Enzymatic protein depalmitoylation by acyl protein thioesterases

Biochemical Society Transactions

Volumn 43, Issue , 2015, Pages 193-198

  Lin, David T S ^a   Conibear, Elizabeth ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Acyl protein thioesterases 1 (APT1); Acyl protein thioesterases 2 (APT2); Palmitoylation; Palmostatin B; Protein depalmitoylation; Thioesterase

Indexed keywords

ESTERASE; PALMITOYL PROTEIN THIOESTERASE; PALMITOYL PROTEIN THIOESTERASE 1; UNCLASSIFIED DRUG; CYSTEINE; LYPLA1 PROTEIN, HUMAN; LYPLA2 PROTEIN, HUMAN; PALMITIC ACID DERIVATIVE; THIOL ESTER HYDROLASE;

ARTICLE; BIOINFORMATICS; CRYSTAL STRUCTURE; ENZYME ACTIVITY; FLUORESCENCE LIFETIME IMAGING MICROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENETICS; HUMAN; MAMMAL CELL; MICROSCOPY; MOLECULAR CLONING; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN DEPALMITOYLATION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; DRUG DEVELOPMENT; LIPOYLATION; METABOLISM; PROTEIN TRANSPORT;

CYSTEINE; DRUG DISCOVERY; HUMANS; LIPOYLATION; PALMITATES; PROTEIN TRANSPORT; THIOLESTER HYDROLASES;

EID: 84934935753     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20140235     Document Type: Article

References (52)

1. Linder, M. E. and Deschenes, R. J. (2007) Palmitoylation: policing protein stability and traffic. Nat. Rev. Mol. Cell Biol. 8, 74-84
2. Omary, M. B. and Trowbridge, I. S. (1981) Biosynthesis of the human transferrin receptor in cultured cells. J. Biol. Chem. 256, 12888-12892 PubMed
3. Staufenbiel, M. (1987) Ankyrin-bound fatty acid turns over rapidly at the erythrocyte plasma membrane. Mol. Cell Biol. 7, 2981-2984 PubMed
4. 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 PubMed
5. Wedegaertner, P. B. and Bourne, H. R. (1994) Activation and depalmitoylation of Gs alpha. Cell 77, 1063-1070
6. Lobo, S., Greentree, W. K., Linder, M. E. and Deschenes, R. J. (2002) Identification of a Ras palmitoyltransferase in Saccharomyces cerevisiae. J. Biol. Chem. 277, 41268-41273
7. 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. 14, 23-28
8. Young, F. B., Butland, S. L., Sanders, S. S., Sutton, L. M. and Hayden, M. R. (2012) Putting proteins in their place: Palmitoylation in Huntington disease and other neuropsychiatric diseases. Prog. Neurobiol. 97, 220-238
9. Long, J. Z. and Cravatt, B. F. (2011) The metabolic serine hydrolases and their functions in mammalian physiology and disease. Chem. Rev. 111, 6022-6063
10. Camp, L. A. and Hofmann, S. L. (1993) Purification and properties of a palmitoyl-protein thioesterase that cleaves palmitate from H-Ras. J. Biol. Chem. 268, 22566-22574 PubMed
11. Camp, L. A., Verkruyse, L. A., Afendis, S. J., Slaughter, C. A. and Hofmann, S. L. (1994) Molecular cloning and expression of palmitoyl-protein thioesterase. J. Biol. Chem. 269, 23212-23219 PubMed
12. Bellizzi, J. J. 3rd, Widom, J., Kemp, C., Lu, J. Y., Das, A. K., Hofmann, S. L. and Clardy, J. (2000) The crystal structure of palmitoyl protein thioesterase 1 and the molecular basis of infantile neuronal ceroid lipofuscinosis. Proc. Natl. Acad. Sci. U. S. A. 97, 4573-4578
13. Verkruyse, L. A. and Hofmann, S. L. (1996) Lysosomal targeting of palmitoyl-protein thioesterase. J. Biol. Chem. 271, 15831-15836
14. Hellsten, E., Vesa, J., Olkkonen, V. M., Jalanko, A. and Peltonen, L. (1996) Human palmitoyl protein thioesterase: evidence for lysosomal targeting of the enzyme and disturbed cellular routing in infantile neuronal ceroid lipofuscinosis. EMBO J. 15, 5240-5245 PubMed
15. Vesa, J., Hellsten, E., Verkruyse, L. A., Camp, L. A., Rapola, J., Santavuori, P., Hofmann, S. L. and Peltonen, L. (1995) Mutations in the palmitoyl protein thioesterase gene causing infantile neuronal ceroid lipofuscinosis. Nature 376, 584-587
16. Kim, S. J., Zhang, Z., Sarkar, C., Tsai, P. C., Lee, Y. C., Dye, L. and Mukherjee, A. B. (2008) Palmitoyl protein thioesterase-1 deficiency impairs synaptic vesicle recycling at nerve terminals, contributing to neuropathology in humans and mice. J. Clin. Invest. 118, 3075-3086
17. Duncan, J. A. and Gilman, A. G. (1998) A cytosoplasmic acyl-protein thioesterase that removes palmitate from G protein alpha subunits and p21 (RAS). J. Biol. Chem. 273, 15830-15837
18. Sugimoto, H., Hayashi, H. and Yamashita, S. (1996) Purification, cDNA cloning, and regulation of lysophospholipase from rat liver. J. Biol. Chem. 271, 7705-7711
19. Devedjiev, Y., Dauter, Z., Kuznetsov, S. R., Jones, T. L. and Derewenda, Z. S. (2000) Crystal structure of the human acyl protein thioesterase I from a single x-ray data set to 1.5 A. Structure 8, 1137-1146
20. Hirano, T., Kishi, M., Sugimoto, H., Taguchi, R., Obinata, H., Ohshima, N., Tatei, K. and Izumi, T. (2009) Thioesterase activity and subcellular localization of acylprotein thioesterase 1/lysophospholipase 1. Biochem. Biophys. Acta 1791, 797-805
21. Duncan, J. A. and Gilman, A. G. (2002) Characterization of Saccharomyces cerevisiae acyl-protein thioesterase 1, the enzyme responsible for G protein alpha subunit deacylation in vivo. J. Biol. Chem. 277, 31740-31752
22. Yeh, D. C., Duncan, J. A., Yamashita, S. and Michel, T. (1999) Depalmitoylation of endothelial nitric-oxide synathase by acyl-protein thioesterase 1 is potentiated by Ca (2+)-calmodulin. J. Biol. Chem. 274, 33148-33154
23. Flaumenhaft, R., Rozenvayn, N., Feng, D. and Dvorak, A. M. (2007) SNAP-23 and syntaxin-2 localize to the extracellular surface of the platelet plasma membrane. Blood 110, 1492-1501
24. Veit, M. and Schmidt, M. F. (2001) Enzymatic depalmitoylation of viral glycoproteins with acyl-protein thioesterase 1 in vitro. Virology 288, 89-95
25. Siegel, G., Obernosterer, G., Fiore, R., Oehmen, M., Bicker, S., Christensen, M., Khudayberdiev, S., Leuschner, P. F., Busch, C. J., Kane, C. et al. (2009) A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nat. Cell Biol. 11, 705-716
26. 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
27. Zeidman, R., Jackson, C. S. and Magee, A. I. (2009) Analysis of protein acylation. Curr. Protoc. Protein Sci. Chapter 14, Unit 14.2 PubMed
28. Toyoda, T., Sugimoto, H. and Yamashita, S. (1999) Sequence, expression in Escherichia coli, and characterization of lysophospholipase II. Biochim. Biophys. Acta 1437, 182-193
29. Tomatis, V. M., Trenchi, A., Gomez, G. A. and Daniotti, J. L. (2010) Acyl-protein thioesterase 2 catalyzes the deacylation of peripheral memberane-associated GAP-43. PLoS One 5, e15045
30. Rusch, M., Zimmermann, T. J., Bürger, M., Dekker, F. J., Görmer, K., Triola, G., Brockmeyer, A., Janning, P., Böttcher, T., Sieber, S. A. et al. (2011) Identification 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
31. Lindgren, C. M., Heid, I. M., Randall, J. C., Lamina, C., Steinthorsdottir, V., Qi, L., Speliotes, E. K., Thorleifsson, G., Willer, C. J., Herrera, B. M. et al. (2009) Genome-wide association scan meta-analysis identifies three loci influencing adiposity and fat distribution. PLoS Genet. 5, e1000508
32. Sepeliotes, E. K., Yerges-Armstrong, L. M., Wu, J., Hernaez, R., Kim, L. J., Palmer, C. D., Gudnason, V., Eiriksdottir, G., Garcia, M. E., Launer, L. J. et al. (2011) Genome-wide association analysis identifies variants associated with nonalcoholic fatty liver disease that have distinct effects on metabolic traits. PLoS Genet. 7, e1001324
33. 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
34. Bürger, M., Zimmermann, T. J., Kondoh, Y., Stege, P., Watanabe, N., Osada, H., Waldmann, H. and Vetter, I. R. (2012) Crystal structure of the predicted phospholipase LYPLAL1 reveals unexpected functional plasticity despite close relationship to acyl protein thioesterases. J. Lipid Res. 53, 43-50
35. Shahinian, S. and Silvius, J. R. (1995) Doubly-lipid-modified protein sequence motifs exhibit long-lived anchorage to lipid bilayer membranes. Biochemistry 34, 3813-3822
36. 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
37. Kong, E., Peng, S., Chandra, G., Sarkar, C., Zhang, Z., Bagh, M. B. and Mukherjee, A. B. (2013) Dynamic palmitoylation links cytosol-membrane shuttling of acyl-protein thioesterase-1 and acyl-protein thioesterase-2 with that of proto-oncogene H-ras product and growth-associated protein-43. J. Biol. Chem. 288, 9112-9125
38. Vartak, N., Papke, B., Grecco, H. E., Rossmannek, L., Waldmann, H., Hedberg, C. and Bastiaens, P. I. (2014) The autodepalmitoylating activity of APT maintains the spatial organization of palmitoylated membrane proteins. Biophys. J. 106, 93-105
39. Ahearn, I. M., Tsai, F. D., Court, H., Zhou, M., Jennings, B. C., Ahmed, M., Fehrenbacher, N., Linder, M. E. and Philips, M. R. (2011) FKBP12 binds to acylated H-ras and promotes depalmitoylation. Mol. Cell 41, 173-185
40. Chandra, A., Grecco, H. E., Pisupati, V., Perera, D., Cassidy, L., Skoulidis, F., Ismail, S. A., Hedberg, C., Hanzal-Bayer, M., Venkitaraman, A. R. et al. (2012) The GDI-like solubilizing factor PDEγ sustains the spatial organization and signalling of Ras family proteins. Nat. Cell Biol. 14, 148-158
41. Frénal, K., Kemp, L. E. and Soldati-Favre, D. (2014) Emerging roles for protein S-palmitoylation in Toxoplasma biology. Int. J. Parasitol. 44, 121-131
42. Kemp, L. E., Rusch, M., Adibekian, A., Bullen, H. E., Graindorge, A., Freymond, C., Rottmann, M., Braun-Breton, C., Baumeister, S., Porfetye, A. T. et al. (2013) Characterization of a serine hydrolase targeted by acyl-protein thioesterase inhibitors in Toxoplasma gondii. J. Biol. Chem. 288, 27002-27018
43. Child, M. A., Hall, C. I., Beck, J. R., Ofori, L. O., Albrow, V. E., Garland, M., Bowyer, P. W., Bradley, P. J., Powers, J. C., Boothroyd, J. C. et al. (2013) Small-molecule inhibition of a depalmitoylase enhances Toxoplasma host-cell invasion. Nat. Chem. Biol. 9, 651-656
44. Martin, B. R., Wang, C., Adibekian, A., Tully, S. E. and Cravatt, B. F. (2011) Global profiling of dynamic protein palmitoylation. Nat. Methods 9, 84-89
45. Adibekian, A., Martin, B. R., Chang, J. W., Hsu, K. L., Tsuboi, K., Bachovchin, D. A., Speers, A. E., Brown, S. J., Spicer, T., Fernandez-Vega, V. et al. (2012) Confirming target engagement for reversible inhibitors in vivo by kinetically tuned activity-based probes. J. Am. Chem. Soc. 134, 10345-10348
46. Jia, L., Chisari, M., Maktabi, M. H., Sobieski, C., Zhou, H., Konopko, A. M., Martin, B. R., Mennerick, S. J. and Blumer, K. J. (2014) A mechanism regulating G protein-coupled receptor signaling that requires cycles of protein palmitoylation and depalmitoylation. J. Biol. Chem. 289, 6249-6257
47. Drisdel, R. C. and Green, W. N. (2004) Labeling and quantifying sites of protein palmitoylation. Biotechniques 36, 276-285 PubMed
48. Bertiaume, L., Peseckis, S. M. and Resh, M. D. (1995) Synthesis and use of iodo-fatty acid analogs. Methods Enzymol 250, 454-466
49. Hang, H. C., Geutjes, E. J., Grotenbreg, G., Pollington, A. M., Bijlmakers, M. J. and Ploegh, H. L. (2007) Chemical probes for the rapid detection of fatty-acylated proteins in mammalian cells. J. Am. Chem. Soc. 129, 2744-2745
50. Zhang, M. M., Tsou, L. K., Charron, G., Raghavan, A. S. and Hang, H. C. (2010) Tandem fluorescence imaging of dynamic S-acylation and protein turnover. Proc. Natl. Acad. Sci. U. S. A. 107, 8627-8632
51. 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
52. Noritake, J., Fukata, Y., Iwanaga, T., Hosomi, N., Tsutsumi, R., Matsuda, N., Tani, H., Iwanari, H., Mochizuki, Y., Kodama, T. et al. (2009) Mobile DHHC palmitoylating enzyme mediates activity-sensitive synaptic targeting of PSD-95. J. Cell Biol. 186, 147-160