Cysteine-string protein isoform beta (Cspβ) is targeted to the trans-Golgi network as a non-palmitoylated CSP in clonal β-cells

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1773, Issue 2, 2007, Pages 109-119

  Boal, Frédéric ^a   Le Pevelen, Séverine ^a   Cziepluch, Celina ^b   Scotti, Pier ^a   Lang, Jochen ^a  

^a INSTITUT EUROPÉEN DE CHIMIE ET BIOLOGIE   (France)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Chaperone; Cysteine string protein; Exocytosis; Palmitoylation; Pancreatic cell; Protein membrane association

Indexed keywords

CHAPERONE; COMPLEMENTARY DNA; CYSTEINE; CYSTEINE STRING PROTEIN; CYSTEINE STRING PROTEIN ALPHA; CYSTEINE STRING PROTEIN BETA; GLUTAMINE; HEAT SHOCK COGNATE PROTEIN 70; INSULIN; ISOPROTEIN; MEMBRANE PROTEIN; PROTEIN DNAJ; PROTEIN SGT; TETRATRICOPEPTIDE REPEAT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA LIBRARY; ENDOCRINE CELL; EXOCYTOSIS; GENE OVEREXPRESSION; LARGE DENSE CORE VESICLE; MEMBRANE BINDING; MOUSE; MUTAGENESIS; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PALMITOYLATION; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; TESTIS CELL; TRANS GOLGI NETWORK; TRANSIENT EXPRESSION; TRANSPORT VESICLE;

EID: 33846289269     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2006.08.054     Document Type: Article

References (42)

1. Lang J. Molecular mechanisms and regulation of insulin exocytosis as a paradigm of endocrine secretion. Eur. J. Biochem. 259 (1999) 3-17
2. Jahn R., Lang T., and Sudhof T.C. Membrane fusion. Cell 112 (2003) 519-533
3. Morgan A., and Burgoyne R.D. Is NSF a fusion protein?. Trends Cell Biol. 5 (1995) 335-339
4. Chamberlain L.H., and Burgoyne R.D. Cysteine-string protein: the chaperone at the synapse. J. Neurochem. 74 (2000) 1781-1789
5. Evans G.J., Morgan A., and Burgoyne R.D. Tying everything together: the multiple roles of cysteine string protein (CSP) in regulated exocytosis. Traffic 4 (2003) 653-659
6. Zhang H., Kelley W.L., Chamberlain L.H., Burgoyne R.D., Wollheim C.B., and Lang J. Cysteine-string proteins regulate exocytosis of insulin independent from transmembrane ion fluxes. FEBS Lett. 437 (1998) 267-272
7. Zinsmaier K.E., and Bronk P. Molecular chaperones and the regulation of neurotransmitter exocytosis. Biochem. Pharmacol. 62 (2001) 1-11
8. Tobaben S., Thakur P., Fernandez-Chacon R., Sudhof T.C., Rettig J., and Stahl B. A trimeric protein complex functions as a synaptic chaperone machine. Neuron 31 (2001) 987-999
9. Tobaben S., Varoqueaux F., Brose N., Stahl B., and Meyer G. A brain-specific isoform of small glutamine-rich tetratricopeptide repeat-containing protein binds to Hsc70 and the cysteine string protein. J. Biol. Chem. 278 (2003) 38376-38383
10. Zinsmaier K.E., Hofbauer A., Heimbeck G., Pflugfelder G.O., Buchner S., and Buchner E. A cysteine-string protein is expressed in retina and brain of Drosophila. J. Neurogenet. 7 (1990) 15-29
11. Umbach J.A., Zinsmaier K.E., Eberle K.K., Buchner E., Benzer S., and Gundersen C.B. Presynaptic dysfunction in Drosophila csp mutants. Neuron 13 (1994) 899-907
12. Zinsmaier K.E., Eberle K.K., Buchner E., Walter N., and Benzer S. Paralysis and early death in cysteine string protein mutants of Drosophila. Science 263 (1994) 977-980
13. Evans G.J., Wilkinson M.C., Graham M.E., Turner K.M., Chamberlain L.H., Burgoyne R.D., and Morgan A. Phosphorylation of cysteine string protein by protein kinase A. Implications for the modulation of exocytosis. J. Biol. Chem. 276 (2001) 47877-47885
14. Braun J.E., Wilbanks S.M., and Scheller R.H. The cysteine string secretory vesicle protein activates Hsc70 ATPase. J. Biol. Chem. 271 (1996) 25989-25993
15. Chamberlain L.H., and Burgoyne R.D. Activation of the ATPase activity of heat-shock proteins Hsc70/Hsp70 by cysteine-string protein. Biochem. J. 322 (1997) 853-858
16. Zhang H., Kelley W.L., Chamberlain L.H., Burgoyne R.D., and Lang J. Mutational analysis of cysteine-string protein function in insulin exocytosis. J. Cell Sci. 112 (1999) 1345-1351
17. Gundersen C.B., Mastrogiacomo A., Faull K., and Umbach J.A. Extensive lipidation of a Torpedo cysteine string protein. J. Biol. Chem. 269 (1994) 19197-19199
18. Coppola T., and Gundersen C. Widespread expression of human cysteine string proteins. FEBS Lett. 391 (1996) 269-272
19. Magga J.M., Jarvis S.E., Arnot M.I., Zamponi G.W., and Braun J.E. Cysteine string protein regulates G protein modulation of N-type calcium channels. Neuron 28 (2000) 195-204
20. Natochin M., Campbell T.N., Barren B., Miller L.C., Hameed S., Artemyev N.O., and Braun J.E. Characterization of the G alpha(s) regulator cysteine string protein. J. Biol. Chem. 280 (2005) 30236-30241
21. Bronk P., Nie Z., Klose M.K., Dawson-Scully K., Zhang J., Robertson R.M., Atwood H.L., and Zinsmaier K.E. The multiple functions of cysteine-string protein analyzed at Drosophila nerve terminals. J. Neurosci. 25 (2005) 2204-2214
22. Boal F., Zhang H., Tessier C., Scotti P., and Lang J. The variable C-terminus of cysteine string proteins modulates exocytosis and protein-protein interactions. Biochemistry 43 (2004) 16212-16223
23. 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., Scheller R.H., Corkey B.E., Berggren P.O., and Meister B. Cysteine string protein (CSP) is an insulin secretory granule- associated protein regulating beta-cell exocytosis. EMBO J. 17 (1998) 5048-5058
24. Fernandez-Chacon R., Wolfel M., Nishimune H., Tabares L., Schmitz F., Castellano-Munoz M., Rosenmund C., Montesinos M.L., Sanes J.R., Schneggenburger R., and Sudhof T.C. The synaptic vesicle protein CSP alpha prevents presynaptic degeneration. Neuron 42 (2004) 237-251
25. Chamberlain L.H., and Burgoyne R.D. Identification of a novel cysteine string protein variant and expression of cysteine string proteins in non-neuronal cells. J. Biol. Chem. 271 (1996) 7320-7323
26. Cziepluch C., Kordes E., Poirey R., Grewenig A., Rommelaere J., and Jauniaux J.C. Identification of a novel cellular TPR-containing protein, SGT, that interacts with the nonstructural protein NS1 of parvovirus H-1. J. Virol. 72 (1998) 4149-4156
27. Gagescu R., Demaurex N., Parton R.G., Hunziker W., Huber L.A., and Gruenberg J. The recycling endosome of Madin-Darby canine kidney cells is a mildly acidic compartment rich in raft components. Mol. Biol. Cell 11 (2000) 2775-2791
28. Monterrat C., Boal F., Grise F., Hemar A., and Lang J. Synaptotagmin 8 is expressed both as a calcium-insensitive soluble and membrane protein in neurons, neuroendocrine and endocrine cells. Biochim. Biophys. Acta 1763 (2006) 73-81
29. van de Goor J., and Kelly R.B. Association of Drosophila cysteine string proteins with membranes. FEBS Lett. 380 (1996) 251-256
30. Mastrogiacomo A., Kohan S.A., Whitelegge J.P., and Gundersen C.B. Intrinsic membrane association of Drosophila cysteine string proteins. FEBS Lett. 436 (1998) 85-91
31. Hess D.T., Slater T.M., Wilson M.C., and Skene J.H. The 25 kDa synaptosomal-associated protein SNAP-25 is the major methionine-rich polypeptide in rapid axonal transport and a major substrate for palmitoylation in adult CNS. J. Neurosci. 12 (1992) 4634-4641
32. Fujiki Y., Hubbard A.L., Fowler S., and Lazarow P.B. Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J. Cell Biol. 93 (1982) 97-102
33. Chamberlain L.H., and Burgoyne R.D. The cysteine-string domain of the secretory vesicle cysteine-string protein is required for membrane targeting. Biochem. J.. 335 (1998) 205-209
34. White S.H., and Wimley W.C. Membrane protein folding and stability: physical principles. Annu. Rev. Biophys. Biomol. Struct. 28 (1999) 319-365
35. Xu Y., Wong S.H., Tang B.L., Subramaniam V.N., Zhang T., and Hong W. A 29-kilodalton Golgi soluble N-ethylmaleimide-sensitive factor attachment protein receptor (Vti1-rp2) implicated in protein trafficking in the secretory pathway. J. Biol. Chem. 273 (1998) 21783-21789
36. Antonin W., Riedel D., and von Mollard G.F. The SNARE Vti1a-b is localized to small synaptic vesicles and participates in a novel SNARE complex. J. Neurosci. 20 (2000) 5724-5732
37. Smotrys J.E., and Linder M.E. Palmitoylation of intracellular signaling proteins: regulation and function. Annu. Rev. Biochem. 73 (2004) 559-587
38. Chamberlain L.H., and Burgoyne R.D. The molecular chaperone function of the secretory vesicle cysteine string proteins. J. Biol. Chem. 272 (1997) 31420-31426
39. Yanai A., Huang K., Kang R., Singaraja R.R., Arstikaitis P., Gan L., Orban P.C., Mullard A., Cowan C.M., Raymond L.A., Drisdel R.C., Green W.N., Ravikumar B., Rubinsztein D.C., El-Husseini A., and Hayden M.R. Palmitoylation of huntingtin by HIP14 is essential for its trafficking and function. Nat. Neurosci. 9 (2006) 824-831
40. Vogel K., Cabaniols J.P., and Roche P.A. Targeting of SNAP-25 to membranes is mediated by its association with the target SNARE syntaxin. J. Biol. Chem. 275 (2000) 2959-2965
41. Joglekar A.P., and Hay J.C. Evidence for regulation of ER/Golgi SNARE complex formation by hsc70 chaperones. Eur. J. Cell Biol. 84 (2005) 529-542
42. Rudiger S., Schneider-Mergener J., and Bukau B. Its substrate specificity characterizes the DnaJ co-chaperone as a scanning factor for the DnaK chaperone. EMBO J. 20 (2001) 1042-1050