Thermodynamic analysis of protein- Ligand interactions in complex biological mixtures using a shotgun proteomics approach

Journal of Proteome Research

Volumn 10, Issue 11, 2011, Pages 4948-4958

  Dearmond, Patrick D ^a   Xu, Ying ^a   Strickland, Erin C ^a   Daniels, Kyle G ^a   Fitzgerald, Michael C ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

iTRAQ; methionine oxidation; NAD+; protein ligand binding; resveratrol; SPROX

Indexed keywords

ALDEHYDE DEHYDROGENASE; HYDROGEN PEROXIDE; LIGAND; METHIONINE; NICOTINAMIDE ADENINE DINUCLEOTIDE; RESVERATROL;

ANIMAL CELL; ARTICLE; CELL LYSATE; COMPLEX FORMATION; CONTROLLED STUDY; LIGAND BINDING; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEOMICS; QUANTITATIVE ANALYSIS; THERMODYNAMICS; YEAST CELL;

ALGORITHMS; AMINO ACID SEQUENCE; ANTIOXIDANTS; GLUTAMATE DEHYDROGENASE; HYDROGEN PEROXIDE; METHIONINE; MOLECULAR SEQUENCE DATA; NAD; OXIDANTS; OXIDATION-REDUCTION; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEOME; SACCHAROMYCES CEREVISIAE PROTEINS; STILBENES; TANDEM MASS SPECTROMETRY; THERMODYNAMICS;

EID: 80655131110     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr200403c     Document Type: Article

References (39)

1. Fields, S.; Song, O. K. A novel genetic system to detect protein protein interactions Nature 1989, 340 (6230) 245-246 (Pubitemid 19171591)
2. Rigaut, G.; Shevchenko, A.; Rutz, B.; Wilm, M.; Mann, M.; Seraphin, B. A generic protein purification method for protein complex characterization and proteome exploration Nat. Biotechnol. 1999, 17 (10) 1030-1032 (Pubitemid 29474865)
3. Bartel, P. L.; Roecklein, J. A.; SenGupta, D.; Fields, S. A protein linkage map of Escherichia coli bacteriophage T7 Nat. Genet. 1996, 12 (1) 72-77 (Pubitemid 26011322)
4. Uetz, P.; Giot, L.; Cagney, G.; Mansfield, T. A.; Judson, R. S.; Knight, J. R.; Lockshon, D.; Narayan, V.; Srinivasan, M.; Pochart, P.; Qureshi-Emili, A.; Li, Y.; Godwin, B.; Conover, D.; Kalbfleisch, T.; Vijayadamodar, G.; Yang, M. J.; Johnston, M.; Fields, S.; Rothberg, J. M. A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae Nature 2000, 403 (6770) 623-627 (Pubitemid 30103994)
5. Ho, Y.; Gruhler, A.; Heilbut, A.; Bader, G. D.; Moore, L.; Adams, S. L.; Millar, A.; Taylor, P.; Bennett, K.; Boutilier, K.; Yang, L. Y.; Wolting, C.; Donaldson, I.; Schandorff, S.; Shewnarane, J.; Vo, M.; Taggart, J.; Goudreault, M.; Muskat, B.; Alfarano, C.; Dewar, D.; Lin, Z.; Michalickova, K.; Willems, A. R.; Sassi, H.; Nielsen, P. A.; Rasmussen, K. J.; Andersen, J. R.; Johansen, L. E.; Hansen, L. H.; Jespersen, H.; Podtelejnikov, A.; Nielsen, E.; Crawford, J.; Poulsen, V.; Sorensen, B. D.; Matthiesen, J.; Hendrickson, R. C.; Gleeson, F.; Pawson, T.; Moran, M. F.; Durocher, D.; Mann, M.; Hogue, C. W. V.; Figeys, D.; Tyers, M. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry Nature 2002, 415 (6868) 180-183 (Pubitemid 34059520)
6. Gavin, A. C.; Bosche, M.; Krause, R.; Grandi, P.; Marzioch, M.; Bauer, A.; Schultz, J.; Rick, J. M.; Michon, A. M.; Cruciat, C. M.; Remor, M.; Hofert, C.; Schelder, M.; Brajenovic, M.; Ruffner, H.; Merino, A.; Klein, K.; Hudak, M.; Dickson, D.; Rudi, T.; Gnau, V.; Bauch, A.; Bastuck, S.; Huhse, B.; Leutwein, C.; Heurtier, M. A.; Copley, R. R.; Edelmann, A.; Querfurth, E.; Rybin, V.; Drewes, G.; Raida, M.; Bouwmeester, T.; Bork, P.; Seraphin, B.; Kuster, B.; Neubauer, G.; Superti-Furga, G. Functional organization of the yeast proteome by systematic analysis of protein complexes Nature 2002, 415 (6868) 141-147 (Pubitemid 34059510)
7. Ito, T.; Chiba, T.; Ozawa, R.; Yoshida, M.; Hattori, M.; Sakaki, Y. A comprehensive two-hybrid analysis to explore the yeast protein interactome Proc. Natl. Acad. Sci. U.S.A. 2001, 98 (8) 4569-4574 (Pubitemid 32295017)
8. Li, S. M.; Armstrong, C. M.; Bertin, N.; Ge, H.; Milstein, S.; Boxem, M.; Vidalain, P. O.; Han, J. D. J.; Chesneau, A.; Hao, T.; Goldberg, D. S.; Li, N.; Martinez, M.; Rual, J. F.; Lamesch, P.; Xu, L.; Tewari, M.; Wong, S. L.; Zhang, L. V.; Berriz, G. F.; Jacotot, L.; Vaglio, P.; Reboul, J.; Hirozane-Kishikawa, T.; Li, Q. R.; Gabel, H. W.; Elewa, A.; Baumgartner, B.; Rose, D. J.; Yu, H. Y.; Bosak, S.; Sequerra, R.; Fraser, A.; Mango, S. E.; Saxton, W. M.; Strome, S.; van den Heuvel, S.; Piano, F.; Vandenhaute, J.; Sardet, C.; Gerstein, M.; Doucette-Stamm, L.; Gunsalus, K. C.; Harper, J. W.; Cusick, M. E.; Roth, F. P.; Hill, D. E.; Vidal, M. A map of the interactome network of the metazoan C. elegans Science 2004, 303 (5657) 540-543 (Pubitemid 38120855)
9. Licitra, E. J.; Liu, J. O. A three-hybrid system for detecting small ligand-protein receptor interactions Proc. Natl. Acad. Sci. U.S.A. 1996, 93 (23) 12817-12821 (Pubitemid 26382726)
10. Ong, S. E.; Schenone, M.; Margolin, A. A.; Li, X. Y.; Do, K.; Doud, M. K.; Mani, D. R.; Kuai, L.; Wang, X.; Wood, J. L.; Tolliday, N. J.; Koehler, A. N.; Marcaurelle, L. A.; Golub, T. R.; Gould, R. J.; Schreiber, S. L.; Carr, S. A. Identifying the proteins to which small molecule probes and drugs bind in cells Proc. Natl. Acad. Sci. U.S.A. 2009, 106 (12) 4617-4622
11. Bach, S.; Knockaert, M.; Reinhardt, J.; Lozach, O.; Schmitt, S.; Baratte, B.; Koken, M.; Coburn, S. P.; Tang, L.; Jiang, T.; Liang, D. C.; Galons, H.; Dierick, J. F.; Pinna, L. A.; Meggio, F.; Totzke, F.; Schachtele, C.; Lerman, A. S.; Carnero, A.; Wan, Y. Q.; Gray, N.; Meijer, L. Roscovitine targets, protein kinases and pyridoxal kinase J. Biol. Chem. 2005, 280 (35) 31208-31219 (Pubitemid 41291858)
12. 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. 2009, 106 (51) 21984-21989
13. Liu, P. F.; Kihara, D.; Park, C. Energetics-based discovery of protein-ligand interactions on a proteomic scale J. Mol. Biol. 2011, 408 (1) 147-162
14. West, G. M.; Tucker, C. L.; Xu, T.; Park, S. K.; Han, X. M.; Yates, 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. 2010, 107 (20) 9078-9082
15. 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. 2011, 22 (3) 418-430
16. 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. 2008, 80 (11) 4175-4185 (Pubitemid 351812772)
17. Reid, G. E.; Roberts, K. D.; Simpson, R. J.; O'Hair, R. A. J. Selective identification and quantitative analysis of methionine containing peptides by charge derivatization and tandem mass spectrometry J. Am. Soc. Mass Spectrom. 2005, 16 (7) 1131-1150 (Pubitemid 40828794)
18. Gevaert, K.; Van Damme, J.; Goethals, M.; Thomas, G. R.; Hoorelbeke, B.; Demol, H.; Martens, L.; Puype, M.; Staes, A.; Vandekerckhove, J. Chromatographic isolation of methionine-containing peptides for gel-free proteome analysis: identification of more than 800 Escherichia coli proteins Mol. Cell. Proteomics 2002, 1 (11) 896-903
19. Grunert, T.; Pock, K.; Buchacher, A.; Allmaier, G. Selective solid-phase isolation of methionine-containing peptides and subsequent matrix-assisted laser desorption/ionisation mass spectrometric detection of methionine- and of methionine sulfoxide-containing peptides Rapid Commun. Mass Spectrom. 2003, 17 (16) 1815-1824 (Pubitemid 36980583)
20. Weinberger, S. R.; Viner, R. I.; Ho, P. Tagless extraction-retentate chromatography: a new global protein digestion strategy for monitoring differential protein expression Electrophoresis 2002, 23 (18) 3182-3192 (Pubitemid 35154169)
21. Ma, L.; Fitzgerald, M. C. A new H/D exchange- and mass spectrometry-based method for thermodynamic analysis of protein-DNA interactions Chem. Biol. 2003, 10 (12) 1205-1213 (Pubitemid 38042724)
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. 1995, 4 (10) 2138-2148
23. Schellman, J. A. Macromolecular Binding Biopolymers 1975, 14, 999-1018
24. Shen, M.; Guo, L.; Wallace, A.; Fitzner, J.; Eisenman, J.; Jacobson, E.; Johnson, R. S. Isolation and isotope labeling of cysteine- and methionine-containing tryptic peptides: application to the study of cell surface proteolysis Mol. Cell. Proteomics 2003, 2 (5) 315-324
25. Shechter, Y.; Rubinstein, M.; Patchornik, A. Selective covalent binding of methionyl-containing peptides and proteins to water insoluble polymeric reagent and their regeneration Biochemistry 1977, 16 (7) 1424-1430 (Pubitemid 8083114)
26. Apweiler, R.; Martin, M. J.; O'Donovan, C.; Magrane, M.; Alam-Faruque, Y.; Antunes, R.; Barrell, D.; Bely, B.; Bingley, M.; Binns, D.; Bower, L.; Browne, P.; Chan, W. M.; Dimmer, E.; Eberhardt, R.; Fazzini, F.; Fedotov, A.; Foulger, R.; Garavelli, J.; Castro, L. G.; Huntley, R.; Jacobsen, J.; Kleen, M.; Laiho, K.; Legge, D.; Lin, Q. A.; Liu, W. D.; Luo, J.; Orchard, S.; Patient, S.; Pichler, K.; Poggioli, D.; Pontikos, N.; Pruess, M.; Rosanoff, S.; Sawford, T.; Sehra, H.; Turner, E.; Corbett, M.; Donnelly, M.; van Rensburg, P.; Xenarios, I.; Bougueleret, L.; Auchincloss, A.; Argoud-Puy, G.; Axelsen, K.; Bairoch, A.; Baratin, D.; Blatter, M. C.; Boeckmann, B.; Bolleman, J.; Bollondi, L.; Boutet, E.; Quintaje, S. B.; Breuza, L.; Bridge, A.; deCastro, E.; Coudert, E.; Cusin, I.; Doche, M.; Dornevil, D.; Duvaud, S.; Estreicher, A.; Famiglietti, L.; Feuermann, M.; Gehant, S.; Ferro, S.; Gasteiger, E.; Gateau, A.; Gerritsen, V.; Gos, A.; Gruaz-Gumowski, N.; Hinz, U.; Hulo, C.; Hulo, N.; James, J.; Jimenez, S.; Jungo, F.; Kappler, T.; Keller, G.; Lara, V.; Lemereier, P.; Lieberherr, D.; Martin, X.; Masson, P.; Moinat, M.; Morgat, A.; Paesano, S.; Pedruzzi, I.; Pilbout, S.; Poux, S.; Pozzato, M.; Redaschi, N.; Rivoire, C.; Roechert, B.; Schneider, M.; Sigrist, C.; Sonesson, K.; Staehli, S.; Stanley, E.; Stutz, A.; Sundaram, S.; Tognolli, M.; Verbregue, L.; Veuthey, A. L.; Wu, C. H.; Arighi, C. N.; Arminski, L.; Barker, W. C.; Chen, C. M.; Chen, Y. X.; Dubey, P.; Huang, H. Z.; Mazumder, R.; McGarvey, P.; Natale, D. A.; Natarajan, T. G.; Nchoutmboube, J.; Roberts, N. V.; Suzek, B. E.; Ugochukwu, U.; Vinayaka, C. R.; Wang, Q. H.; Wang, Y. Q.; Yeh, L. S.; Zhang, J. A.; Consortium, U. Ongoing and future developments at the Universal Protein Resource Nucleic Acids Res. 2011, 39, D214-D219
27. Ehrlich, R. S.; Colman, R. F. Selectivity in the binding of NAD(P)+ analogues to NAD- and NADP-dependent pig heart isocitrate dehydrogenases. A nuclear magnetic resonance study Biochemistry 1992, 31 (49) 12524-12531 (Pubitemid 23163133)
28. Ehrlich, R. S.; Colman, R. F. Histidine in the nucleotide-binding site of NADP-linked isocitrate dehydrogenase from pig heart Eur. J. Biochem. 1978, 89 (2) 575-587 (Pubitemid 8405821)
29. Hurley, J. H.; Dean, A. M.; Koshland, D. E., Jr.; Stroud, R. M. Catalytic mechanism of NADP(+)-dependent isocitrate dehydrogenase: implications from the structures of magnesium-isocitrate and NADP+ complexes Biochemistry 1991, 30 (35) 8671-8678
30. Suhadolnik, R. J.; Lennon, M. B.; Uematsu, T.; Monahan, J. E.; Baur, R. Role of adenine ring and adenine ribose of nicotinamide adenine dinucleotide in binding and catalysis with alcohol, lactate, and glyceraldehyde-3-phosphate dehydrogenases J. Biol. Chem. 1977, 252 (12) 4125-4133 (Pubitemid 8114434)
31. Plapp, B. V. Conformational changes and catalysis by alcohol dehydrogenase Arch. Biochem. Biophys. 2010, 493 (1) 3-12
32. Dalziel, K.; Egan, R. R. The binding of oxidized coenzymes by glutamate dehydrogenase and the effects of glutarate and purine nucleotides Biochem. J. 1972, 126 (4) 975-984
33. Eklund, H.; Samama, J.-P.; Jones, T. A. Crystallographic investigations of nicotinamide adenine dinucleotide binding to horse liver alcohol dehydrogenase Biochemistry 1984, 23 (25) 5982-5996 (Pubitemid 15153472)
34. Ovadi, J.; Osman, I. R.; Batke, J. Local conformational changes induced by successive nicotinamide adenine dinucleotide binding to dissociable tetrameric D-glyceraldehyde-3-phosphate dehydrogenase. Quantitative analysis of a two-step dissociation process Biochemistry 1982, 21 (25) 6375-6382
35. Ouimet, P. M.; Kapoor, M. Analysis of complex formation between Hsp80 and Hsp70, cytosolic molecular chaperones of Neurospora crassa, by enzyme-linked immunosorbent assays (ELISA) Biochem. Cell Biol. 1998, 76 (1) 97-106 (Pubitemid 29135002)
36. Jang, M.; Cai, L.; Udeani, G. O.; Slowing, K. V.; Thomas, C. F.; Beecher, C. W.; Fong, H. H.; Farnsworth, N. R.; Kinghorn, A. D.; Mehta, R. G.; Moon, R. C.; Pezzuto, J. M. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes Science 1997, 275 (5297) 218-220 (Pubitemid 127696281)
37. Howitz, K. T.; Bitterman, K. J.; Cohen, H. Y.; Lamming, D. W.; Lavu, S.; Wood, J. G.; Zipkin, R. E.; Chung, P.; Kisielewski, A.; Zhang, L. L.; Scherer, B.; Sinclair, D. A. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan Nature 2003, 425 (6954) 191-196 (Pubitemid 37150899)
38. Kitson, T. M.; Kitson, K. E.; Moore, S. A. Interaction of sheep liver cytosolic aldehyde dehydrogenase with quercetin, resveratrol and diethylstilbestrol Chem. Biol. Interact. 2001, 130-132 (1-3) 57-69 (Pubitemid 32295803)
39. Cao, Z. X.; Fang, J.; Xia, C.; Shi, X. L.; Jiang, B.-H. Trans-3,4,5′-trihydroxystibene inhibits hypoxia-inducible factor 1 alpha and vascular endothelial growth factor expression in human ovarian cancer cells Clin. Cancer Res. 2004, 10 (15) 5253-5263 (Pubitemid 39099800)