Role of dynamics in enzyme catalysis: Substantial versus semantic controversies

Accounts of Chemical Research

Volumn 48, Issue 2, 2015, Pages 466-473

  Kohen, Amnon ^a  

^a E11 SSH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIHYDROFOLATE REDUCTASE; ENZYME; FORMATE DEHYDROGENASE;

BIOCATALYSIS; CHEMISTRY; HUMAN; KINETICS; METABOLISM; SEMANTICS;

BIOCATALYSIS; ENZYMES; FORMATE DEHYDROGENASES; HUMANS; KINETICS; SEMANTICS; TETRAHYDROFOLATE DEHYDROGENASE;

EID: 84923078953     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar500322s     Document Type: Article

References (47)

1. Wolfenden, R. Degrees of difficulty of water-consuming reactions in the absence of enzymes Chem. Rev. 2006, 106, 3379-3396
2. Atkins, P.; De-Paula, J. Physical Chemistry, 7 th ed.; Oxford University Press: Oxford, U.K., 2002.
3. Klinman, J. P.; Kohen, A. Hydrogen tunneling links protein dynamics to enzyme catalysis Annu. Rev. Biochem. 2013, 82, 471-496
4. Marcus, R. A.; Sutin, N. Electron transfer in chemistry and biology Biochem. Biophys. Acta 1985, 811, 265-322
5. Roston, D.; Cheatum, C. M.; Kohen, A. Hydrogen donor-acceptor fluctuations from kinetic isotope effects: A phenomenological model Biochemistry 2012, 51, 6860-6870
6. Kuznetsov, A. M.; Ulstrup, J. Proton and hydrogen atom tunneling in hydrolytic and redox enzyme catalysis Can. J. Chem. 1999, 77, 1085-1096
7. Knapp, M. J.; Rickert, K.; Klinman, J. P. Temperature-dependent isotope effects in soybean lipoxygenase-1: Correlating hydrogen tunneling with protein dynamics J. Am. Chem. Soc. 2002, 124, 3865-3874
8. Hammes-Schiffer, S. Kinetic isotope effects for proton-coupled electron transfer reactions. In Isotope Effects in Chemistry and Biology; Kohen, A.; Limbach, H. H., Eds.; CRC Press: Boca Raton, FL, 2006; pp 499-520.
9. Pudney, C. R.; Johannissen, L. O.; Sutcliffe, M. J.; Hay, S.; Scrutton, N. S. Direct analysis of donor acceptor distance and relationship to isotope effects and the force constant for barrier compression in enzymatic H-tunneling reactions J. Am. Chem. Soc. 2010, 132, 11329-11335
10. Nagel, Z. D.; Klinman, J. P. Update 1 of: Tunneling and dynamics in enzymatic hydride transfer Chem. Rev. 2010, 110, PR41-PR67
11. Hay, S.; Scrutton, N. S. Good vibrations in enzyme-catalysed reactions Nat. Chem. 2012, 4, 161-168
12. Cheatum, C. M.; Kohen, A. Relationship between femtosecond-picosecond dynamics to enzyme catalyzed H-transfer. In Dynamics in Enzyme Catalysis; Hammes-Schiffer, S.; Klinman, J. P., Eds.; Topics in Current Chemistry, Vol. 337; Springer DE Verlag: Berlin, Heidelberg, 2013; pp 1-39.
13. Stojkovic, V.; Perissinotti, L. L.; Willmer, D.; Benkovic, S. J.; Kohen, A. Effects of the donor-acceptor distance and dynamics on hydride tunneling in the dihydrofolate reductase catalyzed reaction J. Am. Chem. Soc. 2012, 134, 1738-1745
14. Wang, L.; Goodey, N. M.; Benkovic, S. J.; Kohen, A. Coordinated effects of distal mutations on environmentally coupled tunneling in dihydrofolate reductase Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 15753-15758
15. Singh, P. N.; Sen, A.; Francis, K.; Kohen, A. Extension and limits of the network of coupled motions correlated to hydride transfer in dihydrofolate reductase J. Am. Chem. Soc. 2014, 136, 2575-2582
16. Roston, D.; Kohen, A.; Doron, D.; Major, D. T. Simulations of remote mutants of dihydrofolate reductase reveal the nature of a network of residues coupled to hydride transfer J. Comput. Chem. 2014, 35, 1411-1417
17. Wang, Z.; Signh, P.; Czekster, C.; Kohen, A.; Schramm, V. L. Protein mass-modulated effects in the catalytic mechanism of dihydrofolate reductase: beyond promoting vibrations J. Am. Chem. Soc. 2014, 136, 8333-8341
18. Francis, K.; Stojković, V.; Kohen, A. Preservation of protein dynamics in dihydrofolate reductase evolution J. Biol. Chem. 2013, 288, 35961-35968
19. Agarwal, P. K.; Billeter, S. R.; Hammes-Schiffer, S. Nuclear quantum effects and enzyme dynamics in dihydrofolate reductase catalysis J. Phys. Chem. B 2002, 106, 3283-3293
20. Ferrer, S.; Silla, E.; Tuñón, I.; Martí, S.; Moliner, V. Catalytic mechanism of dihydrofolate reductase enzyme. A combined quantum-mechanical/molecular-mechanical characterization of the N5 protonation step J. Phys. Chem. B 2003, 107, 14036-14041
21. Fan, Y.; Cembran, A.; Ma, S.; Gao, J. Connecting protein conformational dynamics with catalytic function as illustrated in dihydrofolate reductase Biochemistry 2013, 52, 2036-2049
22. Wang, Z.; Ferrer, S.; Moliner, V.; Kohen, A. QM/MM calculations suggest a novel intermediate following the proton abstraction catalyzed by thymidylate synthase Biochemistry 2013, 52, 2348-2358
23. Kanaan, N.; Ferrer, S.; Martí, S.; Garcia-Viloca, M.; Kohen, A.; Moliner, V. Temperature dependence of the kinetic isotope effects in thymidylate synthase. A theoretical study J. Am. Chem. Soc. 2011, 133, 6692-6702
24. Islam, Z.; Strutzenberg, S. T.; Gurevic, I.; Kohen, A. Concerted versus step-wise mechanism in thymidylate synthase J. Am. Chem. Soc. 2014, 136, 9850-9853
25. Agrawal, N.; Hong, B.; Mihai, C.; Kohen, A. Vibrationally enhanced hydrogen tunneling in the E. coli thymidylate synthase catalyzed reaction Biochemistry 2004, 43, 1998-2006
26. Wang, Z.; Kohen, A. Thymidylate synthase catalyzed H-transfers: Two chapters in one tale J. Am. Chem. Soc. 2010, 132, 9820-9825
27. Newby, Z.; Lee, T. T.; Morse, R. J.; Liu, Y.; Liu, L.; Venkatraman, P.; Santi, D. V.; Finer-Moore, J. S.; Stroud, R. M. The role of protein dynamics in thymidylate synthase catalysis: Variants of conserved 2′-deoxyuridine 5′-monophosphate (dUMP)-binding Tyr-261 Biochemistry 2006, 45, 7415-7428
28. Wang, Z.; Abeysinghe, T.; Finer-Moore, J. S.; Stroud, R. M.; Kohen, A. A remote mutation affects the hydride transfer by disrupting concerted protein motions in thymidylate synthase J. Am. Chem. Soc. 2012, 134, 17722-17730
29. 2+ binds to the surface of thymidylate synthase and affects hydride transfer at the interior active site J. Am. Chem. Soc. 2013, 135, 7583-7592
30. Bandaria, J.; Dutta, S.; Nydegger, M. W.; Rock, W.; Kohen, A.; Cheatum, C. Characterizing the dynamics of functionally relevant complexes of formate dehydrogenase Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 17974-17979
31. Bandaria, J.; Cheatum, C.; Kohen, A. Examination of enzymatic H-tunneling through kinetics and dynamics J. Am. Chem. Soc. 2009, 131, 10151-10155
32. Francisco, W. A.; Knapp, M. J.; Blackburn, N. J.; Klinman, J. P. Hydrogen tunneling in peptidylglycine-hydroxylating monooxygenase J. Am. Chem. Soc. 2002, 124, 8194-8195
33. Hay, S.; Sutcliffe, M. J.; Scrutton, N. Probing coupled motions in enzymatic hydrogen tunneling reactions: Beyond temperature-dependence studies of kinetic isotope effects. In Quantum Tunnelling in Enzyme Catalyzed Reactions; Allemann, R.; Scrutton, N., Eds.; Royal Society of Chemistry: London, U.K., 2009; Chapter 9; pp 199-218.
34. Loveridge, E. J.; Behiry, E. M.; Guo, J.; Allemann, R. K. Evidence that a 'dynamic knockout' in Escherichia coli dihydrofolate reductase does not affect the chemical step of catalysis Nat. Chem. 2012, 4, 292-297
35. Fan, F.; Gadda, G. Oxygen- and temperature-dependent kinetic isotope effects in choline oxidase: Correlating reversible hydride transfer with environmentally enhanced tunneling J. Am. Chem. Soc. 2005, 127, 17954-17961
36. Sikorski, R. S.; Wang, L.; Markham, K. A.; Rajagopalan, P. T. R.; Benkovic, S. J.; Kohen, A. Tunneling and coupled motion in the Escherichia coli dihydrofolate reductase catalysis J. Am. Chem. Soc. 2004, 126, 4778-4779
37. Sen, A.; Yahashiri, A.; Kohen, A. Triple isotopic labeling and kinetic isotope effects: Exposing H-transfer steps in enzymatic systems Biochemistry 2011, 50, 6462-6468
38. Nagel, Z. D.; Klinman, J. P. A 21st century revisionist's view at a turning point in enzymology Nat. Chem. Biol. 2009, 5, 543-550
39. Kamerlin, S. C. L.; Warshel, A. At the dawn of the 21st century: Is dynamics the missing link for understanding enzyme catalysis? Proteins 2010, 78, 1339-1375
40. Hatcher, E.; Soudackov, A. V.; Hammes-Schiffer, S. Proton-coupled electron transfer in soybean lipoxygenase J. Am. Chem. Soc. 2004, 126, 5763-5775
41. Basner, J. E.; Schwartz, S. D. Donor-acceptor distance and protein promoting vibration coupling to hydride transfer: A possible mechanism for kinetic control in isozymes of human lactate dehydrogenase J. Phys. Chem. B 2004, 108, 444-451
42. Boekelheide, N.; Salomón-Ferrer, R.; Miller, T. F. Dynamics and dissipation in enzyme catalysis Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 16159-16163
43. Leitner, D. M. Energy flow in proteins Annu. Rev. Phys. Chem. 2008, 59, 233-259
44. Basner, J. E.; Schwartz, S. D. How enzyme dynamics helps catalyze a reaction in atomic detail: A transition path sampling study J. Am. Chem. Soc. 2005, 127, 13822-13831
45. Bolhuis, P. G.; Chandler, D.; Dellago, C.; Geissler, P. L. Transition path sampling: Throwing ropes over rough mountain passes, in the dark Annu. Rev. Phys. Chem. 2002, 53, 291-318
46. Warshel, A. Dynamics of reactions in polarsolventys-semi-classical trajectory studies of electron-transfer and proton-transfer reactions J. Phys. Chem. 1982, 86, 2218-2224
47. Silva, R. G.; Murkin, A. S.; Schramm, V. L. Femtosecond dynamics coupled to chemical barrier crossing in a Born-Oppenheimer enzyme Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 18661-18665