Dual role of the cysteine-string domain in membrane binding and palmitoylation-dependent sorting of the molecular chaperone cysteine-string protein

Molecular Biology of the Cell

Volumn 17, Issue 11, 2006, Pages 4748-4759

  Greaves, Jennifer ^a   Chamberlain, Luke H ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CYSTEINE STRING PROTEIN; PALMITIC ACID;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL MEMBRANE TRANSPORT; ENDOPLASMIC RETICULUM; MEMBRANE BINDING; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN TARGETING; RAT; REACTION ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL MARKERS; CELL MEMBRANE; CYSTEINE; ENDOPLASMIC RETICULUM; GREEN FLUORESCENT PROTEINS; HSP40 HEAT-SHOCK PROTEINS; MEMBRANE PROTEINS; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PALMITATES; PC12 CELLS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RATS; RECOMBINANT FUSION PROTEINS; SEQUENCE ANALYSIS, PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 33750516084     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-03-0183     Document Type: Article

References (51)

1. Apolloni, A., Prior, I. A., Lindsay, M., Parton, R. G., and Hancock, J. F. (2000). H-ras but not K-ras traffics to the plasma membrane through the exocytic pathway. Mol. Cell. Biol. 20, 2475-2487.
2. Bartels, D. J., Mitchell, D. A., Dong, X., and Deschenes, R. J. (1999). Erf2, a novel gene product that affects the localisation and palmitoylation of Ras2 in Saccharomyces cerevisiae. Mol. Biol. Cell 19, 6775-6787.
3. Boal, F., Zhang, H., Tessier, C., Scotti, P., and Lang, J. (2004). The variable C-terminus of cysteine string proteins modulates exocytosis and protein-protein interactions. Biochemistry 43, 16212-16223.
4. Braun, J. E., and Scheller, R. H. (1995). Cysteine string protein, a DnaJ family member, is present on diverse secretory vesicles. Neuropharmacology 34, 1361-1369.
5. Brown, H., et al. (1998), Cysteine string protein (CSP) is an insulin secretory granule-associated protein regulating beta-cell exocytosis. EMBO J. 17, 5048-5058.
6. Chamberlain, L. H., Henry, J., and Burgoyne, R. D. (1996). Cysteine string proteins are associated with chromaffin granules. J. Biol. Chem. 271, 19514-19517.
7. Chamberlain, L. H., and Burgoyne, R. D. (1997), The molecular chaperone function of the secretory vesicle cysteine string proteins. J. Biol. Chem. 272, 31420-31426.
8. Chamberlain, L. H., and Burgoyne, R. D. (1998a). The cysteine-string domain of the secretory vesicle cysteine-string protein is required for membrane targeting. Biochem. J. 335, 205-209.
9. Chamberlain, L. H., and Burgoyne, R. D. (1998b) Cysteine string protein functions directly in regulated exocytosis. Mol. Biol. Cell 9, 2259-2267.
10. Chamberlain, L. H., Graham, M. E., Kane, S., Jackson, J. L., Maier, V. H., Burgoyne, R. D., and Gould, G. W. (2001). The synaptic vesicle protein, cysteine-string protein, is associated with the plasma membrane in 3T3-L1 adipocytes and interacts with syntaxin 4. J. Cell Sci. 114, 445-455.
11. Chandra, S., Gallardo, G., Fernandez-Chacon, R., Schluter, O. M., and Südhof, T. C. (2005). Alpha-synuclein cooperates with CSPalpha in preventing neurodegeneration. Cell 123, 383-396.
12. Choy, E., Chiu, V. K., Silletti, J., Feoktistov, M., Morimoto, T., Michaelson, D., Ivanov, I. E., and Philips, M. R. (1999). Endomembrane trafficking of Ras: the CAAX motif targets proteins to the ER and golgi. Cell 98, 69-80.
13. Dunphy, J. T., Greentree, W. K., Manahan, C. L., and Linder, M. E. (1996). G-protein palmitoyltransferase activity is enriched in plasma membrane. J. Biol. Chem. 271, 7154-7159.
14. El-Husseini, A. E., Craven, S. E., Chetkovich, D. M., Firestein, B. L., Schnell, E., Aoki, C., and Bredt, D. S. (2000). Dual palmitoylation of PSD-95 mediates its vesiculotubular sorting, postsynaptic targeting, and ion channel clustering. J. Cell Biol. 148, 159-171.
15. El-Husseini, A. E., Schnell, E., Dakoji, S., Sweeney, N., Zhou, Q., Prange, O., Gauthier-Campbell, C., Aguilera-Moreno, A., Nicoll, R. A., and Bredt, D. S. (2002). Synaptic strength regulated by palmitate cycling on PSD-95. Cell 108, 849-863.
16. Fernandez-Chacon, R., et al. (2004). The synaptic vesicle protein CSPalpha prevents presynaptic degeneration. Neuron 42, 237-251.
17. Fukata, M., Fukata, Y., Adesnik, H., Nicoll, R. A., and Bredt, D. S. (2004). Identification of PSD-95 palmitoylating enzymes. Neuron 44, 987-996.
18. 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.
19. Graham, M. E., and Burgoyne, R. D. (2000). Comparison of cysteine string protein (Csp) and mutant alpha-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.
20. 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.
21. Huang, K., et al. (2004). Huntingtin-interacting protein HIP14 is a palmitoyl transferase involved in palmitoylation and trafficking of multiple neuronal proteins. Neuron 44, 977-986.
22. Huang, K., and El-Husseini, A. (2005). Modulation of neuronal protein trafficking and function by palmitoylation. Curr. Opin. Neurobiol. 15, 527-535.
23. Keller, C. A., Yuan, X., Panzanelli, P., Martin, M. L., Alldred, M., Sassoe-Pognetto, M., and Luscher, B. (2004). The gamma2 subunit of GABA(A) receptors is a substrate for palmitoylation by GODZ. J. Neurosci. 24, 5881-5891.
24. Kleuss, C., and Krause, E. (2003). Galpha(s) is palmitoylated at the N-terminal glycine. EMBO J. 22, 826-832.
25. Koegl, M., Zlatkine, P., Ley, S. C., Courtneidge, S. A., and Magee, A. I. (1994). Palmitoylation of multiple six-family kinases at a homologous N-terminal motif. Biochem. J. 303, 749-753.
26. 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.
27. Lane, S. R., and Liu, Y. (1997). Characterization of the palmitoylation domain of SNAP-25. J. Neurochem. 69, 1864-1869.
28. Lobo, S., Greentree, W. K., Linder, M. E., and Deschenes, R. J. (2002). Identification of a Ras palmitoyl transferase in Saccharomyces cerevisiae. J. Biol. Chem. 277, 41268-41273.
29. Mastrogiacomo, A., Parsons, S. M., Zampighi, G. A., Jenden, D. J., Umbach, J. A., and Gundersen, C. B. (1994). Cysteine-string proteins: a potential link between synaptic vesicles and presynaptic Ca2+ channels. Science 263, 981-982.
30. Mastrogiacomo, A., Kohan, S. A., Whitelegge, J. P., and Gundersen, C. B. (1998). Intrinsic membrane association of Drosophila cysteine string proteins. FEBS Lett. 436, 85-91.
31. Melkonian, K. A., Ostermeyer, A. G., Chen, J. Z., Roth, M. G., and Brown, D. A. (1999). Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated. J. Biol. Chem. 274, 3910-3917.
32. Naeve, C. W., and Williams, D. (1990). Fatty acids on the A/Japan/305/57 influenza virus hemagglutinin have a role in membrane fusion. EMBO J. 9, 3857-3866.
33. Nagano, N., Ota, M., and Nishikawa, K. (1999). Strong hydrophobic nature of cysteine residues in proteins. FEBS Lett. 458, 69-71.
34. Pepinsky, R. B., et al. (1998). Identification of a palmitic acid-modified form of human Sonic hedgehog. J. Biol. Chem. 273, 14037-14045.
35. 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.
36. Putilina, T., Wong, P., and Gentleman, S. (1999). The DHHC domain: a new highly conserved cysteine-rich motif. Mol. Cell. Biochem. 195, 219-226.
37. Roth, A. F., Feng, Y., Chen, L., and Davis, N. G. (2002). The yeast DHHC cysteine-rich domain protein Akr1p is a palmitoyl transferase. J. Cell Biol. 159, 23-28.
38. Salaün, C., Gould, G. W., and Chamberlain, L. H. (2005). The SNARE proteins SNAP-25 and SNAP-23 display different affinities for lipid rafts in PC12 cells: regulation by distinct cysteine-rich domains. J. Biol. Chem. 280, 1236-1240.
39. Smotrys, J. E., and Linder, M. E. (2004). Palmitoylation of intracellular signalling proteins: regulation and function. Annu. Rev. Biochem. 73, 559-587.
40. Steinhauer, D. A., Wharton, S. A., Wiley, D. C., and Skehel, J. J. (1991). Deacylation of the hemagglutinin of influenza A/Aichi/2/68 has no effect on membrane fusion properties. Virology 184, 445-448.
41. Swarthout, J. T., Lobo, S., Farh, L., Croke, M. R., Greentree, W. K., Deschenes, R. J., and Linder, M. E. (2005). DHHC9 and GCP16 constitute a human protein fatty acyl transferase with specificity for H- and N-Ras. J. Biol. Chem. 280, 31141-31148.
42. Tobaben, S., Thakur, P., Fernandez-Chacon, R., Südhof, T. C., Rettig, J., and Stahl, B. (2001). A trimeric protein complex functions as a synaptic chaperone machine. Neuron 31, 987-999.
43. Topinka, J. R., and Bredt, D. S. (1998). N-terminal palmitoylation of FSD-95 regulates association with cell membranes and interaction with K+ channel, Kv1.4. Neuron 20, 125-134.
44. 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.
45. van de Goor, J., and Kelly, R. B. (1996). Association of Drosophila cysteine string proteins with membranes. FEBS Lett. 380, 251-256.
46. Veit, M., Kretzschmar, E., Kuroda, K., Garten, W., Schmidt, M.F.G., Klenk, H.-D., and Rott, R. (1991). Site-specific mutagenesis identifies three cysteine residues in the cytoplasmic tail as acylation sites of influenza virus hemagglutinin. J. Virol. 65, 2491-2500.
47. Washbourne, P., Cansino, V., Mathews, J. R., Graham, M., Burgoyne, R. D., and Wilson, M. C. (2000). Cysteine residues of SNAP-25 are required for SNARE disassembly and exocytosis, but not for membrane targeting. Biochem. J. 357, 625-634.
48. 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.
49. Zhang, H., Peters, K. W., Sun, F., Marino, C. R., Lang, J., Burgoyne, R. D., and Frizzell, R. A. (2002). Cysteine-string protein interacts with and modulates the maturation of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 277, 28948-28958.
50. Zhang, H., Schmidt, B. Z., Sun, F., Condliffe, S. B., Butterworth, M. B., Youker, R. T., Brodsky, J. L., Aridor, M. and Frizzell, R. A. (2006). Cysteine-string protein monitors late steps in CFTR biogenesis. J. Biol. Chem. 281, 11312-11321.
51. 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.