Individual S-acylated cysteines differentially contribute to H-Ras endomembrane traffcking and acylation/deacylation cycles

Molecular Biology of the Cell

Volumn 28, Issue 7, 2017, Pages 962-974

  Pedro, Maria P ^a   Vilcaes, Aldo A ^a   Gomez, Guillermo A ^b   Daniotti, Jose L ^a  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CYAN FLUORESCENT PROTEIN; CYSTEINE; PALMITOYL PROTEIN THIOESTERASE; YELLOW FLUORESCENT PROTEIN; PROTEIN; THIOL ESTER HYDROLASE;

ACYLATION; ACYLATION AND DEACYLATION; ARTICLE; BLEACHING; CELL MEMBRANE; CELL MEMBRANE TRANSPORT; CELL MIGRATION; CELL MUTANT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEACYLATION; GOLGI COMPLEX; ONCOGENE H RAS; PHOTOACTIVATION; PRIORITY JOURNAL; ANIMAL; CELL LINE; CHO CELL LINE; CRICETULUS; METABOLISM; MUTATION; ONCOGENE RAS; PHYSIOLOGY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ACYLATION; ANIMALS; CELL LINE; CELL MEMBRANE; CHO CELLS; CRICETULUS; CYSTEINE; GENES, RAS; GOLGI APPARATUS; MUTATION; PROTEIN TRANSPORT; PROTEINS; SIGNAL TRANSDUCTION; THIOLESTER HYDROLASES;

EID: 85016830065     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E16-08-0603     Document Type: Article

References (59)

1. Agudo-Ibanez L, Herrero A, Barbacid M, Crespo P (2015). H-ras distribution and signaling in plasma membrane microdomains are regulated by acylation and deacylation events. Mol Cell Biol 35, 1898-1914.
2. Ahearn IM, Haigis K, Bar-Sagi D, Philips MR (2012). Regulating the regulator: post-translational modifcation of RAS. Nat Rev Mol Cell Biol 13, 39-51.
3. Ahearn IM, Tsai FD, Court H, Zhou M, Jennings BC, Ahmed M, Fehren-bacher N, Linder ME, Philips MR (2011). FKBP12 binds to acylated H-ras and promotes depalmitoylation. Mol Cell 41, 173-185.
4. Arozarena I, Calvo F, Crespo P (2011). Ras, an actor on many stages: post-translational modifcations, localization, and site-specifed events. Genes Cancer 2, 182-194.
5. Baines AT, Xu D, Der CJ (2011). Inhibition of Ras for cancer treatment: the search continues. Future Med Chem 3, 1787-1808.
6. Beronja S, Janki P, Heller E, Lien WH, Keyes BE, Oshimori N, Fuchs E (2013). RNAi screens in mice identify physiological regulators of oncogenic growth. Nature 501, 185-190.
7. Chamberlain LH, Shipston MJ (2015). The physiology of protein S-acylation. Physiol Rev 95, 341-376.
8. Chen HQ, Tannous M, Veluthakal R, Amin R, Kowluru A (2003). Novel roles for palmitoylation of Ras in IL-1 beta-induced nitric oxide release and caspase 3 activation in insulin-secreting beta cells. Biochem Pharmacol 66, 1681-1694.
9. Chiu VK, Bivona T, Hach A, Sajous JB, Silletti J, Wiener H, Johnson RL 2nd, Cox AD, Philips MR (2002). Ras signalling on the endoplasmic reticulum and the Golgi. Nat Cell Biol 4, 343-350.
10. Choy E, Chiu VK, Silletti J, Feoktistov M, Morimoto T, Michaelson D, Ivanov IE, Philips MR (1999). Endomembrane traffcking of ras: the CAAX motif targets proteins to the ER and Golgi. Cell 98, 69-80.
11. Christner C, Wyrwa R, Marsch S, Kullertz G, Thiericke R, Grabley S, Schumann D, Fischer G (1999). Synthesis and cytotoxic evaluation of cycloheximide derivatives as potential inhibitors of FKBP12 with neuro-regenerative properties. J Med Chem 42, 3615-3622.
12. Cox AD, Der CJ, Philips MR (2015). Targeting RAS membrane association: back to the future for Anti-RAS drug discovery? Clin Cancer Res 21, 1819-1827.
13. Crespo PM, Zurita AR, Daniotti JL (2002). Effect of gangliosides on the distribution of a glycosylphosphatidylinositol-anchored protein in plasma membrane from Chinese hamster ovary-K1 cells. J Biol Chem 277, 44731-44739.
14. Dallavilla T, Abrami L, Sandoz PA, Savoglidis G, Hatzimanikatis V, van der Goot FG (2016). Model-driven understanding of palmitoylation dynamics: Regulated acylation of the endoplasmic reticulum chaperone calnexin. PLoS Comput Biol 12, e1004774.
15. Dekker FJ, Rocks O, Vartak N, Menninger S, Hedberg C, Balamurugan R, Wetzel S, Renner S, Gerauer M, Scholermann B, et al. (2010). Small-molecule inhibition of APT1 affects Ras localization and signaling. Nat Chem Biol 6, 449-456.
16. Di Fiore P P, Gill GN (1999). Endocytosis and mitogenic signaling. Curr Opin Cell Biol 11, 483-488.
17. Duncan JA, Gilman AG (1998). A cytoplasmic acyl-protein thioesterase that removes palmitate from G protein alpha subunits and p21(RAS). J Biol Chem 273, 15830-15837.
18. Eisenberg S, Laude AJ, Beckett AJ, Mageean CJ, Aran V, Hernandez-Valladares M, Henis YI, Prior IA (2013). The role of palmitoylation in regulating Ras localization and function. Biochem Soc Trans 41, 79-83.
19. Giraudo CG, Rosales Fritz VM, Maccioni HJ (1999). GA2/GM2/GD2 syn-thase localizes to the trans-golgi network of CHO-K1 cells. Biochem J 342, 633-640.
20. Gomez GA, Daniotti JL (2005). H-Ras dynamically interacts with recycling endosomes in CHO-K1 cells: involvement of Rab5 and Rab11 in the traffcking of H-Ras to this pericentriolar endocytic compartment. J Biol Chem 280, 34997-35010.
21. Gomez GA, Daniotti JL (2007). Electrical properties of plasma membrane modulate subcellular distribution of K-Ras. FEBS J 274, 2210-2228.
22. Goodwin JS, Drake KR, Rogers C, Wright L, Lippincott-Schwartz J, Philips MR, Kenworthy AK (2005). Depalmitoylated Ras traffcs to and from the Golgi complex via a nonvesicular pathway. J Cell Biol 170, 261-272.
23. Gorfe AA, McCammon JA (2008). Similar membrane affnity of mono-and di-S-acylated ras membrane anchors: a new twist in the role of protein lipidation. J Am Chem Soc 130, 12624-12625.
24. Hancock JF (2003). Ras proteins: different signals from different locations. Nat Rev Mol Cell Biol 4, 373-384.
25. Hedberg C, Dekker FJ, Rusch M, Renner S, Wetzel S, Vartak N, Gerding-Reimers C, Bon RS, Bastiaens PI, Waldmann H (2011). Development of highly potent inhibitors of the Ras-targeting human acyl protein thioesterases based on substrate similarity design. Angew Chem Int Ed Engl 50, 9832-9837.
26. Hobbs GA, Der CJ, Rossman KL (2016). RAS isoforms and mutations in cancer at a glance. J Cell Sci 129, 1287-1292.
27. Iglesias-Bartolome R, Crespo PM, Gomez GA, Daniotti JL (2006). The antibody to GD3 ganglioside, R24, is rapidly endocytosed and recycled to the plasma membrane via the endocytic recycling compartment. Inhibitory effect of brefeldin A and monensin. FEBS J 273, 1744-1758.
28. Jiang X, Sorkin A (2002). Coordinated traffc of Grb2 and Ras during epider-mal growth factor receptor endocytosis visualized in living cells. Mol Biol Cell 13, 1522-1535.
29. Kanaani J, Patterson G, Schaufele F, Lippincott-Schwartz J, Baekkeskov S (2008). A palmitoylation cycle dynamically regulates partitioning of the GABA-synthesizing enzyme GAD65 between ER-Golgi and post-Golgi membranes. J Cell Sci 121, 437-449.
30. Lawrence DS, Zilfou JT, Smith CD (1999). Structure-activity studies of ceru-lenin analogues as protein palmitoylation inhibitors. J Med Chem 42, 4932-4941.
31. Liang X, Lu Y, Neubert TA, Resh MD (2002). Mass spectrometric analysis of GAP-43/neuromodulin reveals the presence of a variety of fatty acylated species. J Biol Chem 277, 33032-33040.
32. Lin DT, Conibear E (2015a). ABHD17 proteins are novel protein depalmi-toylases that regulate N-Ras palmitate turnover and subcellular localization. Elife 4, e11306.
33. Lin DT, Conibear E (2015b). Enzymatic protein depalmitoylation by acyl protein thioesterases. Biochem Soc Trans 43, 193-198.
34. Lobo S, Greentree WK, Linder ME, Deschenes RJ (2002). Identifcation of a Ras palmitoyltransferase in Saccharomyces cerevisiae. J Biol Chem 277, 41268-41273.
35. Paladino S, Pocard T, Catino MA, Zurzolo C (2006). GPI-anchored proteins are directly targeted to the apical surface in fully polarized MDCK cells. J Cell Biol 172, 1023-1034.
36. Patterson GH, Lippincott-Schwartz J (2004). Selective photolabeling of proteins using photoactivatable GFP. Methods 32, 445-450.
37. Pedro M P, Vilcaes AA, Tomatis VM, Oliveira RG, Gomez GA, Daniotti JL (2013). 2-Bromopalmitate reduces protein deacylation by inhibition of acyl-protein thioesterase enzymatic activities. PLoS One 8, e75232.
38. Pol A, Calvo M, Enrich C (1998). Isolated endosomes from quiescent rat liver contain the signal transduction machinery. Differential distribution of activated Raf-1 and Mek in the endocytic compartment. FEBS Lett 441, 34-38.
39. Polishchuk R, Di Pentima A, Lippincott-Schwartz J (2004). Delivery of raft-associated, GPI-anchored proteins to the apical surface of polarized MDCK cells by a transcytotic pathway. Nat Cell Biol 6, 297-307.
40. Rizzo MA, Kraft CA, Watkins SC, Levitan ES, Romero G (2001). Agonist-dependent traffc of raft-associated Ras and Raf-1 is required for activation of the mitogen-activated protein kinase cascade. J Biol Chem 276, 34928-34933.
41. Rizzo MA, Shome K, Watkins SC, Romero G (2000). The recruitment of Raf-1 to membranes is mediated by direct interaction with phosphatidic acid and is independent of association with Ras. J Biol Chem 275, 23911-23918.
42. 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.
43. Rocks O, Peyker A, Kahms M, Verveer PJ, Koerner C, Lumbierres M, Kuhlmann J, Waldmann H, Wittinghofer A, Bastiaens PI (2005). An acylation cycle regulates localization and activity of palmitoylated Ras isoforms. Science 307, 1746-1752.
44. Roy S, Plowman S, Rotblat B, Prior IA, Muncke C, Grainger S, Parton RG, Henis YI, Kloog Y, Hancock JF (2005). Individual palmitoyl residues serve distinct roles in H-ras traffcking, microlocalization, and signaling. Mol Cell Biol 25, 6722-6733.
45. Ruggiero FM, Vilcaes AA, Iglesias-Bartolome R, Daniotti JL (2015). Critical role of evolutionarily conserved glycosylation at Asn211 in the intracellular traf-fcking and activity of sialyltransferase ST3Gal-II. Biochem J 469, 83-95.
46. Rusch M, Zimmermann TJ, Burger M, Dekker FJ, Gormer K, Triola G, Brockmeyer A, Janning P, Bottcher T, Sieber SA, et al. (2011). Identifca-tion of acyl protein thioesterases 1 and 2 as the cellular targets of the Ras-signaling modulators palmostatin B and M. Angew Chem Int Ed Engl 50, 9838-9842.
47. Salaun C, Greaves J, Chamberlain LH (2010). The intracellular dynamic of protein palmitoylation. J Cell Biol 191, 1229-1238.
48. Silvius JR, Bhagatji P, Leventis R, Terrone D (2006). K-ras4B and prenylated proteins lacking "second signals" associate dynamically with cellular membranes. Mol Biol Cell 17, 192-202.
49. Spiegel J, Cromm PM, Zimmermann G, Grossmann TN, Waldmann H (2014). Small-molecule modulation of Ras signaling. Nat Chem Biol 10, 613-622.
50. Swarthout JT, Lobo S, Farh L, Croke MR, Greentree WK, Deschenes RJ, Linder ME (2005). DHHC9 and GCP16 constitute a human protein fatty acyltransferase with specifcity for H-and N-Ras. J Biol Chem 280, 31141-31148.
51. Tomatis VM, Trenchi A, Gomez GA, Daniotti JL (2010). Acyl-protein thioes-terase 2 catalyzes the deacylation of peripheral membrane-associated GAP-43. PLoS One 5, e15045.
52. Trenchi A, Gomez GA, Daniotti JL (2009). Dual acylation is required for traffcking of growth-associated protein-43 (GAP-43) to endosomal recycling compartment via an Arf6-associated endocytic vesicular pathway. Biochem J 421, 357-369.
53. Verstraeten VL, Peckham LA, Olive M, Capell BC, Collins FS, Nabel EG, Young SG, Fong LG, Lammerding J (2011). Protein farnesylation inhibi-tors cause donut-shaped cell nuclei attributable to a centrosome separation defect. Proc Natl Acad Sci USA 108, 4997-5002.
54. Wan J, Roth AF, Bailey AO, Davis NG (2007). Palmitoylated proteins: purif-cation and identifcation. Nat Protoc 2, 1573-1584.
55. Wennerberg K, Rossman KL, Der CJ (2005). The Ras superfamily at a glance. J Cell Sci 118, 843-846.
56. Wright L P, Philips MR (2006). Thematic review series: Lipid posttranslational modifcations. CAAX modifcation and membrane targeting of Ras. J Lipid Res 47, 883-891.
57. Xu J, Hedberg C, Dekker FJ, Li Q, Haigis KM, Hwang E, Waldmann H, Shannon K (2012). Inhibiting the palmitoylation/depalmitoylation cycle selectively reduces the growth of hematopoietic cells expressing onco-genic Nras. Blood 119, 1032-1035.
58. Yokoi N, Fukata Y, Sekiya A, Murakami T, Kobayashi K, Fukata M (2016). Identifcation of PSD-95 depalmitoylating enzymes. J Neurosci 36, 6431-6444.
59. Zeidman R, Jackson CS, Magee AI (2009). Protein acyl thioesterases (Review). Mol Membr Biol 26, 32-41.