Conformational selection and induced changes along the catalytic cycle of Escherichia coli dihydrofolate reductase

Proteins: Structure, Function and Bioinformatics

Volumn 80, Issue 10, 2012, Pages 2369-2383

  Weikl, Thomas R ^a   Boehr, David D ^b  

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

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Conformational dynamics; Enzyme catalysis; Mutational analysis; NMR relaxation dispersion; Protein binding

Indexed keywords

DIHYDROFOLATE REDUCTASE;

ARTICLE; CHEMICAL REACTION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME KINETICS; ENZYME MECHANISM; ENZYME SUBSTRATE; ESCHERICHIA COLI; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PH; PRIORITY JOURNAL;

CATALYTIC DOMAIN; DNA MUTATIONAL ANALYSIS; ENZYME STABILITY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; TETRAHYDROFOLATE DEHYDROGENASE; TETRAHYDROFOLATES; THERMODYNAMICS;

ESCHERICHIA COLI; VERTEBRATA;

EID: 84865999329     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24123     Document Type: Article

References (71)

1. Gerstein M, Krebs W.A database of macromolecular motions.Nucleic Acids Res 1998;26:4280-4290.
2. Goh C-S, Milburn D, Gerstein M.Conformational changes associated with protein-protein interactions.Curr Opin Struct Biol 2004;14:104-109.
3. Eisenmesser EZ, Bosco DA, Akke M, Kern D.Enzyme dynamics during catalysis.Science 2002;295:1520-1523.
4. Boehr DD, McElheny D, Dyson HJ, Wright PE.The dynamic energy landscape of dihydrofolate reductase catalysis.Science 2006;313:1638-1642.
5. Watt ED, Shimada H, Kovrigin EL, Loria JP.The mechanism of rate-limiting motions in enzyme function.Proc Natl Acad Sci USA 2007;104:11981-11986.
6. Mandell DJ, Kortemme T.Backbone flexibility in computational protein design.Curr Opin Biotechnol 2009;20:420-428.
7. Doucet N.Can enzyme engineering benefit from the modulation of protein motions? Lessons learned from NMR relaxation dispersion experiments.Protein Pept Lett 2011;18:336-343.
8. Nagel ZD, Klinman JP.A 21st century revisionist's view at a turning point in enzymology.Nat Chem Biol 2009;5:543-550.
9. Min W, English BP, Luo G, Cherayil BJ, Kou SC, Xie XS.Fluctuating enzymes: lessons from single-molecule studies.Acc Chem Res 2005;38:923-931.
10. Michalet X, Weiss S, Jager M.Single-molecule fluorescence studies of protein folding and conformational dynamics.Chem Rev 2006;106:1785-1813.
11. Smiley RD, Hammes GG.Single molecule studies of enzyme mechanisms.Chem Rev 2006;106:3080-3094.
12. Palmer AG, 3rd. NMR characterization of the dynamics of biomacromolecules.Chem Rev 2004;104:3623-3640.
13. Mittermaier A, Kay LE.New tools provide new insights in NMR studies of protein dynamics.Science 2006;312:224-248.
14. Boehr DD, Dyson HJ, Wright PE.An NMR perspective on enzyme dynamics.Chem Rev 2006;106:3055-3079.
15. Henzler-Wildman K, Kern D.Dynamic personalities of proteins.Nature 2007;450:964-972.
16. Loria JP, Berlow RB, Watt ED.Characterization of enzyme motions by solution NMR relaxation dispersion.Acc Chem Res 2008;41:214-221.
17. Mittermaier AK, Kay LE.Observing biological dynamics at atomic resolution using NMR.Trends Biochem Sci 2009;34:601-611.
18. McElheny D, Schnell JR, Lansing JC, Dyson HJ, Wright PE.Defining the role of active-site loop fluctuations in dihydrofolate reductase catalysis.Proc Natl Acad Sci USA 2005;102:5032-5037.
19. Benkovic SJ, Hammes-Schiffer S.A perspective on enzyme catalysis.Science 2003;301:1196-1202.
20. Hammes-Schiffer S, Benkovic SJ.Relating protein motion to catalysis.Annu Rev Biochem 2006;75:519-541.
21. Schnell JR, Dyson HJ, Wright PE.Structure, dynamics, and catalytic function of dihydrofolate reductase.Annu Rev Biophys Biomol Struct Biophys Biomol Struct 2004;33:119-140.
22. Agarwal PK, Billeter SR, Rajagopalan PTR, Benkovic SJ, Hammes-Schiffer S.Network of coupled promoting motions in enzyme catalysis.Proc Natl Acad Sci USA 2002;99:2794-2799.
23. Thorpe IF, Brooks CL, 3rd.Conformational substates modulate hydride transfer in dihydrofolate reductase.J Am Chem Soc 2005;127:12997-13006.
24. Liu H, Warshel A.The catalytic effect of dihydrofolate reductase and its mutants is determined by reorganization energies.Biochemistry 2007;46:6011-25.
25. Chen J, Dima RI, Thirumalai D.Allosteric communication in dihydrofolate reductase: signaling network and pathways for closed to occluded transition and back.J Mol Biol 2007;374:250-266.
26. Thielges MC, Case DA, Romesberg FE.Carbon-deuterium bonds as probes of dihydrofolate reductase.J Am Chem Soc 2008;130:6597-6603.
27. Tsai CJ, Ma B, Sham YY, Kumar S, Nussinov R.Structured disorder and conformational selection.Proteins 2001;44:418-427.
28. Bosshard HR.Molecular recognition by induced fit: How fit is the concept?News Physiol Sci 2001;16:171-1733.
29. James LC, Roversi P, Tawfik DS.Antibody multispecificity mediated by conformational diversity.Science 2003;299:1362-1367.
30. 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.
31. Tobi D, Bahar I.Structural changes involved in protein binding correlate with intrinsic motions of proteins in the unbound state.Proc Natl Acad Sci USA 2005;102:18908-18913.
32. 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.
33. Qiu L, Gulotta M, Callender R.Lactate dehydrogenase undergoes a substantial structural change to bind its substrate.Biophys J 2007;93:1677-1686.
34. Lange OF, Lakomek N-A, Fares C, Schröder GF, Walter KFA, Becker S, Meiler J, Grubmüller H, Griesinger C, de Groot BL.Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution.Science 2008;320:1471-1475.
35. Braz VA, Barkley MD, Jockusch RA, Wintrode PL.Efavirenz binding site in HIV-1 reverse transcriptase monomers.Biochemistry 2010;49:10565-10573.
36. Masterson LR, Cheng C, Yu T, Tonelli M, Kornev A, Taylor SS, Veglia G.Dynamics connect substrate recognition to catalysis in protein kinase A.Nat Chem Biol 2010;6:821-828.
37. Koshland DE.Application of a theory of enzyme specificity to protein synthesis.Proc Natl Acad Sci USA 1958;44:98-104.
38. 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.
39. Elinder M, Selhorst P, Vanham G, Oberg B, Vrang L, Danielson UH.Inhibition of HIV-1 by non-nucleoside reverse transcriptase inhibitors via an induced fit mechanism - Importance of slow dissociation and relaxation rates for antiviral efficacy.Biochem Pharmacol 2010;80:1133-1140.
40. Fieulaine S, Boularot A, Artaud I, Desmadril M, Dardel F, Meinnel T, Giglione C.Trapping conformational states along ligand-binding dynamics of peptide deformylase: the impact of induced fit on enzyme catalysis.PLoS Biol 2011;9:e1001066.
41. Copeland RA.Conformational adaptation in drug-target interactions and residence time.Future Med Chem 2011;3:1491-1501.
42. Boehr DD.Promiscuity in protein-RNA interactions: Conformational ensembles facilitate molecular recognition in the spliceosome.Bioessays 2011;34:174-180.
43. Boehr DD, Nussinov R, Wright PE.The role of dynamic conformational ensembles in biomolecular recognition.Nat Chem Biol 2009;5:789-796.
44. Weikl TR, von Deuster C.Selected-fit versus induced-fit protein binding: kinetic differences and mutational analysis.Proteins 2009;75:104-110.
45. Sawaya MR, Kraut J.Loop and subdomain movements in the mechanism of Escherichia coli dihydrofolate reductase: crystallographic evidence.Biochemistry 1997;36:586-603.
46. Venkitakrishnan RP, Zaborowski E, McElheny D, Benkovic SJ, Dyson HJ, Wright PE.Conformational changes in the active site loops of dihydrofolate reductase during the catalytic cycle.Biochemistry 2004;43:16046-16055.
47. Bhabha G, Lee J, Ekiert DC, Gam J, Wilson IA, Dyson HJ, Benkovic SJ, Wright PE.A dynamic knockout reveals that conformational fluctuations influence the chemical step of enzyme catalysis.Science 2011;332:234-238.
48. Fierke CA, Johnson KA, Benkovic SJ.Construction and evaluation of the kinetic scheme associated with dihydrofolate reductase from Escherichia coli.Biochemistry 1987;26:4085-4092.
49. Cameron CE, Benkovic SJ.Evidence for a functional role of the dynamics of glycine-121 of Escherichia coli dihydrofolate reductase obtained from kinetic analysis of a site-directed mutant.Biochemistry 1997;36:15792-15800.
50. Boehr DD, Dyson HJ, Wright PE.Conformational relaxation following hydride transfer plays a limiting role in dihydrofolate reductase catalysis.Biochemistry 2008;47:9227-9233.
51. Kiefhaber T, Bachmann A, Jensen KS.Dynamics and mechanisms of coupled protein folding and binding reactions.Curr Opion Struct Biol 2012;22:21-29.
52. Wright PE, Dyson HJ.Linking folding and binding.Curr Opin Struct Biol 2009;19:31-38.
53. Hammond G.A correlation of reaction rates.J Am Chem Soc 1955;77:334-338.
54. Leffler J.Parameters for the description of transition states.Science 1953;117:340-341.
55. 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.
56. Csermely P, Palotai R, Nussinov R.Induced fit, conformational selection and independent dynamic segments: an extended view of binding events.Trends Biochem Sci 2010;35:539-546.
57. Miller GP, Benkovic SJ.Strength of an interloop hydrogen bond determines the kinetic pathway in catalysis by Escherichia coli dihydrofolate reductase.Biochemistry 1998;37:6336-6342.
58. Miller GP, Wahnon DC, Benkovic SJ.Interloop contacts modulate ligand cycling during catalysis by Escherichia coli dihydrofolate reductase.Biochemistry 2001;40:867-875.
59. Rajagopalan PTR, Lutz S, Benkovic SJ.Coupling interactions of distal residues enhance dihydrofolate reductase catalysis: mutational effects on hydride transfer rates.Biochemistry 2002;41:12618-12628.
60. Benedix A, Becker CM, de Groot BL, Caflisch A, Böckmann RA.Predicting free energy changes using structural ensembles.Nat Methods 2009;6:3-4.
61. Potapov V, Cohen M, Schreiber G.Assessing computational methods for predicting protein stability upon mutation: good on average but not in the details.Protein Eng Des Sel 2009;22:553-560.
62. Kellogg EH, Leaver-Fay A, Baker D.Role of conformational sampling in computing mutation-induced changes in protein structure and stability.Proteins 2011;79:830-838.
63. Fierke CA, Kuchta RD, Johnson KA, Benkovic SJ.Implications for enzymic catalysis from free-energy reaction coordinate profiles.Cold Spring Harb Symp Quant Biol 1987;52:631-638.
64. Davies JF, 2nd, Delcamp TJ, Prendergast NJ, Ashford VA, Freisheim JH, Kraut J.Crystal structures of recombinant human dihydrofolate reductase complexed with folate and 5-deazafolate.Biochemistry 1990;29:9467-9479.
65. Richard H, Foster JW.Escherichia coli glutamate- and arginine-dependent acid resistance systems increase internal pH and reverse transmembrane potential.J Bacteriol 2004;186:6032-6041.
66. Kroll RG, Booth IR.The relationship between intracellular pH, the pH gradient and potassium transport in Escherichia coli.Biochem J 1983;216:709-716.
67. Hill TL.Free energy transduction and biochemical cycle kinetics.New York:Springer;1989.
68. Wang L, Goodey NM, Benkovic SJ, Kohen A.Coordinated effects of distal mutations on environmentally coupled tunneling in dihydrofolate reductase.Proc Natl Acad Sci USA 2006;103:15753-15758.
69. Wang L, Tharp S, Selzer T, Benkovic SJ, Kohen A.Effects of a distal mutation on active site chemistry.Biochemistry 2006;45:1383-1392.
70. Swanwick RS, Maglia G, Tey L-h, Allemann RK.Coupling of protein motions and hydrogen transfer during catalysis by Escherichia coli dihydrofolate reductase.Biochem J 2006;394:259-265.
71. van Kampen NG.Stochastic processes in physics and chemistry.Amsterdam:North-Holland;1992.