Palmitoylation and the trafficking of peripheral membrane proteins

Biochemical Society Transactions

Volumn 41, Issue 1, 2013, Pages 62-66

  Chamberlain, Luke H ^a   Lemonidis, Kimon ^a   Sanchez Perez, Maria ^a   Werno, Martin W ^a   Gorleku, Oforiwa A ^a   Greaves, Jennifer ^a  

^a UNIVERSITY OF STRATHCLYDE   (United Kingdom)

Author keywords

25 kDa synaptosome associated protein (SNAP25); Cysteine string protein; DHHC protein; Palmitoylation

Indexed keywords

MEMBRANE PROTEIN; PALMITIC ACID; RAS PROTEIN;

CELLULAR DISTRIBUTION; CONFERENCE PAPER; ENDOSOME; EXOCYTOSIS; HUMAN; HYDROPHOBICITY; MOLECULAR DYNAMICS; NEURONAL CEROID LIPOFUSCINOSIS; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN TRANSPORT;

CELL MEMBRANE; GOLGI APPARATUS; LIPOYLATION; MEMBRANE PROTEINS; PALMITIC ACID; PROTEIN TRANSPORT; RAS PROTEINS; SUBCELLULAR FRACTIONS; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25;

EID: 84873103052     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20120243     Document Type: Conference Paper

References (47)

1. Mitchell, D. A., Vasudevan, A., Linder, M. E. and Deschenes, R. J. (2006) Protein palmitoylation by a family of DHHC protein S-acyltransferases. J. Lipid Res. 47, 1118-1127 (Pubitemid 43830703)
2. Greaves, J. and Chamberlain, L. H. (2011) DHHC palmitoyl transferases: substrate interactions and (patho) physiology. Trends Biochem. Sci. 26, 245-253
3. Fukata, M., Fukata, Y., Adesnik, H., Nicoll, R. A. and Bredt, D. S. (2004) Identification of PSD-95 palmitoylating enzymes. Neuron 44, 987-996 (Pubitemid 39643094)
4. Ohno, Y., Kihara, A., Sano, T. and Igarashi, Y. (2006) Intracellular localization and tissue-specific distribution of human and yeast DHHC cysteine-rich domain-containing proteins. Biochim. Biophys. Acta 1761, 474-483 (Pubitemid 43776463)
5. Roth, A. F., Wan, J., Bailey, A. O., Sun, B., Kuchar, J. A., Green, W. N., Phinney, B. S., Yates, III, J. R. and Davis, N. G. (2006) Global analysis of protein palmitoylation in yeast. Cell 125, 1003-1013 (Pubitemid 43795188)
6. Kümmel, D., Heinemann, U. and Veit, M. (2006) Unique self-palmitoylation activity of the transport protein particle component Bet3: a mechanism required for protein stability. Proc. Natl. Acad. Sci. U. S. A. 103, 12701-12706 (Pubitemid 44298624)
7. Politis, E. G., Roth, A. F. and Davis, N. G. (2005) Transmembrane topology of the protein palmitoyl transferase Akr1. J. Biol. Chem. 280, 10156-10163 (Pubitemid 40395869)
8. Kang, R., Wan, J., Arstikaitis, P., Takahashi, H., Huang, K., Bailey, A. O., Thompson, J. X., Roth, A. F., Drisdel, R. C., Mastro, R. et al. (2008) Neural palmitoyl-proteomics reveals dynamic synaptic palmitoylation. Nature 456, 904-909
9. Salaun, C., Greaves, J. and Chamberlain, L. H. (2010) The intracellular dynamic of protein palmitoylation. J. Cell Biol. 191, 1229-1238
10. Rocks, O. (2005) An acylation cycle regulates localization and activity of palmitoylated Ras isoforms. Science 307, 1746-1752 (Pubitemid 40388611)
11. Duncan, J. A. and Gilman, A. G. (1998) A cytoplasmic acyl-protein thioesterase that removes palmitate from G protein a subunits and p21RAS. J. Biol. Chem. 273, 15830-15837 (Pubitemid 28298205)
12. Tian, L., McClafferty, H., Knaus, H.-G., Ruth, P. and Shipston, M. J. (2012) Distinct acyl protein transferases and thioesterases control surface expression of calcium-activated potassium channels. J. Biol. Chem. 287, 14718-14725
13. Tomatis, V. M., Trenchi, A., Gomez, G. A. and Daniotti, J. L. (2010) Acyl-protein thioesterase 2 catalyzes the deacylation of peripheral membrane-associated GAP-43. PLoS ONE 5, e15045
14. Whelan, J. T., Hollis, S. E., Cha, D. S., Asch, A. S. and Lee, M.-H. (2012) Post-transcriptional regulation of the Ras-ERK/MAPK signaling pathway. J. Cell. Physiol. 227, 1235-1241
15. Pylayeva-Gupta, Y., Grabocka, E. and Bar-Sagi, D. (2011) RAS oncogenes: weaving a tumorigenic web. Nat. Rev. Cancer 11, 761-774
16. Hancock, J. F., Magee, A. I., Childs, J. E. and Marshall, C. J. (1989) All ras proteins are polyisoprenylated but only some are palmitoylated. Cell 57, 1167-1177 (Pubitemid 19169813)
17. Shahinian, S. and Silvius, J. (1995) Doubly-lipid-modified protein sequence motifs exhibit long-lived anchorage to lipid bilayer membranes. Biochemistry 34, 3813-3822
18. 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 (Pubitemid 29331197)
19. Hancock, J. F., Paterson, H. and Marshall, C. J. (1990) A polybasic domain or palmitoylation is required in addition to the CAAX motif to localize p21ras to the plasma membrane. Cell 63, 133-139
20. Rocks, O., Gerauer, M., Vartak, N., Koch, S., Huang, Z.-P., Pechlivanis, M., Kuhlmann, J., Brunsveld, L., Chandra, A., Ellinger, B. et al. (2010) The palmitoylation machinery is a spatially organizing system for peripheral membrane proteins. Cell 141, 458-471
21. Goodwin, J. S., Drake, K. R., Rogers, C., Wright, L., Lippincott-Schwartz, J., Philips, M. R. and Kenworthy, A. K. (2005) Depalmitoylated Ras traffics to and from the Golgi complex via a nonvesicular pathway. J. Cell Biol. 170, 261-272 (Pubitemid 41043808)
22. 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 acyltransferase with specificity for H-and N-Ras. J. Biol. Chem. 280, 31141-31148 (Pubitemid 41291850)
23. Dekker, F. J., Rocks, O., Vartak, N., Menninger, S., Hedberg, C., Balamurugan, R., Wetzel, S., Renner, S., Gerauer, M., Schölermann, B. et al. (2010) Small-molecule inhibition of APT1 affects Ras localization and signaling. Nat. Chem. Biol. 6, 449-456
24. Rocks, O., Peyker, A., Kahms, M., Verveer, P. J., Koerner, C., Lumbierres, M., Kuhlmann, J., Waldmann, H., Wittinghofer, A. and Bastiaens, P. I. H. (2005) An acylation cycle regulates localization and activity of palmitoylated Ras isoforms. Science 307, 1746-1752 (Pubitemid 40388611)
25. Veit, M., Söllner, T. H. and Rothman, J. E. (1996) Multiple palmitoylation of synaptotagmin and the t-SNARE SNAP-25. FEBS Lett. 385, 119-123 (Pubitemid 26155091)
26. 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 (Pubitemid 24233432)
27. 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. (2004) The synaptic vesicle protein CSPa prevents presynaptic degeneration. Neuron 42, 237-251 (Pubitemid 38501647)
28. Nosková, L., Stránecký, V., Hartmannová, H., Přistoupilová, A., Barešová, V., Ivánek, R., Hlková, H., Jahnová, H., van der Zee, J., Staropoli et al. (2011) Mutations in DNAJC5, encoding cysteine-string protein a, cause autosomal-dominant adult-onset neuronal ceroid lipofuscinosis. Am. J. Hum. Genet. 89, 241-252
29. 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 (Pubitemid 28125618)
30. Greaves, J., Gorleku, O. A., Salaun, C. and Chamberlain, L. H. (2010) Palmitoylation of the SNAP25 protein family: specificty and regulation by DHHC palmitoyl transferases. J. Biol. Chem. 285, 24629-24638
31. Huang, K., Sanders, S., Singaraja, R., Orban, P., Cijsouw, T., Arstikaitis, P., Yanai, A., Hayden, M. R. and El-Husseini, A. (2009) Neuronal palmitoyl acyl transferases exhibit distinct substrate specificity. FASEB J. 23, 2605-2615
32. Singaraja, R. R., Huang, K., Sanders, S. S., Milnerwood, A. J., Hines, R., Lerch, J. P., Franciosi, S., Drisdel, R. C., Vaid, K., Young, F. B. et al. (2011) Altered palmitoylation and neuropathological deficits in mice lacking HIP14. Hum. Mol. Genet. 20, 3899-3909
33. Greaves, J. and Chamberlain, L. H. (2011) Differential palmitoylation regulates intracellular patterning of SNAP25. J. Cell Sci. 124, 1351-1360
34. Aikawa, Y. and Martin, T. F. J. (2003) ARF6 regulates a plasma membrane pool of phosphatidylinositol (4, 5) bisphosphate required for regulated exocytosis. J. Cell Biol. 162, 647-659 (Pubitemid 37022942)
35. Greaves, J., Prescott, G. R., Fukata, Y., Fukata, M., Salaun, C. and Chamberlain, L. H. (2009) The hydrophobic cysteine-rich domain of SNAP25 couples with downstream residues to mediate membrane interactions and recognition by DHHC palmitoyl transferases. Mol. Biol. Cell 20, 1845-1854
36. Greaves, J., Salaun, C., Fukata, Y., Fukata, M. and Chamberlain, L. H. (2008) Palmitoylation and membrane interactions of the neuroprotective chaperone cysteine-string protein. J. Biol. Chem. 283, 25014-25026
37. Greaves, J. and Chamberlain, L. H. (2006) Dual role of the cysteine-string domain in membrane binding and palmitoylation-dependent sorting of the molecular chaperone cysteine-string protein. Mol. Biol. Cell 17, 4748-4759 (Pubitemid 44665744)
38. Martin, B. R., Wang, C., Adibekian, A., Tully, S. E. and Cravatt, B. F. (2012) Global profiling of dynamic protein palmitoylation. Nat. Methods 9, 84-89
39. Magee, A. I., Gutierrez, L., McKay, I. A., Marshall, C. J. and Hall, A. (1987) Dynamic fatty acylation of p21N-ras. EMBO J. 6, 3353-3357
40. Lane, S. and Liu, S. (1997) Characterisation of the palmitoylation domain of SNAP-25. J. Neurochem. 69, 1864-1869
41. Heindel, U., Schmidt, M. F. G. and Veit, M. (2003) Palmitoylation sites and processing of synaptotagmin I, the putative calcium sensor for neurosecretion. FEBS Lett. 544, 57-62 (Pubitemid 36628036)
42. Kang, R., Swayze, R., Lise, M. F., Gerrow, K., Mullard, A., Honer, W. G. and El-Husseini, A. (2004) Presynaptic trafficking of synaptotagmin I is regulated by protein palmitoylation. J. Biol. Chem. 279, 50524-50536 (Pubitemid 39577871)
43. Aikawa, Y., Lynch, K. L., Boswell, K. L. and Martin, T. F. J. (2006) A second SNARE role for exocytic SNAP25 in endosome fusion. Mol. Biol. Cell 17, 2113-2124 (Pubitemid 44011728)
44. Salaun, C., Gould, G. W. and Chamberlain, L. H. (2005) Lipid raft association of SNARE proteins regulates exocytosis in PC12 cells. J. Biol. Chem. 280, 19449-19453 (Pubitemid 41379464)
45. Salaun, 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, 1236-40
46. Sim, D. S., Dilks, J. R. and Flaumenhaft, R. (2007) Platelets possess and require an active protein palmitoylation pathway for agonist-mediated activation and in vivo thrombus formation. Arterioscler. Thromb. Vasc. Biol. 27, 1478-1485 (Pubitemid 46809441)
47. Greaves, J., Carmichael, J. A. and Chamberlain, L. H. (2011) The palmitoyl transferase DHHC2 targets a dynamic membrane cycling pathway: regulation by a C-terminal domain. Mol. Biol. Cell 22, 1887-1895