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

Journal of Biological Chemistry

Volumn 288, Issue 13, 2013, Pages 9112-9125

  Kong, Eryan ^a   Peng, Shiyong ^a   Chandra, Goutam ^a   Sarkar, Chinmoy ^a   Zhang, Zhongjian ^a   Bagh, Maria B ^a   Mukherjee, Anil B ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; CYTOSOLIC ENZYMES; MEMBRANE LOCALIZATION; PALMITOYLATION; THIOESTERASES;

ACYLATION; DYNAMICS; PROTEINS;

MEMBRANES;

CHEMICAL COMPOUND; GUANOSINE TRIPHOSPHATASE; H RAS PROTEIN; NEUROMODULIN; PALMITOYL PROTEIN THIOESTERASE; PALMITOYL PROTEIN THIOESTERASE 1; PALMITOYL PROTEIN THIOESTERASE 2; PALMOSTATIN B; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME INACTIVATION; ENZYME INHIBITION; FETUS; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SITE DIRECTED MUTAGENESIS; STEADY STATE;

ANIMALS; ASTROCYTES; CATALYTIC DOMAIN; CELL MEMBRANE; CELLS, CULTURED; CYTOSOL; GAP-43 PROTEIN; HUMANS; MICE; MICROSCOPY, CONFOCAL; MUTAGENESIS; MUTATION; NEURONS; NIH 3T3 CELLS; PALMITIC ACID; PROTEIN BINDING; RAS PROTEINS; SUBCELLULAR FRACTIONS; THIOLESTER HYDROLASES; TRANSFECTION;

EID: 84875972777     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.421073     Document Type: Article

References (33)

1. Schmidt, M. F. (1989) Fatty acylation of proteins. Biochim. Biophys. Acta 988, 411-426
2. Bijlmakers, M. J., and Marsh, M. (2003) The on-off story of protein palmitoylation. Trends Cell Biol. 13, 32-42
3. Smotrys, J. E., and Linder, M. E. (2004) Palmitoylation of intracellular signaling proteins' regulation and function. Annu. Rev. Biochem. 73, 559-587
4. el-Husseini Ael-D., and Bredt, D. S. (2002) Protein palmitoylation: a regulator of neuronal development and function. Nat. Rev. Neurosci. 3, 791-802
5. Resh, M. D. (2006). Palmitoylation of ligands receptors and intracellular signaling molecules. Sci. STKE. 2006, re14
6. Linder, M. E., and Deschenes, R. J. (2007) Palmitoylation: policing protein stability and traffic. Nat. Rev. Mol. Cell Biol. 8, 74-84
7. Fukata, Y., and Fukata, M. (2010) Protein palmitoylation in neuronal development and synaptic plasticity. Nat. Rev. Neurosci. 11, 161-175
8. Resh, M. D. (2012) Targeting protein lipidation in disease. Trends Mol. Med. 18, 206-214
9. Greaves, J., and Chamberlain, L. H. (2007) Palmitoylation-dependent protein sorting. J. Cell Biol. 176, 249-254
10. Salaun, C., Greaves, J., and Chamberlain, L. H. (2010) Intracellular dynamic of protein palmitoylation. J. Cell Biol. 191, 1229-1238
11. Duncan, J. A., and Gilman, A. G. (1998) A cytoplasmic acyl-protein thioesterase that removes palmitate fromGprotein α subunits and p21 (RAS). J. Biol. Chem. 273, 15830-15837
12. 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
13. 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
14. 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
15. Soyombo, A. A., and Hofmann, S. L. (1997) Molecular cloning and expression of palmitoyl-protein thioesterase 2 (PPT2), a homolog of lysosomal palmitoyl-protein thioesterase with distinct substrate specificity. J. Biol. Chem. 272, 27456-27463
16. Verkruyse, L. A., and Hofmann, S. L. (1996) Lysosomal targeting of palmitoyl- protein thioesterase. J. Biol. Chem. 271, 15831-15836
17. 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
18. Zeidman, R., Jackson, C. S., and Magee, A. I. (2009) Protein acyl thioesterases. Mol. Membr. Biol. 26, 32-41
19. Wang, A., Deems, R. A., and Dennis, E. A. (1997) Cloning, expression and catalytic mechanism of murine lysophospholipase 1. J. Biol. Chem. 272, 12723-12729
20. Wang, A., Loo, R., Chen, Z., and Dennis, E. A. (1997) Regiospecificity and catalytic triad of lysophospholipase 1. J. Biol. Chem. 272, 22030-22036
21. Wan, J., Roth, A. F., Bailey, A. O., and Davis, N. G. (2007) Palmitoylated proteins: purification and identification. Nat. Protoc. 2, 1573-1584
22. Wessel, D., and Flügge, U. I. (1984)Amethod for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138, 141-143
23. Adam, R. M., Yang, W., Di Vizio, D., Mukhopadhyay, N. K., and Steen, H. (2008) Rapid preparation of nuclei-depleted detergent-resistant membrane fractions suitable for proteomics analysis. BMC Cell Biol. 9, 30-39
24. Zhou, F., Xue, Y., Yao, X., and Xu, Y. (2006) CSS-Palm: palmitoylation site prediction with a clustering and scoring strategy (CSS). Bioinformatics 22, 894-896
25. Rocks, O., Peyker, A., Kahms, M., Verveer, P. J., Koerner, C., Lumbierres, M., Kuhlmann, J., Waldmann, H., Wittinghofer, A., and Bastiaens, P. I. (2005) An acylation cycle regulates localization and activity of palmitoylated Ras isoforms. Science 307, 1746-1752
26. Rocks, O., Gerauer, M., Vartak, N., Koch, S., Huang, Z. P., Pechlivanis, M., Kuhlmann, J., Brunsveld, L., Chandra, A., Ellinger, B., Waldmann, H., and Bastiaens, P. I. (2010) The palmitoylation machinery is a spatially organizing system for peripheral membrane proteins. Cell 141, 458-471
27. 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 (BK) channels. J. Biol. Chem. 287, 14718-14725
28. 2+-calmodulin. J. Biol. Chem. 274, 33148-33154
29. Ladygina, N., Martin, B. R., and Altman, A. (2011) Dynamic palmitoylation and the role of DHHC protein in T cell activation and anergy. Adv. Immunol. 109, 1-44
30. Dekker, F. J., Rocks, O., Vartak, N., Menninger, S., Hedberg, C., Balamurugan, R., Wetzel, S., Renner, S., Gerauer, M., Schölermann, B., Rusch, M., Kramer, J. W., Rauh, D., Coates, G. W., Brunsveld, L., Bastiaens, P. I., and Waldmann, H. (2010) Small molecule inhibition of APT1 affects Ras localization and signaling. Nat. Chem. Biol. 6, 449-456
31. Rusch, M., Zimmermann, T. J., Bürger, M., Dekker, F. J., Görmer, K., Triola, G., Brockmeyer, A., Janning, P., Böttcher, T., Sieber, S. A., Vetter, I. R., Hedberg, C., and Waldmann, H. (2011) Identification of acyl-protein thioesterase 1 and 2 as the cellular targets of the Ras-signaling modulators palmostatin B and M. Angew. Chem. Int. Ed. Engl. 50, 9838-9842
32. Hirano, T., Kishi, M., Sugimoto, H., Taguchi, R., Obinata, H., Ohshima, N., Tatei, K., and Izumi, T. (2009) Thioesterase activity and subcellular localization of acyl-protein thioesterase 1/lysophospholipase 1. Biochim. Biophys. Acta 1791, 797-805
33. Yang, W., Di Vizio, D., Kirchner, M., Steen, H., and Freeman, M. R. (2010) Proteome scale characterization of human palmitoylated proteins in lipid raft-enriched and non-raft membranes. Mol. Cell. Proteomics 9, 54-70