Network of remote and local protein dynamics in dihydrofolate reductase catalysis

ACS Catalysis

Volumn 5, Issue 5, 2015, Pages 3067-3073

  Singh, Priyanka ^a   Francis, Kevin ^a   Kohen, Amnon ^a  

^a University of Iowa   (United States)

Author keywords

dihydrofolate reductase; dynamic network; enzyme dynamics; kinetic isotope effects; tunneling

Indexed keywords

CARRIER MOBILITY; CHEMICAL ACTIVATION; CHEMICAL BONDS; DYNAMICS; ELECTRON TUNNELING; ENZYME KINETICS; ENZYMES; ESCHERICHIA COLI; ISOTOPES; MOLECULAR DYNAMICS; PROTEINS; RATE CONSTANTS; REACTION KINETICS; TEMPERATURE DISTRIBUTION;

DIHYDROFOLATE REDUCTASE; DYNAMIC NETWORK; ENZYME DYNAMICS; EXPERIMENTAL EVIDENCE; KINETIC ISOTOPE EFFECTS; MICROSCOPIC RATE CONSTANTS; MOLECULAR DYNAMICS CALCULATION; TEMPERATURE DEPENDENCE;

CATALYSIS;

EID: 84928958247     PISSN: 21555435     EISSN: None     Source Type: Journal    
DOI: 10.1021/acscatal.5b00331     Document Type: Article

References (59)

1. Adamczyk, A. J.; Cao, J.; Kamerlin, S. C. L.; Warshel, A. Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 14115-14120 10.1073/pnas.1111252108
2. Hammes, G. G.; Benkovic, S. J.; Hammes-Schiffer, S. Biochemistry 2011, 50, 10422-10430 10.1021/bi201486f
3. Liu, H.; Warshel, A. In Quantum Tunnelling in Enzyme-Catalysed Reactions; Allemann, R. K.; Scrutton, N. S., Eds.; The Royal Society of Chemistry: Cambridge, U.K., 2009; pp 242-267.
4. Ruiz-Pernia, J. J.; Luk, L. Y. P.; García-Meseguer, R.; Martí, S.; Loveridge, E. J.; Tuñón, I.; Moliner, V.; Allemann, R. K. J. Am. Chem. Soc. 2013, 135, 18689-18696 10.1021/ja410519h
5. Fan, Y.; Cembran, A.; Ma, S.; Gao, J. Biochemistry 2013, 52, 2036-2049 10.1021/bi301559q
6. Sawaya, M. R.; Kraut, J. Biochemistry 1997, 36, 586-603 10.1021/bi962337c
7. Rod, T. H.; Radkiewicz, J. L.; Brooks, C. L. Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 6980-6985 10.1073/pnas.1230801100
8. Dametto, M.; Antoniou, D.; Schwartz, S. D. Mol. Phys. 2012, 110, 531-536 10.1080/00268976.2012.655337
9. Fierke, C. A.; Johnson, K. A.; Benkovic, S. J. Biochemistry 1987, 26, 4085-4092 10.1021/bi00387a052
10. Grubbs, J.; Rahmanian, S.; DeLuca, A.; Padmashali, C.; Jackson, M.; Duff, M. R.; Howell, E. E. Biochemistry 2011, 50, 3673-3685 10.1021/bi2002373
11. Radkiewicz, J. L.; Brooks, C. L. J. Am. Chem. Soc. 2000, 122, 225-231 10.1021/ja9913838
12. Hammes-Schiffer, S. Acc. Chem. Res. 2005, 39, 93-100 10.1021/ar040199a
13. Klinman, J. P.; Kohen, A. Annu. Rev. Biochem. 2013, 82, 471-496 10.1146/annurev-biochem-051710-133623
14. Francis, K.; Kohen, A. Curr. Opin. Chem. Biol. 2014, 21, 19-24 10.1016/j.cbpa.2014.03.009
15. Glowacki, D. R.; Harvey, J. N.; Mulholland, A. J. Nat. Chem. 2012, 4, 169-176 10.1038/nchem.1244
16. Lee, J.; Goodey, N. M. Chem. Rev. 2011, 111, 7595-7624 10.1021/cr100042n
17. Liu, H.; Warshel, A. J. Phys. Chem. B 2007, 111, 7852-7861 10.1021/jp070938f
18. Kamerlin, S. C. L.; Warshel, A. Proteins: Struct., Funct., Genet. 2010, 78, 1339-1375 10.1002/prot.22654
19. Nagel, Z. D.; Klinman, J. P. Chem. Rev. 2010, 110, PR41-PR67 10.1021/cr1001035
20. Hay, S.; Scrutton, N. S. Nat. Chem. 2012, 4, 161-168 10.1038/nchem.1223
21. Kohen, A. In Isotopes Effects in Chemistry and Biology; Kohen, A.; Limbach, H.-H., Eds.; Taylor and Francis: Boca Raton, FL, 2006; pp 743-764.
22. Ben-David, M.; Sussman, J. L.; Maxwell, C. I.; Szeler, K.; Kamerlin, S. C. L.; Tawfik, D. S. J. Mol. Biol. 2015, 427, 1359-1374 10.1016/j.jmb.2015.01.013
23. Singh, P.; Sen, A.; Francis, K.; Kohen, A. J. Am. Chem. Soc. 2014, 136, 2575-2582 10.1021/ja411998h
24. Francis, K.; Stojković, V.; Kohen, A. J. Biol. Chem. 2013, 288, 35961-35968 10.1074/jbc.M113.507632
25. Stojković, V.; Perissinotti, L. L.; Willmer, D.; Benkovic, S. J.; Kohen, A. J. Am. Chem. Soc. 2012, 134, 1738-1745 10.1021/ja209425w
26. Wang, L.; Goodey, N. M.; Benkovic, S. J.; Kohen, A. Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 15753-15758 10.1073/pnas.0606976103
27. Maglia, G.; Allemann, R. K. J. Am. Chem. Soc. 2003, 125, 13372-13373 10.1021/ja035692g
28. Roston, D.; Cheatum, C. M.; Kohen, A. Biochemistry 2012, 51, 6860-6870 10.1021/bi300613e
29. Kohen, A. Acc. Chem. Res. 2015, 48, 466-473 10.1021/ar500322s
30. Roston, D.; Islam, Z.; Kohen, A. Molecules 2013, 18, 5543-5567 10.3390/molecules18055543
31. Rajagopalan, P. T. R.; Stefan, L.; Benkovic, S. J. Biochemistry 2002, 41, 12618-12628 10.1021/bi026369d
32. Boehr, D. D.; McElheny, D.; Dyson, H. J.; Wright, P. E. Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 1373-1378 10.1073/pnas.0914163107
33. Antikainen, N. M.; Smiley, R. D.; Benkovic, S. J.; Hammes, G. G. Biochemistry 2005, 44, 16835-16843 10.1021/bi051378i
34. Boehr, D. D.; McElheny, D.; Dyson, H. J.; Wright, P. E. Science 2006, 313, 1638-1642 10.1126/science.1130258
35. Wong, K. F.; Selzer, T.; Benkovic, S. J.; Hammes-Schiffer, S. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 6807-6812 10.1073/pnas.0408343102
36. Agarwal, P. K.; Billeter, S. R.; Rajagopalan, P. T.; Benkovic, S. J.; Hammes-Schiffer, S. Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 2794-2799 10.1073/pnas.052005999
37. Roston, D.; Kohen, A.; Doron, D.; Major, D. T. J. Comput. Chem. 2014, 35, 1411-1417 10.1002/jcc.23629
38. Ramanathan, A.; Agarwal, P. K. PLoS Biol. 2011, 9, e1001193 10.1371/journal.pbio.1001193
39. Hammes-Schiffer, S.; Benkovic, S. J. Annu. Rev. Biochem. 2006, 75, 519-541 10.1146/annurev.biochem.75.103004.142800
40. Agarwal, P. K.; Billeter, S. R.; Hammes-Schiffer, S. J. Phys. Chem. B 2002, 106, 3283-3293 10.1021/jp020190v
41. Schnell, J. R.; Dyson, H. J.; Wright, P. E. Biochemistry 2003, 43, 374-383 10.1021/bi035464z
42. Wang, L.; Tharp, S.; Selzer, T.; Benkovic, S. J.; Kohen, A. Biochemistry 2006, 45, 1383-1392 10.1021/bi0518242
43. Boehr, D. D.; Schnell, J. R.; McElheny, D.; Bae, S.-H.; Duggan, B. M.; Benkovic, S. J.; Dyson, H. J.; Wright, P. E. Biochemistry 2013, 52, 4605-4619 10.1021/bi400563c
44. Mauldin, R. V.; Sapienza, P. J.; Petit, C. M.; Lee, A. L. PLoS One 2012, 7, e33252 10.1371/journal.pone.0033252
45. Agrawal, N.; Kohen, A. Anal. Biochem. 2003, 322, 179-184 10.1016/j.ab.2003.08.012
46. Markham, K. A.; Sikorski, R. S.; Kohen, A. Anal. Biochem. 2004, 322, 26-32 10.1016/j.ab.2003.07.010
47. Markham, K. A.; Sikorski, R. S.; Kohen, A. Anal. Biochem. 2004, 325, 62-67 10.1016/j.ab.2003.10.027
48. McCracken, J. A.; Wang, L.; Kohen, A. Anal. Biochem. 2003, 324, 131-136 10.1016/j.ab.2003.09.025
49. Sen, A.; Yahashiri, A.; Kohen, A. Biochemistry 2011, 50, 6462-6468 10.1021/bi2003873
50. Blakley, R. L. Nature 1960, 188, 231-232 10.1038/188231a0
51. Stojković, V.; Perissinotti, L. L.; Lee, J.; Benkovic, S. J.; Kohen, A. Chem. Commun. 2010, 46, 8974-8976 10.1039/c0cc02988b
52. Cameron, C. E.; Benkovic, S. J. Biochemistry 1997, 36, 15792-15800 10.1021/bi9716231
53. Wang, Z.; Singh, P.; Czekster, C. M.; Kohen, A.; Schramm, V. L. J. Am. Chem. Soc. 2014, 136, 8333-8341 10.1021/ja501936d
54. Liu, C. T.; Francis, K.; Layfield, J. P.; Huang, X.; Hammes-Schiffer, S.; Kohen, A.; Benkovic, S. J. Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 18231-18236 10.1073/pnas.1415940111
55. Sikorski, R. S.; Wang, L.; Markham, K. A.; Rajagopalan, P. T.; Benkovic, S. J.; Kohen, A. J. Am. Chem. Soc. 2004, 126, 4778-4779 10.1021/ja031683w
56. Cheatum, C.; Kohen, A. In Dynamics in Enzyme Catalysis; Klinman, J.; Hammes-Schiffer, S., Eds.; Springer Berlin Heidelberg: Berlin Heidelberg, 2013; Vol. 337, pp 1-39.
57. Kanaan, N.; Ferrer, S.; Martí, S.; Garcia-Viloca, M.; Kohen, A.; Moliner, V. J. Am. Chem. Soc. 2011, 133, 6692-6702 10.1021/ja1114369
58. Wang, Z.; Abeysinghe, T.; Finer-Moore, J. S.; Stroud, R. M.; Kohen, A. J. Am. Chem. Soc. 2012, 134, 17722-17730 10.1021/ja307859m
59. Cook, P. F.; Cleland, W. W.; Taylor and Francis Group LLC: New York, NY, 2007; pp 253-324.