The Erf4 subunit of the yeast Ras palmitoyl acyltransferase is required for stability of the Acyl-Erf2 intermediate and palmitoyl transfer to a Ras2 substrate

Journal of Biological Chemistry

Volumn 287, Issue 41, 2012, Pages 34337-34348

  Mitchell, David A ^a   Hamel, Laura D ^a   Ishizuka, Kayoko ^a   Mitchell, Gayatri ^a   Schaefer, Logan M ^a   Deschenes, Robert J ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; DYNAMIC NATURE; GTPASES; MAMMALIAN CELLS; PALMITOYLATION; POST-TRANSLATIONAL MODIFICATIONS; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN MEMBRANE; PROTEIN SUBSTRATE; RECEPTOR TRAFFICKING; SUB-CELLULAR; THIOESTERS;

ACYLATION; AMINO ACIDS; PROTEOLYSIS; SUBSTRATES; YEAST;

PROTEINS;

ACYLTRANSFERASE; ERF2 PROTEIN; ERF4 PROTEIN; PALMITOYL PROTEIN THIOESTERASE; RAS PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME STABILITY; ENZYME SUBSTRATE; ENZYME SUBUNIT; MAMMAL CELL; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PURIFICATION; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; YEAST CELL;

ACYLTRANSFERASES; CATALYTIC DOMAIN; LIPOYLATION; MEMBRANE PROTEINS; PALMITIC ACID; PROTEIN STABILITY; PROTEOLYSIS; RAS PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN;

EID: 84867267220     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.379297     Document Type: Article

References (43)

1. 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 (Pubitemid 43830703)
2. Linder, M. E., and Deschenes, R. J. (2007) Palmitoylation: policing protein stability and traffic. Nat. Rev. Mol. Cell Biol. 8, 74-84 (Pubitemid 46012016)
3. Iwanaga, T., Tsutsumi, R., Noritake, J., Fukata, Y., and Fukata, M. (2009) Dynamic protein palmitoylation in cellular signaling. Prog. Lipid Res. 48, 117-127
4. Linder, M. E., and Deschenes, R. J. (2003) New insights into the mechanisms of protein palmitoylation. Biochemistry 42, 4311-4320
5. Tsutsumi, R., Fukata, Y., and Fukata, M. (2008) Discovery of protein-palmitoylating enzymes. Pflugers Arch. 456, 1199-1206
6. Prescott, G. R., Gorleku, O. A., Greaves, J., and Chamberlain, L. H. (2009) Palmitoylation of the synaptic vesicle fusion machinery. J. Neurochem. 110, 1135-1149
7. Oyama, T., Miyoshi, Y., Koyama, K., Nakagawa, H., Yamori, T., Ito T., Matsuda, H., Arakawa, H., and Nakamura, Y. (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 (Pubitemid 30620493)
8. Choi, Y. W., Bae, S. M., Kim, Y. W., Lee, H. N., Kim, Y. W., Park, T. C., Ro, D. Y., Shin, J. C., Shin, S. J., Seo, J. S., and Ahn, W. S. (2007) Gene expression profiles in squamous cell cervical carcinoma using array-based comparative genomic hybridization analysis. Int. J. Gynecol Cancer. 17, 687-696 (Pubitemid 46743999)
9. Chen, W. Y., Shi, Y. Y., Zheng, Y. L., Zhao, X. Z., Zhang, G. J., Chen, S. Q., Yang, P. D., and He, L. (2004) Case-control study and transmission disequilibrium test provide consistent evidence for association between schizophrenia and genetic variation in the 22q11 gene ZDHHC8. Hum. Mol. Genet. 13, 2991-2995
10. Mukai, J., Liu, H., Burt, R. A., Swor, D. E., Lai, W. S., Karayiorgou, M., and Gogos, J. A. (2004) Evidence that the gene encoding ZDHHC8 contributes to the risk of schizophrenia. Nat. Genet. 36, 725-731 (Pubitemid 38886634)
11. Raymond, F. L., Tarpey, P. S., Edkins, S., Tofts, C., O'Meara, S., Teague, J., and Butler, A., Stevens, C., Barthorpe, S., Buck, G., Cole, J., Dicks, E., Gray, K., Halliday, K., Hills, K., Hinton, J., Jones, D., Menzies, A., Perry, J., Raine, K., Shepherd, R., Small, A., Varian, J., Widaa, S., Mallya, U., Moon, J., Luo, Y., Shaw, M., Boyle, J., Kerr, B., Turner, G., Quarrell, O., Cole, T., Easton, D. F., Wooster, R., Bobrow, M., Schwartz, C. E., Gecz, J., Stratton, M. R., and Futreal, P. A. (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 (Pubitemid 46668467)
12. Mansouri, M. R., Marklund, L., Gustavsson, P., Davey, E., Carlsson, B., Larsson, C., and White, I., Gustavson, K. H., and Dahl, N. (2005) Loss of ZDHHC15 expression in a woman with a balanced translocation t(X;15)(q13.3;cen) and severe mental retardation. Eur. J. Hum. Genet. 13, 970-977 (Pubitemid 41131746)
13. Mitchell, D. A., Mitchell, G., Ling, Y., Budde, C., and Deschenes, R. J. (2010) Mutational analysis of Saccharomyces cerevisiae Erf2 reveals a two-step reaction mechanism for protein palmitoylation by DHHC enzymes. J. Biol. Chem. 285, 38104-38114
14. Dietrich, L. E., and Ungermann, C. (2004) On the mechanism of protein palmitoylation. EMBO Rep. 5, 1053-1057 (Pubitemid 39600203)
15. 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 (Pubitemid 41291850)
16. Jung, V., Chen, L., Hofmann, S. L., Wigler, M., and Powers, S. (1995) Mutations in the SHR5 gene of Saccharomyces cerevisiae suppress Ras function and block membrane attachment and palmitoylation of Ras proteins. Mol. Cell. Biol. 15, 1333-1342
17. Ohta, E., Misumi, Y., Sohda, M., Fujiwara, T., Yano, A., and Ikehara, Y. (2003) Identification and characterization of GCP16, a novel acylated Golgi protein that interacts with GCP170. J. Biol. Chem. 278, 51957-51967 (Pubitemid 38020443)
18. 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 (Pubitemid 36014366)
19. Ito, H., Fukuda, Y., Murata, K., and Kimura, A. (1983) Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168 (Pubitemid 13119852)
20. Sherman, F. (1991) Guide to yeast genetics and molecular biology. Getting started with yeast. Methods Enzymol. 194, 3-21
21. Peng, J., Schwartz, D., Elias, J. E., Thoreen, C. C., Cheng, D., Marsischky, G., Roelofs, J., Finley, D., and Gygi, S. P. (2003) A proteomics approach to understanding protein ubiquitination. Nat. Biotechnol. 21, 921-926 (Pubitemid 36936199)
22. Budde, C., Schoenfish, M. J., Linder, M. E., and Deschenes, R. J. (2006) Purification and characterization of recombinant protein acyltransferases. Methods 40, 143-150 (Pubitemid 44442971)
23. 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 (Pubitemid 35215719)
24. Dong, X., Mitchell, D. A., Lobo, S., Zhao, L., Bartels, D. J., and Deschenes, R. J. (2003) Palmitoylation and plasma membrane localization of Ras2p by a nonclassical trafficking pathway in Saccharomyces cerevisiae. Mol. Cell. Biol. 23, 6574-6584 (Pubitemid 37075768)
25. Ma, J., and Ptashne, M. (1987) Deletion analysis of GAL4 defines two transcriptional activating segments. Cell 48, 847-853
26. Robzyk, K., and Kassir, Y. (1992) A simple and highly efficient procedure for rescuing autonomous plasmids from yeast. Nucleic Acids Res. 20, 3790
27. 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 (Pubitemid 29441861)
28. Boeke, J. D., Trueheart, J., Natsoulis, G., and Fink, G. R. (1987) 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol. 154, 164-175
29. Berthiaume, L., Peseckis, S. M., and Resh, M. D. (1995) Synthesis and use of iodo-fatty acid analogs. Methods Enzymol. 250, 454-466
30. 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 (Pubitemid 43776463)
31. Ozkaynak, E., Finley, D., Solomon, M. J., and Varshavsky, A. (1987) The yeast ubiquitin genes. A family of natural gene fusions. EMBO J. 6, 1429-1439
32. Hampton, R. Y. (2002) ER-associated degradation in protein quality control and cellular regulation. Curr. Opin. Cell Biol. 14, 476-482
33. Ravid, T., Kreft, S. G., and Hochstrasser, M. (2006) Membrane and soluble substrates of the Doa10 ubiquitin ligase are degraded by distinct pathways. EMBO J. 25, 533-543 (Pubitemid 43237660)
34. Ismail, N., and Ng, D. T. (2006) Have you HRD? Understanding ERAD is DOAble! Cell 126, 237-239 (Pubitemid 44092969)
35. 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 (Pubitemid 40395869)
36. Botero, D., Gereben, B., Goncalves, C., De Jesus, L. A., and Harney, J. W., and Bianco, A. C. (2002) Ubc6p and ubc7p are required for normal and substrate-induced endoplasmic reticulum-associated degradation of the human selenoprotein type 2 iodothyronine monodeiodinase. Mol. Endocrinol. 16, 1999-2007 (Pubitemid 35013450)
37. Benitez, E. M., Stolz, A., and Wolf, D. H. (2011) Yos9, a control protein for misfolded glycosylated and non-glycosylated proteins in ERAD. FEBS Lett. 585, 3015-3019
38. Bays, N. W., Gardner, R. G., Seelig, L. P., and Joazeiro, C. A., Hampton, R. Y. (2001) Hrd1p/Der3p is a membrane-anchored ubiquitin ligase required for ER-associated degradation. Nat. Cell Biol. 3, 24-29 (Pubitemid 32114828)
39. Isasa, M., Katz, E. J., Kim, W., Yugo, V., and González, S., Kirkpatrick, D. S., and Thomson, T. M., Finley, D., Gygi, S. P., and Crosas, B. (2010) Monoubiquitination of RPN10 regulates substrate recruitment to the proteasome. Mol. Cell 38, 733-745
40. Pickart, C. M. (2001) Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70, 503-533
41. 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 (Pubitemid 35191514)
42. Fukata, Y., Iwanaga, T., and Fukata, M. (2006) Systematic screening for palmitoyl transferase activity of the DHHC protein family in mammalian cells. Methods 40, 177-182 (Pubitemid 44442975)
43. Roth, A. F., Wan, J., Bailey, A. O., Sun, B., and Kuchar, J. A., Green, W. N., Phinney, B. S., Yates, J. R., 3rd, and Davis, N. G. (2006) Global analysis of protein palmitoylation in yeast. Cell 125, 1003-1013 (Pubitemid 43795188)