How to Distinguish Conformational Selection and Induced Fit Based on Chemical Relaxation Rates

PLoS Computational Biology

Volumn 12, Issue 9, 2016, Pages

  Paul, Fabian ^a,b   Weikl, Thomas R ^a  

^a MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CONFORMATIONS; LIGANDS;

'INDUCED FIT' BINDING; BINDING EVENTS; CONFORMATIONAL CHANGE; CONFORMATIONAL SELECTION; CONFORMATIONAL TRANSITIONS; INDUCED FIT; PROTEIN-BINDING; PSEUDO-FIRST-ORDER; RELAXATION RATES; TRANSITION RATES;

PROTEINS;

LIGAND; PROTEIN; PROTEIN BINDING;

ARTICLE; BIOLOGICAL MODEL; CHEMICAL ANALYSIS; CHEMICAL PARAMETERS; CONCENTRATION (PARAMETERS); LIGAND BINDING; MATHEMATICAL ANALYSIS; MATHEMATICAL COMPUTING; PROTEIN BINDING; PROTEIN CONFORMATION; BIOLOGY; CHEMISTRY; MOLECULAR MODEL;

COMPUTATIONAL BIOLOGY; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEINS;

EID: 84989352609     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1005067     Document Type: Article

References (45)

1. Gerstein M, Krebs W, A database of macromolecular motions. Nucleic Acids Res. 1998;26:4280–4290. doi: 10.1093/nar/26.18.42809722650
2. Eisenmesser EZ, Millet O, Labeikovsky W, Korzhnev DM, Wolf-Watz M, Bosco DA, et al. Intrinsic dynamics of an enzyme underlies catalysis. Nature. 2005;438:117–121. doi: 10.1038/nature0410516267559
3. Beach H, Cole R, Gill M, Loria J, Conservation of μs-ms enzyme motions in the apo- and substrate-mimicked state. J Am Chem Soc. 2005;127:9167–9176. doi: 10.1021/ja051494915969595
4. Boehr DD, McElheny D, Dyson HJ, Wright PE, The dynamic energy landscape of dihydrofolate reductase catalysis. Science. 2006;313:1638–1642. doi: 10.1126/science.113025816973882
5. Henzler-Wildman KA, Thai V, Lei M, Ott M, Wolf-Watz M, Fenn T, et al. Intrinsic motions along an enzymatic reaction trajectory. Nature. 2007;450:838–844. doi: 10.1038/nature0641018026086
6. Tang C, Schwieters CD, Clore GM, Open-to-closed transition in apo maltose-binding protein observed by paramagnetic NMR. Nature. 2007;449:1078–1082. doi: 10.1038/nature0623217960247
7. Lange OF, Lakomek NA, Fares C, Schröder GF, Walter KFA, Becker S, et al. Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Science. 2008;320:1471–1475. doi: 10.1126/science.115709218556554
8. Kim E, Lee S, Jeon A, Choi JM, Lee HS, Hohng S, et al. A single-molecule dissection of ligand binding to a protein with intrinsic dynamics. Nat Chem Biol. 2013;9:313–318. doi: 10.1038/nchembio.121323502425
9. Munro JB, Gorman J, Ma X, Zhou Z, Arthos J, Burton DR, et al. Conformational dynamics of single HIV-1 envelope trimers on the surface of native virions. Science. 2014;346:759–763. doi: 10.1126/science.125442625298114
10. Ghoneim M, Spies M, Direct correlation of DNA binding and single protein domain motion via dual illumination fluorescence microscopy. Nano Lett. 2014;14:5920–5931. doi: 10.1021/nl502890g25204359
11. Ma B, Kumar S, Tsai CJ, Nussinov R, Folding funnels and binding mechanisms. Protein Eng. 1999;12:713–720. doi: 10.1093/protein/12.9.71310506280
12. Koshland DE, Application of a theory of enzyme specificity to protein synthesis. Proc Natl Acad Sci USA. 1958;44:98–104. doi: 10.1073/pnas.44.2.9816590179
13. Weikl TR, Paul F, Conformational selection in protein binding and function. Protein Sci. 2014;23:1508–1518. doi: 10.1002/pro.253925155241
14. Bosshard HR, Molecular recognition by induced fit: How fit is the concept?News Physiol Sci. 2001;16:171–1733. 11479367
15. Sullivan SM, Holyoak T, Enzymes with lid-gated active sites must operate by an induced fit mechanism instead of conformational selection. Proc Natl Acad Sci USA. 2008;105:13829–13834. doi: 10.1073/pnas.080536410518772387
16. Weikl TR, von Deuster C, Selected-fit versus induced-fit protein binding: kinetic differences and mutational analysis. Proteins. 2009;75:104–110. doi: 10.1002/prot.2222318798570
17. Boehr DD, Nussinov R, Wright PE, The role of dynamic conformational ensembles in biomolecular recognition. Nat Chem Biol. 2009;5:789–796. doi: 10.1038/nchembio.23219841628
18. Hammes GG, Chang YC, Oas TG, Conformational selection or induced fit: a flux description of reaction mechanism. Proc Natl Acad Sci USA. 2009;106:13737–13741. doi: 10.1073/pnas.090719510619666553
19. Wlodarski T, Zagrovic B, Conformational selection and induced fit mechanism underlie specificity in noncovalent interactions with ubiquitin. Proc Natl Acad Sci USA. 2009;106:19346–19351. doi: 10.1073/pnas.090696610619887638
20. Changeux JP, Edelstein S, Conformational selection or induced fit? 50 years of debate resolved. F1000 Biol Rep. 2011;3:19. doi: 10.3410/B3-1921941598
21. Weikl TR, Boehr DD, Conformational selection and induced changes along the catalytic cycle of Escherichia coli dihydrofolate reductase. Proteins. 2012;80:2369–2383. doi: 10.1002/prot.2412322641560
22. Vogt AD, Di Cera E, Conformational selection or induced fit? A critical appraisal of the kinetic mechanism. Biochemistry. 2012;51:5894–5902. doi: 10.1021/bi300691322775458
23. Kiefhaber T, Bachmann A, Jensen KS, Dynamics and mechanisms of coupled protein folding and binding reactions. Curr Opion Struct Biol. 2012;22:21–29. doi: 10.1016/j.sbi.2011.09.010
24. Vogt AD, Pozzi N, Chen Z, Di Cera E, Essential role of conformational selection in ligand binding. Biophys Chem. 2014;186:13–21. doi: 10.1016/j.bpc.2013.09.00324113284
25. Pozzi N, Vogt AD, Gohara DW, Di Cera E, Conformational selection in trypsin-like proteases. Curr Opin Struct Biol. 2012;22:421–431. doi: 10.1016/j.sbi.2012.05.00622664096
26. Daniels KG, Tonthat NK, McClure DR, Chang YC, Liu X, Schumacher MA, et al. Ligand concentration regulates the pathways of coupled protein folding and binding. J Am Chem Soc. 2014;136:822–825. doi: 10.1021/ja408672624364358
27. Daniels KG, Suo Y, Oas TG, Conformational kinetics reveals affinities of protein conformational states. Proc Natl Acad Sci USA. 2015;112:9352–9357. doi: 10.1073/pnas.150208411226162682
28. Chakrabarti KS, Agafonov RV, Pontiggia F, Otten R, Higgins MK, Schertler GFX, et al. Conformational selection in a protein-protein interaction revealed by dynamic pathway analysis. Cell Reports. 2016;14:32–42. doi: 10.1016/j.celrep.2015.12.01026725117
29. James LC, Roversi P, Tawfik DS, Antibody multispecificity mediated by conformational diversity. Science. 2003;299:1362–1367. doi: 10.1126/science.107973112610298
30. Heredia VV, Thomson J, Nettleton D, Sun S, Glucose-induced conformational changes in glucokinase mediate allosteric regulation: transient kinetic analysis. Biochemistry. 2006;45:7553–7562. doi: 10.1021/bi060253q16768451
31. Kim YB, Kalinowski SS, Marcinkeviciene J, A pre-steady state analysis of ligand binding to human glucokinase: Evidence for a preexisting equilibrium. Biochemistry. 2007;46:1423–1431. doi: 10.1021/bi061730817260972
32. Tummino PJ, Copeland RA, Residence time of receptor-ligand complexes and its effect on biological function. Biochemistry. 2008;47:5481–5492. doi: 10.1021/bi800202318412369
33. Antoine M, Boutin JA, Ferry G, Binding kinetics of glucose and allosteric activators to human glucokinase reveal multiple conformational states. Biochemistry. 2009;48:5466–5482. doi: 10.1021/bi900374c19459610
34. Vogt AD, Di Cera E, Conformational selection is a dominant mechanism of ligand binding. Biochemistry. 2013;52:5723–5729. doi: 10.1021/bi400929b23947609
35. Gianni S, Dogan J, Jemth P, Distinguishing induced fit from conformational selection. Biophys Chem. 2014;189:33–39. doi: 10.1016/j.bpc.2014.03.00324747333
36. Vogt AD, Chakraborty P, Di Cera E, Kinetic dissection of the pre-existing conformational equilibrium in the trypsin fold. J Biol Chem. 2015;290:22435–22445. doi: 10.1074/jbc.M115.67553826216877
37. Jarosz AF, Wiley J, What are the odds? A practical guide to computing and reporting Bayes factors. J Problem Solving. 2014;7:2. doi: 10.7771/1932-6246.1167
38. Peuker S, Cukkemane A, Held M, Noé F, Kaupp UB, Seifert R, Kinetics of ligand-receptor interaction reveals an induced-fit mode of binding in a cyclic nucleotide-activated protein. Biophys J. 2013;104:63–74. doi: 10.1016/j.bpj.2012.11.381623332059
39. Greives N, Zhou HX, Both protein dynamics and ligand concentration can shift the binding mechanism between conformational selection and induced fit. Proc Natl Acad Sci USA. 2014;111:10197–10202. doi: 10.1073/pnas.140754511124982141
40. Suddala KC, Wang J, Hou Q, Walter NG, Mg2+ shifts ligand-mediated folding of a riboswitch from induced-fit to conformational selection. J Am Chem Soc. 2015;137:14075–14083. doi: 10.1021/jacs.5b0974026471732
41. Mathematica, Version 10.3. Wolfram Research, Inc., Champaign, Illinois; 2015.
42. Storn R, Price K, Differential evolution—a simple and efficient heuristic for global optimization over continuous spaces. J Global Optim. 1997;11:341–359. doi: 10.1023/A:1008202821328
43. Cavanaugh JE, Unifying the derivations of the Akaike and corrected Akaike information criteria. Stat Probabil Lett. 1997;31:201–208. doi: 10.1016/S0167-7152(96)00128-9
44. Jaynes ET, Probability theory: the logic of science. Cambridge University Press; 2003.
45. Strachan RW, van Dijk HK, Improper priors with well-defined Bayes factors. Liverpool, L69 7ZA, United Kingdom: Department of Economics and Accounting, University of Liverpool; 2005. EI 2004–18.