Side-chain conformational heterogeneity of intermediates in the escherichia coli dihydrofolate reductase catalytic cycle

Biochemistry

Volumn 52, Issue 20, 2013, Pages 3464-3477

  Tuttle, Lisa M ^a   Dyson, H Jane ^a   Wright, Peter E ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC SIDE CHAINS; CONFORMATIONAL HETEROGENEITY; COUPLING CONSTANTS; DIHYDROFOLATE REDUCTASE; DYNAMIC INFORMATION; ENZYME FUNCTIONS; SIDE-CHAIN DYNAMICS; STRUCTURAL CHANGE;

AROMATIC COMPOUNDS; LIGANDS;

ESCHERICHIA COLI;

ADENOSINE; DIHYDROFOLATE REDUCTASE;

ARTICLE; CATALYSIS; ENZYME CONFORMATION; ESCHERICHIA COLI; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; TIME;

BINDING SITES; BIOCATALYSIS; CATALYTIC DOMAIN; ESCHERICHIA COLI; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; TETRAHYDROFOLATE DEHYDROGENASE;

EID: 84878224305     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400322e     Document Type: Article

References (40)

1. Bystroff, C., Oatley, S. J., and Kraut, J. (1990) Crystal structures of Escherichia coli dihydrofolate reductase: the NADP+ holoenzyme and the folate.NADP+ ternary complex. Substrate binding and a model for the transition state Biochemistry 29, 3263-3277
2. Bystroff, C. and Kraut, J. (1991) Crystal structure of unliganded Escherichia coli dihydrofolate reductase. Ligand-induced conformational changes and cooperativity in binding Biochemistry 30, 2227-2239
3. Sawaya, M. R. and Kraut, J. (1997) Loop and subdomain movements in the mechanism of Escherichia coli dihydrofolate reductase: crystallographic evidence Biochemistry 36, 586-603
4. Schnell, J. R., Dyson, H. J., and Wright, P. E. (2004) Structure, dynamics and catalytic function of dihydrofolate reductase Annu. Rev. Biophys. Biomol. Struct. 33, 119-140
5. Boehr, D. D., McElheny, D., Dyson, H. J., and Wright, P. E. (2010) Millisecond timescale fluctuations in dihydrofolate reductase are exquisitely sensitive to the bound ligands Proc. Natl. Acad. Sci. U. S. A. 107, 1373-1378
6. Boehr, D. D., McElheny, D., Dyson, H. J., and Wright, P. E. (2006) The dynamic energy landscape of dihydrofolate reductase catalysis Science 313, 1638-1642
7. Mittermaier, A., Kay, L. E., and Forman-Kay, J. D. (1999) Analysis of deuterium relaxation-derived methyl axis order parameters and correlation with local structure J. Biomol. NMR 13, 181-185
8. 13C-relaxation studies of randomly fractionally labeled protein Biochemistry 35, 6116-6125
9. Schnell, J. R., Dyson, H. J., and Wright, P. E. (2004) Effect of cofactor binding and loop conformation on side chain methyl dynamics in dihydrofolate reductase Biochemistry 43, 374-383
10. Fraser, J. S., van den Bedem, H., Samelson, A. J., Lang, P. T., Holton, J. M., Echols, N., and Alber, T. (2011) Accessing protein conformational ensembles using room-temperature X-ray crystallography Proc. Natl. Acad. Sci. U. S. A. 108, 16247-16252
11. Osborne, M. J., Schnell, J., Benkovic, S. J., Dyson, H. J., and Wright, P. E. (2001) Backbone dynamics in dihydrofolate reductase complexes: Role of loop flexibility in the catalytic mechanism Biochemistry 40, 9846-9859
12. Radkiewicz, J. L. and Brooks, C. L. (2000) Protein dynamics in enzymatic catalysis: Exploration of dihydrofolate reductase J. Am. Chem. Soc. 122, 225-231
13. Agarwal, P. K., Billeter, S. R., Rajagopalan, P. T. R., Benkovic, S. J., and Hammes-Schiffer, S. (2002) Network of coupled promoting motions in enzyme catalysis Proc. Natl. Acad. Sci. U. S. A. 99, 2794-2799
14. Chou, J. J., Case, D. A., and Bax, A. (2003) Insights into the mobility of methyl-bearing side chains in proteins from (3)J(CC) and (3)J(CN) coupling J. Am. Chem. Soc. 125, 8959-8966
15. Shapovalov, M. V. and Dunbrack, R. L., Jr. (2011) A smoothed backbone-dependent rotamer library for proteins derived from adaptive kernel density estimates and regressions Structure 19, 844-858
16. MacArthur, M. W. and Thornton, J. M. (1999) Protein side-chain conformation: a systematic variation of chi 1 mean values with resolution-a consequence of multiple rotameric states? Acta Crystallogr. D. Biol. Crystallogr. 55, 994-1004
17. Shapovalov, M. V. and Dunbrack, R. L., Jr. (2007) Statistical and conformational analysis of the electron density of protein side chains Proteins 66, 279-303
18. Karplus, M. (1963) Vicinal proton coupling in nuclear magnetic resonance J. Am. Chem. Soc. 85, 2870-2871
19. Schmidt, J. M. (2007) Asymmetric Karplus curves for the protein side-chain 3J couplings J. Biomol. NMR 37, 287-301
20. Pachler, K. G. R. (1963) Nuclear magnetic resonance study of some [alpha]-amino acids - I: Coupling constants in alkaline and acidic medium Spectrochim. Acta 19, 2085-2092
21. Pachler, K. G. R. (1964) Nuclear magnetic resonance study of some [alpha]-amino acids - II: Rotational isomerism Spectrochim. Acta 20, 581-587
22. Fraser, J. S., Clarkson, M. W., Degnan, S. C., Erion, R., Kern, D., and Alber, T. (2009) Hidden alternative structures of proline isomerase essential for catalysis Nature 462, 669-673
23. Bhabha, G., Lee, J., Ekiert, D. C., Gam, J., Wilson, I. A., Dyson, H. J., Benkovic, S. J., and Wright, P. E. (2011) A Dynamic Knockout Reveals That Conformational Fluctuations Influence the Chemical Step of Enzyme Catalysis Science 332, 234-238
24. 13C NMR Chemical Shifts ChemBioChem 10, 1477-1479
25. Bhabha, G., Tuttle, L., Martinez-Yamout, M. A., and Wright, P. E. (2011) Identification of endogenous ligands bound to bacterially expressed human and E. coli dihydrofolate reductase by 2D NMR FEBS Lett. 585, 3528-3532
26. 13C magnetization J. Magn. Reson. Ser. B 101, 114-119
27. Montelione, G. T., Lyons, B. A., Emerson, S. D., and Tashiro, M. (1992) An efficient triple resonance experiment using carbon-13 isotropic mixing for determining sequence-specific resonance assignments of isotopically-enriched proteins J. Am. Chem. Soc. 114, 10974-10975
28. Grzesiek, S. and Bax, A. (1992) Improved 3D triple-resonance NMR techniques applied to a 31 kDa protein J. Magn. Reson. 96, 432-440
29. CC couplings between backbone carbonyl and methyl carbons in isotopically enriched proteins J. Biomol. NMR 3, 487-493
30. 13C J. Am. Chem. Soc. 115, 5334-5335
31. NCγ couplings in isotopically enriched proteins J. Biomol. NMR 9, 323-328
32. NCγ couplings J. Am. Chem. Soc. 119, 1803-1804
33. Perez, C., Löhr, F., Rüterjans, H., and Schmidt, J. M. (2001) Self-consistent Karplus parametrization of 3J couplings depending on the polypeptide side-chain torsion chi1 J. Am. Chem. Soc. 123, 7081-7093
34. 15N NMR spectroscopy J. Mol. Biol. 288, 705-723
35. 13C' chemical shifts in proteins using a density functional database J. Biomol. NMR 21, 321-333
36. Case, D. A., Scheurer, C., and Brüschweiler, R. (2000) Static and dynamic effects on vicinal scalar J couplings in proteins and peptides: A MD/DFT analysis J. Am. Chem. Soc. 122, 10390-10397
37. Vajpai, N., Gentner, M., Huang, J. r., Blackledge, M., and Grzesiek, S. (2010) Side-Chain χ1 Conformations in Urea-Denatured Ubiquitin and Protein G from 3J Coupling Constants and Residual Dipolar Coupling J. Am. Chem. Soc. 132, 3196-3203
38. Dunbrack, R. L., Jr. (2002) Rotamer libraries in the 21st century Curr. Opin. Struct. Biol. 12, 431-440
39. Hu, H., Hermans, J., and Lee, A. L. (2005) Relating side-chain mobility in proteins to rotameric transitions: Insights from molecular dynamics simulations and NMR J. Biomol. NMR 32, 151-162
40. Scouras, A. D. and Daggett, V. (2011) The Dynameomics rotamer library: amino acid side chain conformations and dynamics from comprehensive molecular dynamics simulations in water Protein Sci. 20, 341-352