Chemical proteomics with sulfonyl fluoride probes reveals selective labeling of functional tyrosines in glutathione transferases

Chemistry and Biology

Volumn 20, Issue 4, 2013, Pages 541-548

  Gu, Christian ^a   Shannon, D Alexander ^d   Colby, Tom ^a   Wang, Zheming ^a   Shabab, Mohammed ^e   Kumari, Selva ^a   Villamor, Joji Grace ^a   McLaughlin, Christopher J ^d   Weerapana, Eranthie ^b,d   Kaiser, Markus ^c   Cravatt, Benjamin F ^b   Van Der Hoorn, Renier A L ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

^d BOSTON COLLEGE   (United States)

^e MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORIDE; GLUTATHIONE TRANSFERASE; SERINE PROTEINASE; SULFONYL HALIDE; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL LABELING; ENZYME ACTIVE SITE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEOMICS; SEQUENCE HOMOLOGY;

ANIMALS; BINDING SITES; GLUTATHIONE TRANSFERASE; KINETICS; MICE; PROTEIN STRUCTURE, TERTIARY; PROTEOME; PROTEOMICS; SULFINIC ACIDS; TYROSINE;

ANIMALIA;

EID: 84876468280     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2013.01.016     Document Type: Article

References (34)

1. K. Arnold, L. Bordoli, J. Kopp, and T. Schwede The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling Bioinformatics 22 2006 195 201
2. I. Axarli, P. Dhavala, A.C. Papageorgiou, and N.E. Labrou Crystal structure of Glycine max glutathione transferase in complex with glutathione: investigation of the mechanism operating by the Tau class glutathione transferases Biochem. J. 422 2009 247 256
3. I. Axarli, P. Dhavala, A.C. Papageorgiou, and N.E. Labrou Crystallographic and functional characterization of the fluorodifen-inducible glutathione transferase from Glycine max reveals an active site topography suited for diphenylether herbicides and a novel L-site J. Mol. Biol. 385 2009 984 1002
4. R.L. Bateman, P. Bhanumoorthy, J.F. Witte, R.W. McClard, M. Grompe, and D.E. Timm Mechanistic inferences from the crystal structure of fumarylacetoacetate hydrolase with a bound phosphorus-based inhibitor J. Biol. Chem. 276 2001 15284 15291
5. P.G. Board, M. Coggan, G. Chelvanayagam, S. Easteal, L.S. Jermiin, G.K. Schulte, D.E. Danley, L.R. Hoth, M.C. Griffor, and A.V. Kamath Identification, characterization, and crystal structure of the Omega class glutathione transferases J. Biol. Chem. 275 2000 24798 24806
6. C.M. Bruns, I. Hubatsch, M. Ridderström, B. Mannervik, and J.A. Tainer Human glutathione transferase A4-4 crystal structures and mutagenesis reveal the basis of high catalytic efficiency with toxic lipid peroxidation products J. Mol. Biol. 288 1999 427 439
7. R.M.F. Cardoso, D.S. Daniels, C.M. Bruns, and J.A. Tainer Characterization of the electrophile binding site and substrate binding mode of the 26-kDa glutathione S-transferase from Schistosoma japonicum Proteins 51 2003 137 146
8. B.F. Cravatt, A.T. Wright, and J.W. Kozarich Activity-based protein profiling: from enzyme chemistry to proteomic chemistry Annu. Rev. Biochem. 77 2008 383 414
9. D.P. Dixon, and R. Edwards Glutathione transferases Arabidopsis Book 8 2010 e0131
10. R. Edwards, D.P. Dixon, and V. Walbot Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health Trends Plant Sci. 5 2000 193 198
11. J. Gobom, M. Schuerenberg, M. Mueller, D. Theiss, H. Lehrach, and E. Nordhoff Alpha-cyano-4-hydroxycinnamic acid affinity sample preparation. A protocol for MALDI-MS peptide analysis in proteomics Anal. Chem. 73 2001 434 438
12. J.D. Hayes, J.U. Flanagan, and I.R. Jowsey Glutathione transferases Annu. Rev. Pharmacol. Toxicol. 45 2005 51 88
13. W.P. Heal, and E.W. Tate Getting a chemical handle on protein post-translational modification Org. Biomol. Chem. 8 2010 731 738
14. D.A. Jeffery, and M. Bogyo Chemical proteomics and its application to drug discovery Curr. Opin. Biotechnol. 14 2003 87 95
15. W.W. Johnson, S. Liu, X. Ji, G.L. Gilliland, and R.N. Armstrong Tyrosine 115 participates both in chemical and physical steps of the catalytic mechanism of a glutathione S-transferase J. Biol. Chem. 268 1993 11508 11511
16. F.X. Kober, W. Koelmel, J. Kuper, J. Drechsler, C. Mais, H.M. Hermanns, and H. Schindelin The crystal structure of the protein disulfide isomerase family member ERp27 provides insights into its substrate-binding capabilities J. Biol. Chem. 288 2013 2029 2039
17. M. Lo Bello, A.J. Oakley, A. Battistoni, A.P. Mazzetti, M. Nuccetelli, G. Mazzarese, J. Rossjohn, M.W. Parker, and G. Ricci Multifunctional role of Tyr 108 in the catalytic mechanism of human glutathione transferase P1-1. Crystallographic and kinetic studies on the Y108F mutant enzyme Biochemistry 36 1997 6207 6217
18. M.A. McTigue, D.R. Williams, and J.A. Tainer Crystal structures of a schistosomal drug and vaccine target: glutathione S-transferase from Schistosoma japonica and its complex with the leading antischistosomal drug praziquantel J. Mol. Biol. 246 1995 21 27
19. R.D. Mindnich, and T.M. Penning Aldo-keto reductase (AKR) superfamily: genomics and annotation Hum. Genomics 3 2009 362 370
20. A.J. Oakley, M. Lo Bello, A. Battistoni, G. Ricci, J. Rossjohn, H.O. Villar, and M.W. Parker The structures of human glutathione transferase P1-1 in complex with glutathione and various inhibitors at high resolution J. Mol. Biol. 274 1997 84 100
21. I. Quesada-Soriano, L.J. Parker, A. Primavera, J.M. Casas-Solvas, A. Vargas-Berenguel, C. Barón, C.J. Morton, A.P. Mazzetti, M. Lo Bello, M.W. Parker, and L. García-Fuentes Influence of the H-site residue 108 on human glutathione transferase P1-1 ligand binding: structure-thermodynamic relationships and thermal stability Protein Sci. 18 2009 2454 2470
22. U. Rix, and G. Superti-Furga Target profiling of small molecules by chemical proteomics Nat. Chem. Biol. 5 2009 616 624
23. S. Serim, U. Haedke, and S.H.L. Verhelst Activity-based probes for the study of proteases: recent advances and developments ChemMedChem 7 2012 1146 1159
24. D.A. Shannon, C. Gu, C.J. McLaughlin, M. Kaiser, R.A.L. van der Hoorn, and E. Weerapana Sulfonyl fluoride analogues as activity-based probes for serine proteases ChemBioChem 13 2012 2327 2330
25. D. Sheehan, G. Meade, V.M. Foley, and C.A. Dowd Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily Biochem. J. 360 2001 1 16
26. A.E. Speers, and B.F. Cravatt A tandem orthogonal proteolysis strategy for high-content chemical proteomics J. Am. Chem. Soc. 127 2005 10018 10019
27. D. Suckau, A. Resemann, M. Schuerenberg, P. Hufnagel, J. Franzen, and A. Holle A novel MALDI LIFT-TOF/TOF mass spectrometer for proteomics Anal. Bioanal. Chem. 376 2003 952 965
28. D.M. Townsend, and K.D. Tew The role of glutathione-S-transferase in anti-cancer drug resistance Oncogene 22 2003 7369 7375
29. M.C. Vega, S.B. Walsh, T.J. Mantle, and M. Coll The three-dimensional structure of Cys-47-modified mouse liver glutathione S-transferase P1-1. Carboxymethylation dramatically decreases the affinity for glutathione and is associated with a loss of electron density in the αB-310B region J. Biol. Chem. 273 1998 2844 2850
30. E. Weerapana, A.E. Speers, and B.F. Cravatt Tandem orthogonal proteolysis-activity-based protein profiling (TOP-ABPP) - a general method for mapping sites of probe modification in proteomes Nat. Protoc. 2 2007 1414 1425
31. E. Weerapana, G.M. Simon, and B.F. Cravatt Disparate proteome reactivity profiles of carbon electrophiles Nat. Chem. Biol. 4 2008 405 407
32. E. Weerapana, C. Wang, G.M. Simon, F. Richter, S. Khare, M.B. Dillon, D.A. Bachovchin, K. Mowen, D. Baker, and B.F. Cravatt Quantitative reactivity profiling predicts functional cysteines in proteomes Nature 468 2010 790 795
33. G. Xiao, S. Liu, X. Ji, W.W. Johnson, J. Chen, J.F. Parsons, W.J. Stevens, G.L. Gilliland, and R.N. Armstrong First-sphere and second-sphere electrostatic effects in the active site of a class mu gluthathione transferase Biochemistry 35 1996 4753 4765
34. 153Eu isotope dilution ICP/MS Angew. Chem. Int. Ed. Engl. 51 2012 3358 3363