Divergent evolution of protein conformational dynamics in dihydrofolate reductase

Nature Structural and Molecular Biology

Volumn 20, Issue 11, 2013, Pages 1243-1249

  Bhabha, Gira ^a,c   Ekiert, Damian C ^a,c   Jennewein, Madeleine ^a   Zmasek, Christian M ^b   Tuttle, Lisa M ^a   Kroon, Gerard ^a   Dyson, H Jane ^a   Godzik, Adam ^b   Wilson, Ian A ^a   Wright, Peter E ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b BURNHAM INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIHYDROFOLATE REDUCTASE;

ARTICLE; BACTERIAL CELL; DIVERGENT EVOLUTION; ENZYME ACTIVE SITE; ESCHERICHIA COLI; GENETIC DRIFT; HUMAN; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; NATURAL SELECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN FUNCTION; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; GENETIC COMPLEMENTATION TEST; GENETIC DRIFT; HUMANS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN CONFORMATION; SELECTION, GENETIC; SEQUENCE ALIGNMENT; TETRAHYDROFOLATE DEHYDROGENASE;

ESCHERICHIA COLI;

EID: 84887464612     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2676     Document Type: Article

References (54)

1. Halabi, N., Rivoire, O., Leibler, S. & Ranganathan, R. Protein sectors: evolutionary units of three-dimensional structure. Cell 138, 774-786 (2009).
2. Alexander, P.A., He, Y., Chen, Y., Orban, J. & Bryan, P.N. A minimal sequence code for switching protein structure and function. Proc. Natl. Acad. Sci. USA 106, 21149-21154 (2009).
3. Thompson, J. & Baker, D. Incorporation of evolutionary information into Rosetta comparative modeling. Proteins 79, 2380-2388 (2011).
4. Kohen, A. & Klinman, J.P. Protein flexibility correlates with degree of hydrogen tunneling in thermophilic and mesophilic alcohol dehydrogenases. J. Am. Chem. Soc. 122, 10738-10739 (2000).
5. Wolf-Watz, M. et al. Linkage between dynamics and catalysis in a thermophilic-mesophilic enzyme pair. Nat. Struct. Mol. Biol. 11, 945-949 (2004).
6. Schnell, J.R., Dyson, H.J. & Wright, P.E. Structure, dynamics and catalytic function of dihydrofolate reductase. Annu. Rev. Biophys. Biomol. Struct. 33, 119-140 (2004).
7. Brown, K.M. et al. Compensatory mutations restore fitness during the evolution of dihydrofolate reductase. Mol. Biol. Evol. 27, 2682-2690 (2010).
8. Fierke, C.A., Johnson, K.A. & Benkovic, S.J. Construction and evaluation of the kinetic scheme associated with dihydrofolate reductase from Escherichia coli. Biochemistry 26, 4085-4092 (1987).
9. Appleman, J.R. et al. Unusual transient-and steady-state kinetic behavior is predicted by the kinetic scheme operational for recombinant human dihydrofolate reductase. J. Biol. Chem. 265, 2740-2748 (1990).
10. Appleman, J.R. et al. Atypical transient state kinetics of recombinant human dihydrofolate reductase produced by hysteretic behavior: comparison with dihydrofolate reductases from other sources. J. Biol. Chem. 264, 2625-2633 (1989).
11. Beard, W.A., Appleman, J.R., Delcamp, T.J., Freisheim, J.H. & Blakley, R.L. Hydride transfer by dihydrofolate reductase: causes and consequences of the wide range of rates exhibited by bacterial and vertebrate enzymes. J. Biol. Chem. 264, 9391-9399 (1989).
12. Matthews, D.A. et al. Dihydrofolate reductase: X-ray structure of the binary complex with methotrexate. Science 197, 452-455 (1977).
13. Beard, W.A. et al. Role of the conserved active site residue tryptophan-24 of human dihydrofolate reductase as revealed by mutagenesis. Biochemistry 30, 1432-1440 (1991).
14. Bhabha, G. et al. A dynamic knockout reveals that conformational fluctuations influence the chemical step of enzyme catalysis. Science 332, 234-238 (2011).
15. Hammes, G.G., Benkovic, S.J. & Hammes-Schiffer, S. Flexibility, diversity, and cooperativity: pillars of enzyme catalysis. Biochemistry 50, 10422-10430 (2011).
16. Boehr, D.D., McElheny, D., Dyson, H.J. & Wright, P.E. The dynamic energy landscape of dihydrofolate reductase catalysis. Science 313, 1638-1642 (2006).
17. Bystroff, C. & Kraut, J. Crystal structure of unliganded Escherichia coli dihydrofolate reductase: ligand-induced conformational changes and cooperativity in binding. Biochemistry 30, 2227-2239 (1991).
18. Sawaya, M.R. & Kraut, J. Loop and subdomain movements in the mechanism of Escherichia coli dihydrofolate reductase: crystallographic evidence. Biochemistry 36, 586-603 (1997).
19. Osborne, M.J., Schnell, J., Benkovic, S.J., Dyson, H.J. & Wright, P.E. Backbone dynamics in dihydrofolate reductase complexes: role of loop flexibility in the catalytic mechanism. Biochemistry 40, 9846-9859 (2001).
20. Osborne, M.J., Venkitakrishnan, R.P., Dyson, H.J. & Wright, P.E. Diagnostic chemical shift markers for loop conformation and cofactor binding in dihydrofolate reductase complexes. Protein Sci. 12, 2230-2238 (2003).
21. Venkitakrishnan, R.P. et al. Conformational changes in the active site loops of dihydrofolate reductase during the catalytic cycle. Biochemistry 43, 16046-16055 (2004).
22. Miller, G.P. & Benkovic, S.J. Stretching exercises: flexibility in dihydrofolate reductase catalysis. Chem. Biol. 5, R105-R113 (1998).
23. Miller, G.P., Wahnon, D.C. & Benkovic, S.J. Interloop contacts modulate ligand cycling during catalysis by Escherichia coli dihydrofolate reductase. Biochemistry 40, 867-875 (2001).
24. Davies, J.F. II et al. Crystal structures of recombinant human dihydrofolate reductase complexed with folate and 5-deazafolate. Biochemistry 29, 9467-9479 (1990).
25. Boehr, D.D., McElheny, D., Dyson, H.J. & Wright, P.E. Millisecond timescale fluctuations in dihydrofolate reductase are exquisitely sensitive to the bound ligands. Proc. Natl. Acad. Sci. USA 107, 1373-1378 (2010).
26. Miller, G.P. & Benkovic, S.J. Strength of an interloop hydrogen bond determines the kinetic pathway in catalysis by Escherichia coli dihydrofolate reductase. Biochemistry 37, 6336-6342 (1998).
27. Cody, V., Pace, J. & Rosowsky, A. Structural analysis of a holoenzyme complex of mouse dihydrofolate reductase with NADPH and a ternary complex with the potent and selective inhibitor 2,4-diamino-6-(2'-hydroxydibenz[b,f]azepin-5- yl)methylpteridine. Acta Crystallogr. D Biol. Crystallogr. 64, 977-984 (2008).
28. Liu, C.T. et al. Functional significance of evolving protein sequence in dihydrofolate reductase from bacteria to humans. Proc. Natl. Acad. Sci. USA 110, 10159-10164 (2013).
29. Whitlow, M. et al. X-ray crystallographic studies of Candida albicans dihydrofolate reductase. J. Biol. Chem. 272, 30289-30298 (1997).
30. Ahmad, S.I., Kirk, S.H. & Eisenstark, A. Thymine metabolism and thymineless death in prokaryotes and eukaryotes. Annu. Rev. Microbiol. 52, 591-625 (1998).
31. Fierke, C.A., Kuchta, R.D., Johnson, K.A. & Benkovic, S.J. Implications for enzymic catalysis from free-energy reaction coordinate profiles. Cold Spring Harb. Symp. Quant. Biol. 52, 631-638 (1987).
32. Allegra, C.J., Fine, R.L., Drake, J.C. & Chabner, B.A. The effect of methotrexate on intracellular folate pools in human MCF-7 breast cancer cells. Evidence for direct inhibition of purine synthesis. J. Biol. Chem. 261, 6478-6485 (1986).
33. Greenbaum, A.L., Gumaa, K.A. & Mclean, P. The distribution of hepatic metabolites and the control of the pathways of carbohydrate metabolism in animals of different dietary and hormonal status. Arch. Biochem. Biophys. 143, 617-663 (1971).
34. Cameron, C.E. & Benkovic, S.J. 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 36, 15792-15800 (1997).
35. Johnson, G.T., Autin, L., Goodsell, D.S., Sanner, M.F. & Olson, A.J. ePMV embeds molecular modeling into professional animation software environments. Structure 19, 293-303 (2011).
36. Edelstein, A., Amodaj, N., Hoover, K., Vale, R. & Stuurman, N. Computer control of microscopes using ?Manager. Curr. Protoc. Mol. Biol. 92, 14.20 (2010).
37. Bhabha, G., Tuttle, L., Martinez-Yamout, M.A. & Wright, P.E. Identification of endogenous ligands bound to bacterially expressed human and E. coli dihydrofolate reductase by 2D NMR. FEBS Lett. 585, 3528-3532 (2011).
38. Loria, J.P., Rance, M. & Palmer, A.G. III. A relaxation-compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy. J. Am. Chem. Soc. 121, 2331-2332 (1999).
39. McElheny, D., Schnell, J.R., Lansing, J.C., Dyson, H.J. & Wright, P.E. Defining the role of active-site loop fluctuations in dihydrofolate reductase catalysis. Proc. Natl. Acad. Sci. USA 102, 5032-5037 (2005).
40. Sugase, K., Konuma, T., Lansing, J.C. & Wright, P.E. Fast and accurate fitting of relaxation dispersion data using the flexible software package GLOVE. J. Biomol. NMR 56, 275-283 (2013).
41. Massi, F., Johnson, E., Wang, C., Rance, M. & Palmer, A.G. III. NMR R1? rotating-frame relaxation with weak radio frequency fields. J. Am. Chem. Soc. 126, 2247-2256 (2004).
42. Farrow, N.A. et al. Backbone dynamics of a free and a phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33, 5984-6003 (1994).
43. Farrow, N.A., Zhang, O., Forman-Kay, J.D. & Kay, L.E. A heteronuclear correlation experiment for simultaneous determination of 15N longitudinal decay and chemical exchange rates of systems in slow equilibrium. J. Biomol. NMR 4, 727-734 (1994).
44. Massi, F., Grey, M.J. & Palmer, A.G. III. Microsecond timescale backbone conformational dynamics in ubiquitin studied with NMR R1? relaxation experiments. Protein Sci. 14, 735-742 (2005).
45. Lewis, W.S. et al. Methotrexate-resistant variants of human dihydrofolate reductase with substitutions of leucine 22: kinetics, crystallography, and potential as selectable markers. J. Biol. Chem. 270, 5057-5064 (1995).
46. Adams, P.D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948-1954 (2002).
47. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
48. Chen, V.B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21 (2010).
49. Hayward, S. & Berendsen, H.J. Systematic analysis of domain motions in proteins from conformational change: new results on citrate synthase and T4 lysozyme. Proteins 30, 144-154 (1998).
50. Punta, M. et al. The Pfam protein families database. Nucleic Acids Res. 40, D290-D301 (2012).
51. Edgar, R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
52. Katoh, K. & Toh, H. Parallelization of the MAFFT multiple sequence alignment program. Bioinformatics 26, 1899-1900 (2010).
53. Desper, R. & Gascuel, O. Fast and accurate phylogeny reconstruction algorithms based on the minimum-evolution principle. J. Comput. Biol. 9, 687-705 (2002).
54. Datsenko, K.A. & Wanner, B.L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97, 6640-6645 (2000).