2-bromopalmitate and 2-(2-hydroxy-5-nitro-benzylidene)-benzo[b] thiophen-3-one inhibit DHHC-mediated palmitoylation in vitro

Journal of Lipid Research

Volumn 50, Issue 2, 2009, Pages 233-242

  Jennings, Benjamin C ^a   Nadolski, Marissa J ^a   Ling, Yiping ^b   Baker, Meredith Beckham ^c   Harrison, Marietta L ^c   Deschenes, Robert J ^b   Linder, Maurine E ^a  

^a WASHINGTON UNIVERSITY   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c PURDUE UNIVERSITY   (United States)

Author keywords

Asp His His Cys; DHHC; Enzyme; Fatty acylation; Inhibitor; Lipidation; S acylation

Indexed keywords

2 (2 HYDROXY 5 NITRO BENZYLIDENE) BENZO[B]THIOPHEN 3 ONE; 2 BROMOPALMITIC ACID; ASPARTYLHISTIDYLHISTIDYLCYSTEINE; BENZOTHIOPHENE DERIVATIVE; PALMITOYLTRANSFERASE; PEPTIDE; RAS PROTEIN; TRANSFERASE; UNCLASSIFIED DRUG; 2 (2 HYDROXY 5 NITROBENZYLIDENE)BENZO(B)THIOPHEN 3 ONE; 2-(2-HYDROXY-5-NITROBENZYLIDENE)BENZO(B)THIOPHEN-3-ONE; 2-BROMOPALMITATE; ACYLTRANSFERASE; ENZYME INHIBITOR; ERF2 PROTEIN, S CEREVISIAE; GLYCYLPEPTIDE N-TETRADECANOYLTRANSFERASE; MEMBRANE PROTEIN; NITROPHENOL; PALMITIC ACID DERIVATIVE; PROTEIN N MYRISTOYLTRANSFERASE; SACCHAROMYCES CEREVISIAE PROTEIN; SHR5 PROTEIN, S CEREVISIAE; THIOPHENE DERIVATIVE; TUMOR SUPPRESSOR PROTEIN; ZDHHC2 PROTEIN, HUMAN; ZDHHC9 PROTEIN, HUMAN;

ACYLATION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENCY; DRUG SELECTIVITY; ENZYME INHIBITION; ENZYME SUBSTRATE COMPLEX; INHIBITION KINETICS; INSECT CELL CULTURE; MYRISTYLATION; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MODIFICATION; AMINO ACID SEQUENCE; ANIMAL; CELL CULTURE; DRUG ANTAGONISM; GENETICS; HUMAN; LIPOYLATION; METABOLISM; MOLECULAR GENETICS; MOUSE;

ACYLTRANSFERASES; AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; ENZYME INHIBITORS; HUMANS; LIPOYLATION; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; NITROPHENOLS; PALMITATES; SACCHAROMYCES CEREVISIAE PROTEINS; THIOPHENES; TUMOR SUPPRESSOR PROTEINS;

EID: 64749106134     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M800270-JLR200     Document Type: Article

References (46)

1. Resh, M. D. 2006. Palmitoylation of ligands, receptors, and intracellular signaling molecules. Sci. STKE. 2006: re14.
2. Linder, M. E., and R. J. Deschenes. 2007. Palmitoylation: policing protein stability and traffic. Nat. Rev. Mol. Cell Biol. 8: 74-84.
3. Mitchell, D. A., A. Vasudevan, M. E. Linder, and R. J. Deschenes. 2006. Protein pamitoylation by a family of DHHC protein S-acyltransferases. J. Lipid Res. 47: 1118-1127.
4. el-Husseini Ael, D., and D. S. Bredt. 2002. Protein palmitoylation: a regulator of neuronal development and function. Nat. Rev. Neurosci. 3: 791-802.
5. Singaraja, R. R., S. Hadano, M. Metzler, S. Givan, C. L. Wellington, S. Warby, A. Yanai, C. A. Gutekunst, B. R. Leavitt, H. Yi, et al. 2002. HIP14, a novel ankyrin domain-containing protein, links huntingtin to intracellular trafficking and endocytosis. Hum. Mol. Genet. 11: 2815-2828.
6. Huang, K., A. Yanai, R. Kang, P. Arstikaitis, R. R. Singaraja, M. Metzler, A. Mullard, B. Haigh, C. Gauthier-Campbell, C. A. Gutekunst, et al. 2004. Huntingtin-interacting protein HIP14 is a palmitoyl transferase involved in palmitoylation and trafficking of multiple neuronal proteins. Neuron. 44: 977-986.
7. Yanai, A., K. Huang, R. Kang, R. R. Singaraja, P. Arstikaitis, L. Gan, P. C. Orban, A. Mullard, C. M. Cowan, L. A. Raymond, et al. 2006. Palmitoylation of huntingtin by HIP14is essential for its trafficking and function. Nat. Neurosci. 9: 824-831.
8. Stowers, R. S., and E. Y. Isacoff. 2007. Drosophila huntingtininteracting protein 14 is a presynaptic protein required for photoreceptor synaptic transmission and expression of the palmitoylated proteins synaptosome-associated protein 25 and cysteine string protein. J. Neurosci. 27: 12874-12883.
9. Ohyama, T., P. Verstreken, C. V. Ly, T. Rosenmund, A. Rajan, A. C. Tien, C. Haueter, K. L. Schulze, and H. J. Bellen. 2007. Huntingtininteracting protein 14, a palmitoyl transferase required for exocytosis and targeting of CSP to synaptic vesicles. J. Cell Biol. 179: 1481-1496.
10. Willumsen, B. M., A. D. Cox, P. A. Solski, C. J. Der, and J. E. Buss. 1996. Novel determinants of H-Ras plasma membrane localization and transformation. Oncogene. 13: 1901-1909.
11. Ducker, C. E., E. M. Stettler, K. J. French, J. J. Upson, and C. D. Smith. 2004. Huntingtin interacting protein 14 is an oncogenic human protein: palmitoyl acyltransferase. Oncogene. 23: 9230-9237.
12. Ducker, C. E., L. K. Griffel, R. A. Smith, S. N. Keller, Y. Zhuang, Z. Xia, J. D. Diller, and C. D. Smith. 2006. Discovery and characterization of inhibitors of human palmitoyl acyltransferases. Mol. Cancer Ther. 5: 1647-1659.
13. Mansilla, F., K. Birkenkamp-Demtroder, M. Kruhoffer, F. B. Sorensen, C. L. Andersen, P. Laiho, L. A. Aaltonen, H. W. Verspaget, and T. F. Orntoft. 2007. Differential expression of DHHC9 in microsatellite stable and instable human colorectal cancer subgroups. Br. J. Cancer. 96: 1896-1903.
14. Oyama, T., Y. Miyoshi, K. Koyama, H. Nakagawa, T. Yamori, T. Ito, H. Matsuda, H. Arakawa, and Y. Nakamura. 2000. Isolation of a novel gene on 8p21.3-22 whose expression is reduced significantly in human colorectal cancers with liver metastasis. Genes Chromosomes Cancer. 29: 9-15.
15. 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.
16. Fukata, M., Y. Fukata, H. Adesnik, R. A. Nicoll, and D. S. Bredt. 2004. Identification of PSD-95 palmitoylating enzymes. Neuron. 44: 987-996.
17. Chase, J. F., and P. K. Tubbs. 1972. Specific inhibition of mitochondrial fatty acid oxidation by 2-bromopalmitate and its coenzyme A and carnitine esters. Biochem. J. 129: 55-65.
18. 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.
19. Omura, S. 1976. The antibiotic cerulenin, a novel tool for biochemistry as an inhibitor of fatty acid synthesis. Bacteriol. Rev. 40: 681-697.
20. DeJesus, G., and O. A. Bizzozero. 2002. Effect of 2-fluoropalmitate, cerulenin and tunicamycin on the palmitoylation and intracellular translocation of myelin proteolipid protein. Neurochem. Res. 27: 1669-1675.
21. Patterson, S. I., and J. H. Skene. 1995. Inhibition of dynamic protein palmitoylation in intact cells with tunicamycin. Methods Enzymol. 250: 284-300.
22. Dunphy, J. T., W. K. Greentree, C. L. Manahan, and M. E. Linder. 1996. G-protein palmitoyltransferase activity is enriched in plasma membranes. J. Biol. Chem. 271: 7154-7159.
23. Duncan, J. A., and A. G. Gilman. 1996. Autoacylation of G protein alpha subunits. J. Biol. Chem. 271: 23594-23600.
24. Duronio, R. J., E. Jackson-Machelski, R. O. Heuckeroth, P. O. Olins, C. S. Devine, W. Yonemoto, L. W. Slice, S. S. Taylor, and J. I. Gordon. 1990. Protein N-myristoylation in Escherichia coli: reconstitution of a eukaryotic protein modification in bacteria. Proc. Natl. Acad. Sci. USA. 87: 1506-1510.
25. Duronio, R. J., S. I. Reed, and J. I. Gordon. 1992. Mutations of human myristoyl-CoA:protein N-myristoyltransferase cause temperature-sensitive myristic acid auxotrophy in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 89: 4129-4133.
26. Swarthout, J. T., S. Lobo, L. Farh, M. R. Croke, W. K. Greentree, R. J. Deschenes, and M. E. Linder. 2005. DHHC9 and GCP16 constitute a human protein fatty acyltransferase with specificity for H- and N-Ras. J. Biol. Chem. 280: 31141-31148.
27. Budde, C., M. J. Schoenfish, M. E. Linder, and R. J. Deschenes. 2006. Purification and characterization of recombinant protein acyltransferases. Methods. 40: 143-150.
28. Smotrys, J. E., M. J. Schoenfish, M. A. Stutz, and M. E. Linder. 2005. The vacuolar DHHC-CRD protein Pfa3p is a protein acyltransferase for Vac8p. J. Cell Biol. 170: 1091-1099.
29. Osanai, K., K. Takahashi, K. Nakamura, M. Takahashi, M. Ishigaki, T. Sakuma, H. Toga, T. Suzuki, and D. R. Voelker. 2005. Expression and characterization of Rab38, a new member of the Rab small G protein family. Biol. Chem. 386: 143-153.
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. Bijlmakers, M. J., M. Isobe-Nakamura, L. J. Ruddock, and M. Marsh. 1997. Intrinsic signals in the unique domain target p56(lck) to the plasma membrane independently of CD4. J. Cell Biol. 137: 1029-1040.
32. Turner, J. M., M. H. Brodsky, B. A. Irving, S. D. Levin, R. M. Perlmutter, and D. R. Littman. 1990. Interaction of the unique Nterminal region of tyrosine kinase p56lck with cytoplasmic domains of CD4 and CD8 is mediated by cysteine motifs. Cell. 60: 755-765.
33. Resh, M. D. 1994. Myristylation and palmitylation of Src family members: the fats of the matter. Cell. 76: 411-413.
34. Fernandez-Hernando, C., M. Fukata, P. N. Bernatchez, Y. Fukata, M. I. Lin, D. S. Bredt, and W. C. Sessa. 2006. Identification of Golgi-localized acyl transferases that palmitoylate and regulate endothelial nitric oxide synthase. J. Cell Biol. 174: 369-377.
35. Sharma, C., X. H. Yang, and M. E. Hemler. 2008. DHHC2 affects palmitoylation, stability, and functions of tetraspanins CD9 and CD151. Mol. Biol. Cell. 19: 3415-3425.
36. Raymond, F. L., P. S. Tarpey, S. Edkins, C. Tofts, S. O'Meara, J. Teague, A. Butler, C. Stevens, S. Barthorpe, G. Buck, et al. 2007. Mutations in ZDHHC9, which encodes a palmitoyltransferase of NRAS and HRAS, cause X-linked mental retardation associated with a Marfanoid habitus. Am. J. Hum. Genet. 80: 982-987.
37. el-Aleem, S. A., and H. Schulz. 1987. Evaluation of inhibitors of fatty acid oxidation in rat myocytes. Biochem. Pharmacol. 36: 4307-4312.
38. Fong, J. C., S. J. Leu, and S. P. Chai. 1997. Differential inhibition of lipolysis by 2-bromopalmitic acid and 4-bromocrotonic acid in 3T3-L1 adipocytes. Biochim. Biophys. Acta. 1344: 65-73.
39. Raaka, B. M., and J. M. Lowenstein. 1979. Inhibition of fatty acid oxidation by 2-bromooctanoate. Evidence for the enzymatic formation of 2-bromo-3-ketooctanoyl coenzyme A and the inhibition of 3-ketothiolase. J. Biol. Chem. 254: 6755-6762.
40. Mikic, I., S. Planey, J. Zhang, C. Ceballos, T. Seron, B. von Massenbach, R. Watson, S. Callaway, P. M. McDonough, J. H. Price, et al. 2006. A live cell, image-based approach to understanding the enzymology and pharmacology of 2-bromopalmitate and palmitoylation. Methods Enzymol. 414: 150-187.
41. Baron, R. A., Y. K. Peterson, J. C. Otto, J. Rudolph, and P. J. Casey. 2007. Time-dependent inhibition of isoprenylcysteine carboxyl methyltransferase by indole-based small molecules. Biochemistry. 46: 554-560.
42. Hou, H., K. Subramanian, T. J. LaGrassa, D. Markgraf, L. E. Dietrich, J. Urban, N. Decker, and C. Ungermann. 2005. The DHHC protein Pfa3 affects vacuole-associated palmitoylation of the fusion factor Vac8. Proc. Natl. Acad. Sci. USA. 102: 17366-17371.
43. Anderson, J. L., H. Frase, S. Michaelis, and C. A. Hrycyna. 2005. Purification, functional reconstitution, and characterization of the Saccharomyces cerevisiae isoprenylcysteine carboxylmethyltransferase Ste14p. J. Biol. Chem. 280: 7336-7345.
44. Roth, A. F., J. Wan, A. O. Bailey, B. Sun, J. A. Kuchar, W. N. Green, B. S. Phinney, J. R. Yates 3rd, and N. G. Davis. 2006. Global analysis of protein palmitoylation in yeast. Cell. 125: 1003-1013.
45. Yang, J., M. S. Brown, G. Liang, N. V. Grishin, and J. L. Goldstein. 2008. Identification of the acyltransferase that octanoylates ghrelin, an appetite-stimulating peptide hormone. Cell. 132: 387-396.
46. Buglino, J. A., and M. D. Resh. 2008. Hhat is a palmitoylacyltransferase with specificity for N-palmitoylation of sonic hedgehog. J. Biol. Chem. 283: 22076-22088.