SILAC-pulse proteolysis: A mass spectrometry-based method for discovery and cross-validation in proteome-wide studies of ligand binding

Journal of the American Society for Mass Spectrometry

Volumn 25, Issue 12, 2014, Pages 2073-2083

  Adhikari, Jagat ^a   Fitzgerald, Michael C ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b DUKE UNIVERSITY   (United States)

Author keywords

ATP; Chemical denaturation; Cyclosporine A; Mass spectrometry; Protein folding; Proteomics; Thermodynamics

Indexed keywords

ADENOSINETRIPHOSPHATE; AMINO ACIDS; BINDING ENERGY; CELL CULTURE; CELLS; COMPLEXATION; DRUG PRODUCTS; EXPERIMENTS; ISOTOPES; LIGANDS; MASS SPECTROMETRY; MOLECULAR BIOLOGY; PROTEIN FOLDING; PROTEOLYSIS; THERMODYNAMIC PROPERTIES; THERMODYNAMICS; YEAST;

BIOLOGICAL MIXTURES; CHEMICAL DENATURATION; CYCLOSPORINE A; FALSE POSITIVE RATES; PROOF-OF-PRINCIPLE EXPERIMENTS; PROTEIN-LIGAND COMPLEXES; PROTEOMICS; STABLE-ISOTOPE LABELING;

PROTEINS;

ADENOSINE TRIPHOSPHATE DERIVATIVE; CYCLOSPORIN A; ADENOSINE TRIPHOSPHATE; CYCLOSPORIN; FUNGAL PROTEIN; LIGAND; PROTEIN BINDING; PROTEOME;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CELL FUNCTION; CELL LYSATE; CONTROLLED STUDY; DISSOCIATION CONSTANT; FRACTIONATION; LIGAND BINDING; MASS SPECTROMETRY; MOLECULAR WEIGHT; NONHUMAN; OXIDATION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PULSE PROTEOLYSIS; STABLE ISOTOPE LABELING WITH AMINO ACID IN CELL CULTURE; YEAST CELL; ANALOGS AND DERIVATIVES; CHEMISTRY; ISOTOPE LABELING; METABOLISM; PROCEDURES; PROTEIN DENATURATION; PROTEOMICS; REPRODUCIBILITY; THERMODYNAMICS;

ADENOSINE TRIPHOSPHATE; CYCLOSPORINE; FUNGAL PROTEINS; ISOTOPE LABELING; LIGANDS; MASS SPECTROMETRY; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEOME; PROTEOMICS; REPRODUCIBILITY OF RESULTS; THERMODYNAMICS;

EID: 84919911357     PISSN: 10440305     EISSN: 18791123     Source Type: Journal    
DOI: 10.1007/s13361-014-0992-y     Document Type: Article

References (32)

1. West, G.M.; Tang, L.; Fitzgerald, M.C.: Thermodynamic analysis of protein stability and ligand binding using a chemical modification- and mass spectrometry-based strategy. Anal. Chem. 80(11), 4175-4185 (2008)
2. West, G.M.; Tucker, C.L.; Xu, T.; Park, S.K.; Han, X.; Yates III, J.R.; Fitzgerald, M.C.: Quantitative proteomics approach for identifying protein-drug interactions in complex mixtures using protein stability measurements. Proc. Natl. Acad. Sci. U. S. A. 107(20), 9078-9082 (2010)
3. Park, C.; Marqusee, S.: Pulse proteolysis: a simple method for quantitative determination of protein stability and ligand binding. Nat. Methods 2(3), 207-212 (2005)
4. Liu, P.F.; Kihara, D.; Park, C.: Energetics-based discovery of protein-ligand interactions on a proteomic scale. J. Mol. Biol. 408(1), 147-162 (2011)
5. Xu, Y.; Falk, I.N.; Hallen, M.A.; Fitzgerald, M.C.: Mass spectrometry- and lysine amidination-based protocol for thermodynamic analysis of protein folding and ligand binding interactions. Anal. Chem. 83(9), 3555-3562 (2011)
6. Tran, D.T.; Banerjee, S.; Alayash, A.I.; Crumbliss, A.L.; Fitzgerald, M.C.: Slow histidine H/D exchange protocol for thermodynamic analysis of protein folding and stability using mass spectrometry. Anal. Chem. 84(3), 1653-1660 (2012)
7. Ghaemmaghami, S.; Fitzgerald, M.C.; Oas, T.G.: A quantitative, high-throughput screen for protein stability. Proc. Natl. Acad. Sci. U. S. A. 97(15), 8296-8301 (2000)
8. Isom, D.G.; Vardy, E.; Oas, T.G.; Hellinga, H.W.: Picomole-scale characterization of protein stability and function by quantitative cysteine reactivity. Proc. Natl. Acad. Sci. U. S. A. 107(11), 4908-4913 (2010)
9. Dearmond, P.D.; Xu, Y.; Strickland, E.C.; Daniels, K.G.; Fitzgerald, M.C.: Thermodynamic analysis of protein-ligand interactions in complex biological mixtures using a shotgun proteomics approach. J. Protein Res. 10(11), 4948-4958 (2011)
10. Strickland, E.C.; Geer, M.A.; Tran, D.T.; Adhikari, J.; West, G.M.; DeArmond, P.D.; Xu, Y.; Fitzgerald, M.C.: Thermodynamic analysis of protein-ligand binding interactions in complex biological mixtures using the stability of proteins from rates of oxidation. Nat. Protoc. 8(1), 148-161 (2013)
11. Chang, Y.; Schlebach, J.P.; Verheul, R.A.; Park, C.: Simplified proteomics approach to discover protein-ligand interactions. Protein Sci. 21(9), 1269-1277 (2012)
12. Molina, D.M.; Jafari, R.; Ignatushchenko, M.; Seki, T.; Larsson, E.A.; Dan, C.; Sreekumar, L.; Cao, Y.; Nordlund, P.: Monitoring drug target engagement in cells and tissues using the cellular thermal shift assay. Science 341(6141), 84-87 (2013)
13. Tran, D.T.; Adhikari, J.; Fitzgerald, M.C.: SILAC-based strategy for proteome-wide thermodynamic analysis of protein-ligand binding interactions. Mol. Cell. Proteomics 13, 1800-1813 (2014)
14. Strickland, E.C.; Geer, M.A.; Hong, J.Y.; Fitzgerald, M.C.: False-positive rate determination of protein target discovery using a covalent modification- and mass spectrometry-based proteomics platform. J. Am. Soc. Mass Spectrom. 25(1), 132-140 (2014)
15. Lomenick, B.; Olsen, R.W.; Huang, J.: Identification of direct protein targets of small molecules. ACS Chem. Biol. 6(1), 34-46 (2011)
16. Villamor, J.G.; Kaschani, F.; Colby, T.; Oeljeklaus, J.; Zhao, D.; Kaiser, M.; Patricelli, M.P.; van der Hoorn, R.A.L.: Profiling protein kinases and other ATP binding proteins in Arabidopsis using Acyl-ATP probes. Mol. Cell. Proteomics 12(9), 2481-2496 (2013)
17. Lomenick, B.; Hao, R.; Jonai, N.; Chin, R.M.; Aghajan, M.; Warburton, S.; Wang, J.N.; Wu, R.P.; Gomez, F.; Loo, J.A.; Wohlschlegel, J.A.; Vondriska, T.M.; Pelletier, J.; Herschman, H.R.; Clardy, J.; Clarke, C.F.; Huang, J.: Target identification using drug affinity responsive target stability (DARTS). Proc. Natl. Acad. Sci. U. S. A. 106(51), 21984-21989 (2009)
18. Walther, T.C.; Olsen, J.V.; Mann, M.: Yeast expression proteomics by high-resolution mass spectrometry. Methods Enzymol. 470, 259-280 (2010)
19. Pace, C.N.: Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131, 266-280 (1986)
20. Shevchenko, A.; Tomas, H.; Havlis, J.; Olsen, J.V.; Mann, M.: In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1(6), 2856-2860 (2006)
21. Wang, M.Z.; Shetty, J.T.; Howard, B.A.; Campa, M.J.; Patz Jr.; E.F.; Fitzgerald, M.C.: Thermodynamic analysis of cyclosporin a binding to cyclophilin a in a lung tumor tissue lysate. Anal. Chem. 76(15), 4343-4348 (2004)
22. Myers, J.K.; Pace, C.N.; Scholtz, J.M.: Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci. 4(10), 2138-2148 (1995)
23. Prodromou, C.; Roe, S.M.; OBrien, R.; Ladbury, J.E.; Piper, P.W.; Pearl, L.H.: Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90(1), 65-75 (1997)
24. Harding, M.W.; Handschumacher, R.E.: Cyclophilin, a primary molecular target for cyclosporine. Structural and functional implications. Transplantation 46(2 Suppl), 29S-35S (1988)
25. Handschumacher, R.E.; Harding, M.W.; Rice, J.; Drugge, R.J.; Speicher, D.W.: Cyclophilin: a specific cytosolic binding protein for cyclosporin A. Science 226(4674), 544-547 (1984)
26. Liu, J.; Albers, M.W.; Chen, C.M.; Schreiber, S.L.; Walsh, C.T.: Cloning, expression, and purification of human cyclophilin in Escherichia coli and assessment of the catalytic role of cysteines by site-directed mutagenesis. Proc. Natl. Acad. Sci. U. S. A. 87(6), 2304-2308 (1990)
27. Jorgensen, P.L.; Hakansson, K.O.; Karlish, S.J.D.: Structure and mechanism of Na,K-ATPase: functional sites and their interactions. Annu. Rev. Physiol. 65, 817-849 (2003)
28. Arnesano, F.; Banci, L.; Bertini, I.; Ciofi-Baffoni, S.; Molteni, E.; Huffman, D.L.; O Halloran, T.V.: Metallochaperones and metal-transporting ATPases: a comparative analysis of sequences and structures. Genome Res. 12(2), 255-271 (2002)
29. Pause, A.; Methot, N.; Sonenberg, N.: The HRIGRXXR region of the dead box RNA helicase eukaryotic translation initiation factor-4a is required for RNA-binding and ATP hydrolysis. Mol. Cell. Biol. 13(11), 6789-6798 (1993)
30. Weng, Y.M.; Czaplinski, K.; Peltz, S.W.: ATP is a cofactor of the Upf1 protein that modulates its translation termination and RNA binding activities. RNA-Publ. RNA Soc. 4(2), 205-214 (1998)
31. DeArmond, P.D.; West, G.M.; Huang, H.T.; Fitzgerald, M.C.: Stable isotope labeling strategy for protein-ligand binding analysis in multi-component protein mixtures. J. Am. Soc. Mass Spectrom. 22(3), 418-430 (2011)
32. Apweiler, R.; Bateman, A.; Martin, M.J.; O Donovan, C.; Magrane, M.; Alam-Faruque, Y.; Alpi, E.; Antunes, R.; Arganiska, J.; Casanova, E.B.; Bely, B.; Bingley, M.; Bonilla, C.; Britto, R.; Bursteinas, B.; Chan, W.M.; Chavali, G.; Cibrian-Uhalte, E.; Da Silva, A.; De Giorgi, M.; Fazzini, F.; Gane, P.; Castro, L.G.; Garmiri, P.; Hatton-Ellis, E.; Hieta, R.; Huntley, R.; Legge, D.; Liu, W.D.; Luo, J.; MacDougall, A.; Mutowo, P.; Nightingale, A.; Orchard, S.; Pichler, K.; Poggioli, D.; Pundir, S.; Pureza, L.; Qi, G.Y.; Rosanoff, S.; Sawford, T.; Shypitsyna, A.; Turner, E.; Volynkin, V.; Wardell, T.; Watkins, X.; Zellner, H.; Corbett, M.; Donnelly, M.; Van Rensburg, P.; Goujon, M.; McWilliam, H.; Lopez, R.; Xenarios, I.; Bougueleret, L.; Bridge, A.; Poux, S.; Redaschi, N.; Aimo, L.; Auchincloss, A.; Axelsen, K.; Bansal, P.; Baratin, D.; Binz, P.A.; Blatter, M.C.; Boeckmann, B.; Bolleman, J.; Boutet, E.; Breuza, L.; Casal-Casas, C.; de Castro, E.; Cerutti, L.; Coudert, E.; Cuche, B.; Doche, M.; Dornevil, D.; Duvaud, S.; Estreicher, A.; Famiglietti, L.; Feuermann, M.; Gasteiger, E.; Gehant, S.; Gerritsen, V.; Gos, A.; Gruaz-Gumowski, N.; Hinz, U.; Hulo, C.; James, J.; Jungo, F.; Keller, G.; Lara, V.; Lemercier, P.; Lew, J.; Lieberherr, D.; Lombardot, T.; Martin, X.; Masson, P.; Morgat, A.; Neto, T.; Paesano, S.; Pedruzzi, I.; Pilbout, S.; Pozzato, M.; Pruess, M.; Rivoire, C.; Roechert, B.; Schneider, M.; Sigrist, C.; Sonesson, K.; Staehli, S.; Stutz, A.; Sundaram, S.; Tognolli, M.; Verbregue, L.; Veuthey, A.L.; Wu, C.H.; Arighi, C.N.; Arminski, L.; Chen, C.M.; Chen, Y.X.; Garavelli, J.S.; Huang, H.Z.; Laiho, K.; McGarvey, P.; Natale, D.A.; Suzek, B.E.; Vinayaka, C.R.; Wang, Q.H.; Wang, Y.Q.; Yeh, L.S.; Yerramalla, M.S.; Zhang, J.: Consortium U, activities at the Universal Protein Resource (UniProt). Nucleic Acids Res. 42(D1), D191-D198 (2014)