Systems Analysis of Protein Fatty Acylation in Herpes Simplex Virus-Infected Cells Using Chemical Proteomics

Chemistry and Biology

Volumn 22, Issue 8, 2015, Pages 1008-1017

  Serwa, Remigiusz A ^a   Abaitua, Fernando ^a   Krause, Eberhard ^b   Tate, Edward W ^a   O'Hare, Peter ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOTRANSFERASE; PROTEIN; PROTEOME; VIRUS ENZYME; VIRUS GLYCOPROTEIN; VIRUS PROTEIN; MYRISTIC ACID; VIRAL PROTEIN;

ARTICLE; CONTROLLED STUDY; FLUORESCENCE IMAGING; HERPES SIMPLEX; MASS SPECTROMETRY; MYRISTYLATION; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEOMICS; ACYLATION; CELL CULTURE; CHEMISTRY; CYTOLOGY; HIGH THROUGHPUT SCREENING; HUMAN; LIPOYLATION; METABOLISM; PIGMENT EPITHELIUM; PROCEDURES; SIMPLEXVIRUS; SYSTEM ANALYSIS;

SIMPLEXVIRUS;

ACYLATION; CELLS, CULTURED; HERPES SIMPLEX; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; LIPOYLATION; MYRISTIC ACID; PIGMENT EPITHELIUM OF EYE; PROTEOME; PROTEOMICS; SIMPLEXVIRUS; SYSTEMS ANALYSIS; VIRAL PROTEINS;

EID: 84939621793     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2015.06.024     Document Type: Article

References (46)

1. C. Aicart-Ramos, R.A. Valero, and I. Rodriguez-Crespo Protein palmitoylation and subcellular trafficking Biochim. Biophys. Acta 1808 2011 2981 2994
2. R. Apweiler, A. Bairoch, C.H. Wu, W.C. Barker, B. Boeckmann, S. Ferro, E. Gasteiger, H.Z. Huang, R. Lopez, M. Magrane, and et al. UniProt: the Universal Protein knowledgebase Nucleic Acids Res. 32 2004 D115 D119
3. A.F.H. Berry, W.P. Heal, A.K. Tarafder, T. Tolmachova, R.A. Baron, M.C. Seabra, and E.W. Tate Rapid multilabel detection of geranylgeranylated proteins by using bioorthogonal ligation chemistry Chembiochem 11 2010 771 773
4. M.J. Bijlmakers Protein acylation and localization in T cell signaling (Review) Mol. Membr. Biol. 26 2009 93 103
5. A.L. Brass, I.C. Huang, Y. Benita, S.P. John, M.N. Krishnan, E.M. Feeley, B.J. Ryan, J.L. Weyer, L. van der Weyden, E. Fikrig, and et al. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus Cell 139 2009 1243 1254
6. M. Broncel, R.A. Serwa, P. Ciepla, E. Krause, M.J. Dallman, A.I. Magee, and E.W. Tate Multifunctional reagents for quantitative proteome-wide analysis of protein modification in human cells and dynamic profiling of protein lipidation during vertebrate development Angew. Chem. Int. Ed. Engl. 54 2015 5948 5951
7. V. Bruss, J. Hagelstein, E. Gerhardt, and P.R. Galle Myristylation of the large surface protein is required for hepatitis B virus in vitro infectivity Virology 218 1996 396 399
8. Y.F. Chiu, B. Sugden, P.J. Chang, L.W. Chen, Y.J. Lin, Y.C. Lan, C.H. Lai, J.Y. Liou, S.T. Liu, and C.H. Hung Characterization and intracellular trafficking of Epstein-Barr virus BBLF1, a protein involved in virion maturation J. Virol. 86 2012 9647 9655
9. P. Ciepla, A.D. Konitsiotis, R.A. Serwa, N. Masumoto, W.P. Leong, M.J. Dallman, A.I. Magee, and E.W. Tate New chemical probes targeting cholesterylation of Sonic Hedgehog in human cells and zebrafish Chem. Sci. 5 2014 4249 4259
10. J. Cox, and M. Mann MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification Nat. Biotechnol. 26 2008 1367 1372
11. J. Cox, N. Neuhauser, A. Michalski, R.A. Scheltema, J.V. Olsen, and M. Mann Andromeda: a peptide search engine integrated into the MaxQuant environment J. Proteome Res. 10 2011 1794 1805
12. D.N. Everly Jr., P. Feng, I.S. Mian, and G.S. Read mRNA degradation by the virion host shutoff (Vhs) protein of herpes simplex virus: genetic and biochemical evidence that Vhs is a nuclease J. Virol. 76 2002 8560 8571
13. M.T. Forrester, D.T. Hess, J.W. Thompson, R. Hultman, M.A. Moseley, J.S. Stamler, and P.J. Casey Site-specific analysis of protein S-acylation by resin-assisted capture J. Lipid Res. 52 2011 393 398
14. J.A. Frearson, S. Brand, S.P. McElroy, L.A.T. Cleghorn, O. Smid, L. Stojanovski, H.P. Price, M.L.S. Guther, L.S. Torrie, D.A. Robinson, and et al. N-myristoyltransferase inhibitors as new leads to treat sleeping sickness Nature 464 2010 728 732
15. T. Geiger, J.R. Wisniewski, J. Cox, S. Zanivan, M. Kruger, Y. Ishihama, and M. Mann Use of stable isotope labeling by amino acids in cell culture as a spike-in standard in quantitative proteomics Nat. Protoc. 6 2011 147 157
16. V. Goncalves, J.A. Brannigan, E. Thinon, T.O. Olaleye, R. Serwa, S. Lanzarone, A.J. Wilkinson, E.W. Tate, and R.J. Leatherbarrow A fluorescence-based assay for N-myristoyltransferase activity Anal. Biochem. 421 2012 342 344
17. P. Gripon, J. Le Seyec, S. Rumin, and C. Guguen-Guillouzo Myristylation of the hepatitis B virus large surface protein is essential for viral infectivity Virology 213 1995 292 299
18. W.P. Heal, M.H. Wright, E. Thinon, and E.W. Tate Multifunctional protein labeling via enzymatic N-terminal tagging and elaboration by click chemistry Nat. Protoc. 7 2012 105 117
19. D.W. Huang, B.T. Sherman, and R.A. Lempicki Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 4 2009 44 57
20. T. Iwanaga, R. Tsutsumi, J. Noritake, Y. Fukata, and M. Fukata Dynamic protein palmitoylation in cellular signaling Prog. Lipid Res. 48 2009 117 127
21. P.S. Kabouridis, A.I. Magee, and S.C. Ley S-acylation of LCK protein tyrosine kinase is essential for its signalling function in T lymphocytes EMBO J. 16 1997 4983 4998
22. A.D. Konitsiotis, B. Jovanovic, P. Ciepla, M. Spitaler, T. Lanyon-Hogg, E.W. Tate, and A.I. Magee Topological analysis of hedgehog acyltransferase, a multipalmitoylated transmembrane protein J. Biol. Chem. 290 2015 3293 3307
23. J.S. Loomis, J.B. Bowzard, R.J. Courtney, and J.W. Wills Intracellular trafficking of the UL11 tegument protein of herpes simplex virus type 1 J. Virol. 75 2001 12209 12219
24. C.A. MacLean, B. Clark, and D.J. McGeoch Gene UL11 of herpes simplex virus type 1 encodes a virion protein which is myristylated J. Gen. Virol. 70 1989 3147 3157
25. D.R. Macrae, V. Bruss, and D. Ganem Myristylation of a duck hepatitis B virus envelope protein is essential for infectivity but not for virus assembly Virology 181 1991 359 363
26. B.R. Martin, and B.F. Cravatt Large-scale profiling of protein palmitoylation in mammalian cells Nat. Methods 6 2009 135 138
27. B.R. Martin, C. Wang, A. Adibekian, S.E. Tully, and B.F. Cravatt Global profiling of dynamic protein palmitoylation Nat. Methods 9 2012 84 89
28. S.B. Milne, K.A. Tallman, R. Serwa, C.A. Rouzer, M.D. Armstrong, L.J. Marnett, C.M. Lukehart, N.A. Porter, and H.A. Brown Capture and release of alkyne-derivatized glycerophospholipids using cobalt chemistry Nat. Chem. Biol. 6 2010 205 207
29. N. Nozawa, T. Daikoku, T. Koshizuka, Y. Yamauchi, T. Yoshikawa, and Y. Nishiyama Subcellular localization of herpes simplex virus type 1 UL51 protein and role of palmitoylation in Golgi apparatus targeting J. Virol. 77 2003 3204 3216
30. Y. Ohno, A. Kashio, R. Ogata, A. Ishitomi, Y. Yamazaki, and A. Kihara Analysis of substrate specificity of human DHHC protein acyltransferases using a yeast expression system Mol. Biol. Cell 23 2012 4543 4551
31. S.E. Ong, B. Blagoev, I. Kratchmarova, D.B. Kristensen, H. Steen, A. Pandey, and M. Mann Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics Mol. Cell. Proteomics 1 2002 376 386
32. G.S. Read, and N. Frenkel Herpes simplex virus mutants defective in the virion-associated shutoff of host polypeptide synthesis and exhibiting abnormal synthesis of alpha (immediate early) viral polypeptides J. Virol. 46 1983 498 512
33. M.D. Resh A myristoyl switch regulates membrane binding of HIV-1 Gag Proc. Natl. Acad. Sci. USA 101 2004 417 418
34. M.D. Resh Targeting protein lipidation in disease Trends Mol. Med. 18 2012 206 214
35. V.V. Rostovtsev, L.G. Green, V.V. Fokin, and K.B. Sharpless A stepwise huisgen cycloaddition process: copper(I)-catalyzed regioselective "ligation" of azides and terminal alkynes Angew. Chem. Int. Ed. Engl. 41 2002 2596 2599
36. V. Sanchez, E. Sztul, and W.J. Britt Human cytomegalovirus pp28 (UL99) localizes to a cytoplasmic compartment which overlaps the endoplasmic reticulum-golgi-intermediate compartment J. Virol. 74 2000 3842 3851
37. E.M. Storck, R.A. Serwa, and E.W. Tate Chemical proteomics: a powerful tool for exploring protein lipidation Biochem. Soc. Trans. 41 2013 56 61
38. T. Suzutani, M. Nagamine, T. Shibaki, M. Ogasawara, I. Yoshida, T. Daikoku, Y. Nishiyama, and M. Azuma The role of the UL41 gene of herpes simplex virus type 1 in evasion of non-specific host defence mechanisms during primary infection J. Gen. Virol. 81 2000 1763 1771
39. E.W. Tate, K.A. Kalesh, T. Lanyon-Hogg, E.M. Storck, and E. Thinon Global profiling of protein lipidation using chemical proteomic technologies Curr. Opin. Chem. Biol. 24 2015 48 57
40. E. Thinon, R.A. Serwa, M. Broncel, J.A. Brannigan, U. Brassat, M.H. Wright, W.P. Heal, A.J. Wilkinson, D.J. Mann, and E.W. Tate Global profiling of co- and post-translationally N-myristoylated proteomes in human cells Nat. Commun. 5 2014 4919
41. C.W. Tornoe, C. Christensen, and M. Meldal Peptidotriazoles on solid phase: [1,2,3]-triazoles by regiospecific copper(I)-catalyzed 1,3-dipolar cycloadditions of terminal alkynes to azides J. Org. Chem. 67 2002 3057 3064
42. J.P. Wilson, A.S. Raghavan, Y.Y. Yang, G. Charron, and H.C. Hang Proteomic analysis of fatty-acylated proteins in mammalian cells with chemical reporters reveals S-acylation of histone H3 variants Mol. Cell. Proteomics 10 2011 10.1074/mcp.M110.001198 M110.001198
43. M.H. Wright, D. Pappe, E.M. Storck, R.A. Serwa, D.F. Smith, and E.W. Tate Global analysis of protein N-myristoylation and exploration of N-myristoyltransferase as a drug target in the neglected human pathogen Leishmania donovani Chem. Biol. 22 2015 342 354
44. K. Yasuda, A. Kosugi, F. Hayashi, S. Saitoh, M. Nagafuku, Y. Mori, M. Ogata, and T. Hamaoka Serine 6 of Lck tyrosine kinase: a critical site for Lck myristoylation, membrane localization, and function in T lymphocytes J. Immunol. 165 2000 3226 3231
45. J.S. Yount, B. Moltedo, Y.Y. Yang, G. Charron, T.M. Moran, C.B. Lopez, and H.C. Hang Palmitoylome profiling reveals S-palmitoylation-dependent antiviral activity of IFITM3 Nat. Chem. Biol. 6 2010 610 614
46. L.K. Yurchak, and B.M. Sefton Palmitoylation of either Cys-3 or Cys-5 is required for the biological activity of the Lck tyrosine protein kinase Mol. Cell. Biol. 15 1995 6914 6922