaryotic homologues of Escherichia coli dnaJ: a diverse protein family that functions with Hsp70 stress proteins. Mol. Biol. Cell, 4, 555-563.
9. 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.
10. Chamberlain, L.H. and Burgoyne, R.D. (1997) Activation of the ATPase activity of heat-shock proteins Hsc70 and Hsp70 by cysteine-string protein. Biochem. J., 322, 853-858.
11. Chamberlain, L.H., Henry, J. and Burgoyne, R.D. (1996) Cysteine string proteins are associated with chromaffin granules. J. Biol. Chem., 271, 19514-19517.
12. Coppola, T. and Gundersen, C.B. (1996) Widespread expression of human cysteine string proteins. FEBS Lett., 391, 269-272.
13. Dagerlind, Å., Friberg, K., Bean, A.J. and Hökfelt, T. (1992) Sensitive mRNA detection using unfixed tissue: combined radioactive and non-radioactive in situ hybridization histochemistry. Histochemistry, 98, 39-49.
14. Efendic, S., Kindmark, H. and Berggren, P.-O. (1991) Mechanisms involved in the regulation of the insulin secretory process. J. Intern. Med. Suppl. 2, 229, 9-22.
15. Gazdar, A.F., Chick, W.L., Oie, H.K., Sims, H.L., King, D.L., Weir, G.C. and Lauris, V. (1980) Continuous, clonal, insulin - and somatostatin -secreting cell lines established from a transplantable rat islet cell tumour. Proc. Natl Acad. Sci. USA, 77, 3519-3523.
16. 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.
17. 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.
18. 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.
19. Hames, B.D. (1990) One-dimensional polyacrylamide gel electrophoresis. In Hames, B.D. and Rickwood, D. (eds), Gel Electrophoresis of Proteins. A Practical Approach. 2nd edn. IRL Press, Oxford, UK, pp. 1-147.
20. Hamill, O.P., Marty, A., Neher, E., Sakman, B. and Sigworth, F.J. (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch., 391, 85-100.
21. Jacobsson, G., Bean, A.J., Scheller, R.H., Juntti-Berggren, L., Deeney, J.T., Berggren, P.-O. and Meister, B. (1994) Identification of synaptic proteins and their isoform mRNAs in compartments of pancreatic endocrine cells. Proc. Natl Acad. Sci. USA, 91, 12487-12491.
22. 2+-stimulated exocytosis of insulin. Biochem. J., 314, 199-203.
23. 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 rat. J. Neurosci., 15, 6230-6238.
24. Lacy, P.E. and Kostianovsky, M. (1967) Method for the isolation of intact islets of Langerhans from the rat pancreas. Diabetes, 16, 35-39.
25. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
26. Lang, J., Fukuda, M., Zhang, H., Mikoshiba, K. and Wollheim, C.B. (1997) 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.
27. Lernmark, Å. (1974) The preparation of and studies on, free cell suspensions from mouse pancreatic islets. Diabetologia, 10, 431-438.
28. Martell, A.E. and Smith, R.M. (1974) Critical stability constants. Vol I. Amino Acids. Vol II. Amines. Plenum Press, New York, NY.
29. Martin, F., Moya, F., Gutierrez, L.M., Reig, J.A. and Soria, B. (1995) Role of syntaxin in mouse pancreatic beta cells. Diabetologia, 38, 860-863.
30. 2+ but not guanosine-5′-[γ-thio]triphosphate-induced secretion. Biochem. J., 320, 201-205.
31. Martin-Moutout, N., Charvin, N., Leveque, C., Sato, K., Nishiki, T., Kozaki, S., Takahashi, M. and Seager, M. (1996) Interaction of SNARE complexes with P/Q-type calcium channels in rat cerebellar synaptosomes. J. Biol. Chem., 271, 6567-6570.
32. 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.
33. Mastrogiacomo, A., Parsons, S.M., Zampighi, G.A., Jenden, D.J., Umbach, J.A. and Gundersen, C.B. (1994a) Cysteine string proteins: a potential link between synaptic vesicles and presynaptic calcium channels. Science, 263, 981-982.
34. Mastrogiacomo, A., Evans, C.J. and Gundersen, C.B. (1994b) Antipeptide antibodies against a Torpedo cysteine-string protein. J. Neurochem., 62, 873-880.
35. Mizuta, M., Kurose, T., Miki, T., Shoji-Kasai, Y., Takahashi, M., Seino, S. and Matsukura, S. (1997) Localization and functional role of synaptotagmin III in insulin secretory vesicles in pancreatic β-cells. Diabetes, 46, 2002-2006.
36. Nagamatsu, S., Fujiwara, T., Nakamichi, Y., Watanabe, T., Katahira, H. and Seino, S. (1996) Expression and functional role of syntaxin 1/HPC-1 in pancreatic beta cells. Syntaxin 1A, but not 1B, plays a negative role in regulatory insulin release pathway. J. Biol. Chem., 2271, 1160-1165.
37. 2+ in insulinoma cell line βTC3. Biochem. Biophys. Res. Comm., 231, 89-93.
38. Pelham, H.R. (1986) Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell, 46, 959-961.
39. Pupier, S., Leveque, C., Marqueze, B., Kataoka, M., Takahashi, M. and Seagar, M.J. (1997) Cysteine string proteins associated with secretory granules of the rat neurohypophysis. J. Neurosci., 17, 2722-2727.
40. 2+ but not for GTPγS-induced insulin secretion. EMBO J., 14. 2723-2730.
41. 2+-induced insulin exocytosis. EMBO J., 15, 6951-6959.
42. Sadoul, K., Lang, J., Montecucco, C., Weller, U., Regazzi, R., Catsicas, S., Wollheim, C.B. and Halban, P.A. (1995) SNAP-25 is expressed in islets of Langerhans and is involved in insulin release. J. Cell Biol., 128, 1019-1028.
43. Schlossman, D.M., Schmid, S.L., Braell, W.A. and Rothman, J. (1984) An enzyme that removes clathrin coats: purification of an uncoating ATPase. J. Cell Biol., 99, 723-733.
44. Smith, P.A., Duchen, M.R. and Ashcroft, F.M. (1995) A fluorimetric and amperometric study of calcium and secretion in isolated mouse pancreatic beta-cells. Pflügers Arch., 430, 808-818.
45. Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl Acad. Sci. USA, 76, 4350-4354.
46. 2+-dependent secretion of neurotransmitter at Drosophila neuromuscular junction. J. Neurosci., 17, 7203-7209.
47. 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.
48. Wheeler, M.B. et al. (1996) Characterization of the SNARE protein expression in beta-cell lines and pancreatic islets. Endocrinology, 137, 1340-1348.
49. Wightman, R.M., Jankowski, J.A., Kennedy, R.T., Kawagoe, K.T., Schroeder, T.J., Leszczyszyn, D.J., Near, J.A., Diliberto, E.J.,Jr and Viveros, O.H. (1991) Temporally resolved catecholamine spikes correspond to single vesicle release from individual chromaffin cells. Proc. Natl Acad. Sci. USA, 88, 10754-10758.
50. Young, W.S.,III (1990) In situ-hybridization histochemistry. In Björklund, A., Hökfelt, T., Wouterlood, F.G. and van den Pol, A.N. (eds), Handbook of Chemical Neuroanatomy: Analysis of Neuronal Microcircuits and Synaptic Interactions. Elsevier, Amsterdam. The Netherlands, pp. 481-512.
51. Zhou, Z. and Misler, S. (1996) Amperometric detection of quantal secretion from patch-clamped rat pancreatic β-cells. J. Biol. Chem., 270, 270-277.
52. 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.
53. 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.