Individual palmitoyl residues serve distinct roles in H-ras trafficking, microlocalization, and signaling

Molecular and Cellular Biology

Volumn 25, Issue 15, 2005, Pages 6722-6733

  Roy, Sandrine ^a   Plowman, Sarah ^a   Rotblat, Barak ^b   Prior, Ian A ^c   Muncke, Cornelia ^a   Grainger, Sarah ^a   Parton, Robert G ^a   Henis, Yoav I ^b   Kloog, Yoel ^b   Hancock, John F ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b TEL AVIV UNIVERSITY   (Israel)

^c UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; CYSTEINE; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; MUTANT PROTEIN; PALMITIC ACID; RAF PROTEIN; TRITIUM;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL STRAIN BHK; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; ENZYME ASSAY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GOLGI COMPLEX; ISOTOPE LABELING; NONHUMAN; ONCOGENE H RAS; ONCOGENE N RAS; PLASMID; PRIORITY JOURNAL; PROTEIN LOCALIZATION; WESTERN BLOTTING;

ANIMALS; CELL LINE; CELL MEMBRANE; CRICETINAE; CYSTEINE; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENES, RAS; GOLGI APPARATUS; KINETICS; MAP KINASE KINASE KINASES; MUTATION; ONCOGENE PROTEIN P21(RAS); PALMITIC ACIDS; PC12 CELLS; PROTEIN TRANSPORT; RAF KINASES; RATS; SERINE;

EID: 22544440260     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.15.6722-6733.2005     Document Type: Article

References (57)

1. Apolloni, A., I. A. Prior, M. Lindsay, R. G. Parton, and J. F. Hancock. 2000. H-ras but not K-ras traffics to the plasma membrane through the exocytic pathway. Mol. Cell. Biol. 20:2475-2487.
2. Axelrod, D., D. E. Koppel, J. Schlessinger, E. Elson, and W. W. Webb. 1976. Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys. J. 16:1055-1069.
3. Baker, T. L., H. Zheng, J. Walker, J. L. Coloff, and J. E. Buss. 2003. Distinct rates of palmitate turnover on membrane-bound cellular and oncogenic H-ras. J. Biol. Chem. 278:19292-19300.
4. Besag, J. E. 1977. Contribution to the discussion of Dr. Ripley's paper. J. R. Statist. Soc. B. 39:193-195.
5. Bivona, T, G., I. Perez De Castro, I. M. Ahearn, T. M. Grana, V. K. Chiu, P. J. Lockyer, P. J. Cullen, A. Pellicer, A. D. Cox, and M. R. Philips. 2003. Phospholipase Cgamma activates Ras on the Golgi apparatus apparatus by means of RasGRP1. Nature 424:694-698.
6. Bivona, T. G., and M. R. Philips. 2003. Ras pathway signaling on endomembranes. Curr. Opin. Cell Biol. 15:136-142.
7. Chiu, V. K., T. Bivona, A. Hach, J. B. Sajous, J. Silletti, H. Wiener, R. L. Johnson II, A. D. Cox, and M. R. Philips. 2002. Ras signalling on the endoplasmic reticulum and the Golgi apparatus. Nat. Cell Biol. 4:343-350.
8. Choy, E., V. K. Chiu, J. Silletti, M. Feoktistov, T. Morimoto, D. Michaelson, I. E. Ivanov, and M. R. Philips. 1999. Endomembrane trafficking of ras: the CAAX motif targets proteins to the ER and Golgi apparatus. Cell 98:69-80.
9. Coleman, R. A., P. Rao, R. J. Fogelsong, and E. S. Bardes. 1992. 2-Bromopalmitoyl-CoA and 2-bromopalmitate: promiscuous inhibitors of membrane-bound enzymes. Biochim. Biophys. Acta 1125:203-209.
10. Diggle, P. J., J. Mateu, and H. E. Clough. 2000. A comparison between parametric and non-parametric approaches to the analysis of replicated spatial point patterns. Adv. Appl. Probab. 32:331-343.
11. Dunphy, J. T., W. K. Greentree, and M. E. Linder. 2001. Enrichment of G-protein palmitoyltransferase activity in low density membranes: in vitro reconstitution of Galphai to these domains requires palmitoyltransferase activity. J. Biol. Chem. 276:43300-43304.
12. Ehrlich, M., A. Shmuely, and Y. I. Henis. 2001. A single internalization signal from the di-leucine family is critical for constitutive endocytosis of the type II TGF-beta receptor. J. Cell Sci. 114:1777-1786.
13. Elson, E. L., and J. A. Reidler. 1979. Analysis of cell surface interactions by measurements of lateral mobility. J. Supramol. Struct. 12:481-489.
14. Fukata, M., Y. Fukata, H. Adesnik, R. A. Nicoll, and D. S. Bredt. 2004. Identification of PSD-95 palmitoylating enzymes. Neuron 44:987-996.
15. Gorfe, A. A., R. Pellarin, and A. Caflisch. 2004. Membrane localization and flexibility of a lipidated ras peptide studied by molecular dynamics simulations. J. Am. Chem. Soc. 126:15277-15286.
16. Hancock, J. F. 2003. Ras proteins: different signals from different locations. Nat. Rev. Mol. Cell Biol. 4:373-384.
17. Hancock, J. F., K. Cadwallader, and C. J. Marshall. 1991. Methylation and proteolysis are essential for efficient membrane binding of prenylated p21K-ras(B). EMBO J. 10:641-646.
18. Hancock, J. F., K. Cadwallader, H. Paterson, and C. J. Marshall. 1991. A CAAX or a CAAL motif and a second signal are sufficient for plasma membrane targeting of ras proteins. EMBO J. 10:4033-4039.
19. Hancock, J. F., A. I. Magee, J. E. Childs, and C. J. Marshall. 1989. All ras proteins are polyisoprenylated but only some are palmitoylated. Cell 57: 1167-1177.
20. Hancock, J. F., and R. G. Parton. 2005. Ras plasma membrane signalling platforms. Biochem. J. 389:1-11.
21. Hancock, J. F., H. Paterson, and C. J. Marshall. 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.
22. Hua, X., J. Sakai, M. S. Brown, and J. L. Goldstein. 1996. Regulated cleavage of sterol regulatory element binding proteins requires sequences on both sides of the endoplasmic reticulum membrane. J. Biol. Chem. 271: 10379-10384.
23. Huang, K., A. Yanai, R. Kang, P. Arstikaitis, R. R. Singaraja, M. Metzler, A. Mullard, B. Haigh, C. Gauthier-Campbell, C. A. Gutekunst, M. R. Hayden, and A. El-Husseini. 2004. Huntingtin-interacting protein HIP14 is a palmitoyl transferase involved in palmitoylation and trafficking of multiple neuronal proteins. Neuron 44:977-986.
24. Huster, D., A. Vogel, C. Katzka, H. A. Scheidt, H. Binder, S. Dante, T. Gutberlet, O. Zschornig, H. Waldmann, and K. Arnold. 2003. Membrane insertion of a lipidated ras peptide studied by FTIR, solid-state NMR, and neutron diffraction spectroscopy. J. Am. Chem. Soc. 125:4070-4079.
25. Illenberger, D., C. Walliser, J. Strobel, O. Gutman, H. Niv, V. Gaidzik, Y. Kloog, P. Gierschik, and Y. I. Henis. 2003. Rac2 regulation of phospholipase C-beta 2 activity and mode of membrane interactions in intact cells. J. Biol. Chem. 278:8645-8652.
26. Janosch, S., C. Nicolini, B. Ludolph, C. Peters, M. Volkert, T. L. Hazlet, E. Gratton, H. Waldmann, and R. Winter. 2004. Partitioning of dual-lipidated peptides into membrane microdomains: lipid sorting vs peptide aggregation. J. Am. Chem. Soc. 126:7496-7503.
27. Jiang, X., and A. Sorkin. 2002. Coordinated traffic of Grb2 and Ras during epidermal growth factor receptor endocytosis visualized in living cells. Mol. Biol. Cell 13:1522-1535.
28. Kanaani, J., D. el-Husseini Ael, A. Aguilera-Moreno, J. M. Diacovo, D. S. Bredt, and S. Baekkeskov. 2002. A combination of three distinct trafficking signals mediates axonal targeting and presynaptic clustering of GAD65. J. Cell Biol. 158:1229-1238.
29. Linder, M. E., and R. J. Deschenes. 2004. Model organisms lead the way to protein palmitoyltransferases. J. Cell Sci. 117:521-526.
30. Lobo, S., W. K. Greentree, M. E. Linder, and R. J. Deschenes. 2002. Identification of a Ras palmitoyltransferase in Saccharomyces cerevisiae. J. Biol. Chem. 277:41268-41273.
31. Lu, J. Y., and S. L. Hofmann. 1995. Depalmitoylation of CAAX motif proteins. Protein structural determinants of palmitate turnover rate. J. Biol. Chem. 270:7251-7256.
32. Magee, A. I., L. Gutierrez, I. A. McKay, C. J. Marshall, and A. Hall. 1987. Dynamic fatty acylation of p21N-ras. EMBO J. 6:3353-3357.
33. Magee, A. I., and M. C. Seabra. 2005. Fatty acylation and prenylation of proteins: what's hot in fat. Curr. Opin. Cell Biol. 17:190-196.
34. Niv, H., O. Gutman, Y. I. Henis, and Y. Kloog. 1999. Membrane interactions of a constitutively active GFP-Ki-ras 4B and their role in signaling. Evidence from lateral mobility studies. J. Biol. Chem. 274:1606-1613.
35. Niv, H., O. Gutman, Y. Kloog, and Y. I. Henis. 2002. Activated K-ras and H-ras display different interactions with saturable nonraft sites at the surface of live cells. J. Cell Biol. 157:865-872.
36. Parton, R. G., and J. F. Hancock. 2001. Caveolin and Ras function. Methods Enzymol. 333:172-183.
37. Parton, R. G., and J. F. Hancock. 2004. Lipid rafts and plasma membrane microorganization: insights from Ras. Trends Cell Biol. 14:141-147.
38. Perez de Castro, I., T. G. Bivona, M. R. Philips, and A. Pellicer. 2004. Ras activation in Jurkat T cells following low-grade stimulation of the T-cell receptor is specific to N-ras and occurs only on the Golgi apparatus apparatus. Mol. Cell. Biol. 24:3485-3496.
39. Petersen, N. O., and E. L. Elson. 1986. Measurements of diffusion and chemical kinetics by fluorescence photobleaching recovery and fluorescence correlation spectroscopy. Methods Enzymol. 130:454-484.
40. Plowman, S., C. Muncke, R. G. Parton, and J. F. Hancock. H-ras, K-ras and inner plasma membrane raft proteins operate in nanoclusters with differential dependence on the actin cytoskeleton. Submitted for publication.
41. Prior, I. A., A. Harding, J. Yan, J. Sluimer, R. G. Parton, and J. F. Hancock. 2001. GTP-dependent segregation of H-ras from lipid rafts is required for biological activity. Nat. Cell Biol. 3:368-375.
42. Prior, I. A., C. Muncke, R. G. Parton, and J. F. Hancock. 2003. Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J. Cell Biol. 160:165-170.
43. Prior, I. A., R. G. Parton, and J. F. Hancock. 2003. Observing cell surface signaling domains using electron microscopy. Sci. STKE 177:p19.
44. Resh, M. D. 1996. Regulation of cellular signalling by fatty acid acylation and prenylation of signal transduction proteins. Cell Signal. 8:403-412.
45. Ripley, B. D. 1977. Modelling spatial patterns. J. R. Statist. Soc. B. 39:172-192.
46. Rizzo, M. A., C. A. Kraft, S. C. Watkins, E. S. Levitan, and G. Romero. 2001. Agonist-dependent traffic of raft-associated Ras and Raf-1 is required for activation of the mitogen-activated protein kinase cascade. J. Biol. Chem. 276:34928-34933.
47. Rocks, O., A. Peyker, M. Kahms, P. J. Verveer, C. Koerner, M. Lumbierres, J. Kuhlmann, H. Waldmann, A. Wittinghofer, and P. I. Bastiaens. 2005. An acylation cycle regulates localization and activity of palmitoylated Ras isoforms. Science 307:1746-1752.
48. Rotblat, B., I. A. Prior, C. Muncke, R. G. Parton, Y. Kloog, Y. I. Henis, and J. F. Hancock. 2004. Three separable domains regulate GTP-dependent association of H-ras with the plasma membrane. Mol. Cell. Biol. 24:6799-6810.
49. Roy, S., A. Lane, J. Yan, R. McPherson, and J. F. Hancock. 1997. Activity of plasma membrane-recruited Raf-1 is regulated by Ras via the Raf zinc finger. J. Biol. Chem. 272:20139-20145.
50. Roy, S., R. Luetterforst, A. Harding, A. Apolloni, M. Etheridge, E. Stang, B. Rolls, J. F. Hancock, and R. G. Parton. 1999. Dominant-negative caveolin inhibits H-ras function by disrupting cholesterol-rich plasma membrane domains. Nat. Cell Biol. 1:98-105.
51. Roy, S., B. Wyse, and J. F. Hancock. 2002. H-ras signaling and K-ras signaling are differentially dependent on endocytosis. Mol. Cell. Biol. 22:5128-5140.
52. Schroeder, H., R. Leventis, S. Rex, M. Schelhaas, E. Nagele, H. Waldmann, and J. R. Silvius. 1997. S-acylation and plasma membrane targeting of the farnesylated carboxyl-terminal peptide of N-ras in mammalian fibroblasts. Biochemistry 36:13102-13109.
53. Shvartsman, D. E., M. Kotler, R. D. Tall, M. G. Roth, and Y. I. Henis. 2003. Differently anchored influenza hemagglutinin mutants display distinct interaction dynamics with mutual rafts. J. Cell Biol. 163:879-888.
54. van't Hof, W., and M. D. Resh. 1997. Rapid plasma membrane anchoring of newly synthesized p59fyn: selective requirement for NH2-terminal myristoylation and palmitoylation at cysteine-3. J. Cell Biol. 136:1023-1035.
55. Verkruyse, L. A., and S. L. Hofmann. 1996. Lysosomal targeting of palmitoyl-protein thioesterase. J. Biol. Chem. 271:15831-15836.
56. Webb, Y., L. Hermida-Matsumoto, and M. D. Resh. 2000. Inhibition of protein palmitoylation, raft localization, and T cell signaling by 2-bromopalmitate and polyunsaturated fatty acids. J. Biol. Chem. 275:261-270.
57. Zhao, L., S. Lobo, X. Dong, A. D. Ault, and R. J. Deschenes. 2002. Erf4p and Erf2p form an endoplasmic reticulum-associated complex involved in the plasma membrane localization of yeast Ras proteins. J. Biol. Chem. 277: 49352-49359.