A novel motif at the C-terminus of palmitoyltransferases is essential for Swf1 and Pfa3 function in vivo

Biochemical Journal

Volumn 419, Issue 2, 2009, Pages 301-308

  González Montoro, Ayelén ^a   Quiroga, Rodrigo ^a   Maccioni, Hugo J F ^a   Valdèz Taubas, Javier ^a  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

Author keywords

Conserved motif; Palmitoylation; Palmitoyltransferase; Pfa3; Phylogeny; Swf1; Yeast

Indexed keywords

CONSERVED MOTIF; PALMITOYLATION; PALMITOYLTRANSFERASE; PFA3; PHYLOGENY; SWF1;

ACTIVATION ANALYSIS; ACYLATION; AMINES; CELL MEMBRANES; YEAST;

PROTEINS;

MEMBRANE PROTEIN; PALMITOYLTRANSFERASE; PROTEIN; PROTEIN FATTY ACYLTRANSFERASE 3; PROTEIN SWF1; PROTEIN TLG1; SNARE PROTEIN; TRANSFERASE; TYROSINE; UNCLASSIFIED DRUG; ACYLTRANSFERASE; ERF2 PROTEIN, S CEREVISIAE; PFA3 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SWF1 PROTEIN, S CEREVISIAE;

AMINO ACID SEQUENCE; ARTICLE; ASCOMYCETES; CARBOXY TERMINAL SEQUENCE; EUKARYOTE; GENE MUTATION; IN VIVO STUDY; NONHUMAN; PALMITOYLATION; PALMITOYLTRANSFERASE CONSERVED CARBOXY TERMINAL; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN MOTIF; STRUCTURE ACTIVITY RELATION; CHEMISTRY; GENETICS; METABOLISM; MUTAGENESIS; WESTERN BLOTTING;

EUKARYOTA;

ACYLTRANSFERASES; AMINO ACID MOTIFS; BLOTTING, WESTERN; MEMBRANE PROTEINS; MUTAGENESIS; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 64249172320     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20080921     Document Type: Article

References (46)

1. Valdez-Taubas, J. and Pelham, H. (2005) Swf1-dependent palmitoylation of the SNARE Tlg1 prevents its ubiquitination and degradation. EMBO J. 24, 2524-2532
2. Bijlmakers, M. J. and Marsh, M. (2003) The on-off story of protein palmitoylation. Trends Cell Biol. 13, 32-42
3. Linder, M. E. and Deschenes, R. J. (2007) Palmitoylation: policing protein stability and traffic. Nat. Rev. Mol. Cell. Biol. 8, 74-84
4. Ponimaskin, E. and Schmidt, M. F. (1998) Domain-structure of cytoplasmic border region is main determinant for palmitoylation of influenza virus hemagglutinin (H7). Virology 249, 325-335
5. Yik, J. H. N. and Weigel, P. H. (2002) The position of cysteine relative to the transmembrane domain is critical for palmitoylation of H1, the major subunit of the human asialoglycoprotein receptor. J. Biol. Chem. 277, 47305-47312
6. Putilina, T., Wong, P. and Gentleman, S. (1999) The DHHC domain: a new highly conserved cysteine-rich motif. Mol. Cell. Biochem. 195, 219-226
7. 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
8. 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. 159, 23-28
9. Mitchell, D. A., Vasudevan, A., Linder, M. E. and Deschenes, R. J. (2006) Protein palmitoylation by a family of DHHC protein S-acyltransferases. J. Lipid Res. 47, 1118-1127
10. Politis, E. G., Roth, A. F. and Davis, N. G. (2005) Transmembrane topology of the protein palmitoyl transferase Akr1. J. Biol. Chem. 280, 10156-10163
11. Fukata, M., Fukata, Y., Adesnik, H., Nicoll, R. A. and Bredt, D. S. (2004) Identification of PSD-95 palmitoylating enzymes. Neuron 44, 987-996
12. Ducker, C. E., Stettler, E. M., French, K. J., Upson, J. J. and Smith, C. D. (2004) Huntingtin interacting protein 14 is an oncogenic human protein: palmitoyl acyltransferase. Oncogene 23, 9230-9237
13. Fang, C., Deng, L., Keller, C. A., Fukata, M., Fukata, Y., Chen, G. and Luscher, B. (2006) GODZ-mediated palmitoylation of GABA(A) receptors is required for normal assembly and function of GABAergic inhibitory synapses. J. Neurosci. 26, 12758-12768
14. Roth, A. F., Wan, J., Bailey, A. O., Sun, B., Kuchar, J. A., Green, W. N., Phinney, B. S., Yates, 3rd, J. R. and Davis, N. G. (2006) Global analysis of protein palmitoylation in yeast. Cell 125, 1003-1013
15. Smotrys, J. E., Schoenfish, M. J., Stutz, M. A. and Linder, M. E. (2005) The vacuolar DHHC-CRD protein Pfa3p is a protein acyltransferase for Vac8p. J. Cell Biol. 170, 1091-1099
16. Keller, C. A., Yuan, X., Panzanelli, P., Martin, M. L., Alldred, M., Sassoe-Pognetto, M. and Luscher, B. (2004) The γ 2 subunit of GABAA receptors is a substrate for palmitoylation by GODZ. J. Neurosci. 24, 5881-5891
17. Swarthout, J. T., Lobo, S., Farh, L., Croke, M. R., Greentree, W. K., Deschenes, R. J. and Linder, M. E. (2005) DHHC9 and GCP16 constitute a human protein fatty acyltransferase with specificity for H- and N-ras. J. Biol. Chem. 280, 31141-31148
18. Linder, M. E. and Deschenes, R. J. (2003) New insights into the mechanisms of protein palmitoylation. Biochemistry 42, 4311-4320
19. Dietrich, L. E. and Ungermann, C. (2004) On the mechanism of protein palmitoylation. EMBO Rep. 5, 1053-1057
20. Raymond, F. L., Tarpey, P. S., Edkins, S., Tofts, C., O'Meara, S., Teague, J., Butler, A., Stevens, C., Barthorpe, S., Buck, G. 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
21. Ohno, Y., Kihara, A., Sano, T. and Igarashi, Y. (2006) Intracellular localization and tissue-specific distribution of human and yeast DHHC cysteine-rich domain-containing proteins. Biochim. Biophys. Acta 1761, 474-483
22. Huh, W. K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weissman, J. S. and O'Shea, E. K. (2003) Global analysis of protein localization in budding yeast. Nature 425, 686-691
23. Wang, Y. X., Catlett, N. L. and Weisman, L. S. (1998) Vac8p, a vacuolar protein with armadillo repeats, functions in both vacuole inheritance and protein targeting from the cytoplasm to vacuole. J. Cell Biol. 140, 1063-1074
24. Pan, X. and Goldfarb, D. S. (1998) YEB3/VAC8 encodes a myristylated armadillo protein of the Saccharomyces cerevisiae vacuolar membrane that functions in vacuole fusion and inheritance. J. Cell Sci. 111, 2137-2147
25. Fleckenstein, D., Rohde, M., Klionsky, D. J. and Rudiger, M. (1998) Yel013p (Vac8p), an armadillo repeat protein related to plakoglobin and importin alpha is associated with the yeast vacuole membrane. J. Cell Sci. 111, 3109-3118
26. Wang, Y. X., Kauffman, E. J., Duex, J. E. and Weisman, L. S. (2001) Fusion of docked membranes requires the armadillo repeat protein Vac8p. J. Biol. Chem. 276, 35133-35140
27. Veit, M., Laage, R., Dietrich, L., Wang, L. and Ungermann, C. (2001) Vac8p release from the SNARE complex and its palmitoylation are coupled and essential for vacuole fusion. EMBO J. 20, 3145-3155
28. Eddy, S. R. (1998) Profile hidden Markov models. Bioinformatics 14, 755-763
29. Finn, R. D., Tate, J., Mistry, J., Coggill, P. C., Sammut, S. J., Hotz, H. R., Ceric, G., Forslund, K., Eddy, S. R., Sonnhammer, E. L. and Bateman, A. (2008) The Pfam protein families database. Nucleic Acids Res. 36, D281-D288
30. Clamp, M., Cuff, J., Searle, S. M. and Barton, G. J. (2004) The Jalview Java alignment editor. Bioinformatics 20, 426-427
31. Crooks, G. E., Hon, G., Chandonia, J. M. and Brenner, S. E. (2004) WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190
32. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R. et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948
33. Abascal, F., Zardoya, R. and Posada, D. (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104-2105
34. Jones, D. T., Taylor, W. R. and Thornton, J. M. (1992) The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8, 275-282
35. Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425
36. Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599
37. Letunic, I. and Bork, P. (2007) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127-128
38. Volland, C., Urban-Grimal, D., Geraud, G. and Haguenauer-Tsapis, R. (1994) Endocytosis and degradation of the yeast uracil permease under adverse conditions. J. Biol. Chem. 269, 9833-9841
39. Hibbett, D. S., Binder, M., Bischoff, J. F., Blackwell, M., Cannon, P. F., Eriksson, O. E., Huhndorf, S., James, T., Kirk, P. M., Lucking, R. et al. (2007) A higher-level phylogenetic classification of the Fungi. Mycol. Res. 111, 509-547
40. Liu, Y. J., Hodson, M. C. and Hall, B. D. (2006) Loss of the flagellum happened only once in the fungal lineage: phylogenetic structure of kingdom Fungi inferred from RNA polymerase II subunit genes. BMC Evol. Biol. 6, 74
41. Robbertse, B., Reeves, J. B., Schoch, C. L. and Spatafora, J. W. (2006) A phylogenomic analysis of the Ascomycota. Fungal Genet. Biol. 43, 715-725
42. Warringer, J., Ericson, E., Fernandez, L., Nerman, O. and Blomberg, A. (2003) High-resolution yeast phenomics resolves different physiological features in the saline response. Proc. Natl. Acad. Sci. U.S.A. 100, 15724-15729
43. Vida, T. A. and Emr, S. D. (1995) A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol. 128, 779-792
44. Zhao, L., Lobo, S., Dong, X., Ault, A. D. and Deschenes, R. J. (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
45. Dighe, S. A. and Kozminski, K. G. (2008) Swf1p, a member of the DHHC-CRD family of palmitoyltransferases, regulates the actin cytoskeleton and polarized secretion independently of its DHHC motif. Mol. Biol. Cell 19, 4454-4468
46. Bartels, D. J., Mitchell, D. A., Dong, X. and Deschenes, R. J. (1999) Erf2, a novel gene product that affects the localization and palmitoylation of Ras2 in Saccharomyces cerevisiae. Mol. Cell. Biol. 19, 6775-6787