Evolutionarily conserved linkage between enzyme fold, flexibility, and catalysis

PLoS Biology

Volumn 9, Issue 11, 2011, Pages

  Ramanathan, Arvind ^a,b   Agarwal, Pratul K ^b  

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ISOMERASE; NUCLEASE; OXIDOREDUCTASE; PROLYL PEPTIDYL ISOMERASE; UNCLASSIFIED DRUG; CYCLOPHILIN; ENZYME; PEPTIDYLPROLYL ISOMERASE; RIBONUCLEASE;

ARTICLE; CATALYSIS; CATTLE; CHEMICAL REACTION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME CONFORMATION; ENZYME FLEXIBILITY; ENZYME FOLDING; ENZYME MECHANISM; GENETIC CONSERVATION; HUMAN; MATHEMATICAL MODEL; NONHUMAN; PLASMODIUM FALCIPARUM; THERMODYNAMICS; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; METABOLISM; MOLECULAR EVOLUTION; PROTEIN FOLDING;

CATALYSIS; COMPUTER SIMULATION; CYCLOPHILINS; ENZYMES; EVOLUTION, MOLECULAR; HUMANS; MODELS, MOLECULAR; OXIDOREDUCTASES; PEPTIDYLPROLYL ISOMERASE; PROTEIN FOLDING; RIBONUCLEASES;

EID: 82455175792     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001193     Document Type: Article

References (88)

1. Furnham N, Blundell T. L, DePristo M. A, Terwilliger T. C, (2006) Is one solution good enough? Nat Struct Mol Biol 13: 184-185.
2. Hammes-Schiffer S, Benkovic S. J, (2006) Relating protein motion to catalysis. Annu Rev Biochem 75: 519-541.
3. Boehr D. D, Dyson H. J, Wright P. E, (2006) An NMR perspective on enzyme dynamics. Chem Rev 106: 3055-3079.
4. Olsson M. H, Parson W. W, Warshel A, (2006) Dynamical contributions to enzyme catalysis: critical tests of a popular hypothesis. Chem Rev 106: 1737-1756.
5. Henzler-Wildman K. A, Lei M, Thai V, Kerns S. J, Karplus M, et al. (2007) A hierarchy of timescales in protein dynamics is linked to enzyme catalysis. Nature 450: 913-916.
6. Nagel Z. D, Klinman J. P, (2009) A 21(st) century revisionist's view at a turning point in enzymology. Nat Chem Biol 5: 543-550.
7. Pisliakov A. V, Cao J, Kamerlin S. C. L, Warshel A, (2009) Enzyme millisecond conformational dynamics do not catalyze the chemical step. Proc Natl Acad Sci U S A 106: 17359-17364.
8. Koshland D. E, (1958) Application of a theory of enzyme specificity to protein synthesis. Proc Natl Acad Sci U S A 44: 98-104.
9. Benkovic S. J, Hammes G. G, Hammes-Schiffer S, (2008) Free-energy landscape of enzyme catalysis. Biochemistry 47: 3317-3321.
10. Doucet N, Watt E. D, Loria J. P, (2009) The flexibility of a distant loop modulates active site motion and product release in ribonuclease A. Biochemistry 48: 7160-7168.
11. Radkiewicz J, Brooks I. C, (2000) Protein dynamics in enzymatic catalysis: exploration of dihydrofolate reductase. J Am Chem Soc 122: 225-231.
12. Agarwal P. K, Billeter S. R, Rajagopalan P. T. R, Benkovic S. J, Hammes-Schiffer S, (2002) Network of coupled promoting motions in enzyme catalysis. Proc Natl Acad Sci U S A 99: 2794-2799.
13. Garcia-Viloca M. T, Truhlar D. G, Gao J. L, (2003) Reaction-path energetics and kinetics of the hydride transfer reaction catalyzed by dihydrofolate reductase. Biochemistry 42: 13558-13575.
14. Mincer J. S, Schwartz S. D, (2004) Rate-promoting vibrations and coupled hydrogen-electron transfer reactions in the condensed phase: a model for enzymatic catalysis. J Chem Phys 120: 7755-7760.
15. Agarwal P. K, (2006) Enzymes: an integrated view of structure, dynamics and function. Microbial Cell Fact 5: 2.
16. Cannon W. R, Benkovic S. J, (1998) Solvation, reorganization energy, and biological catalysis. J Biol Chem 273: 26257-26260.
17. Schwartz S. D, Schramm V. L, (2009) Enzymatic transition states and dynamic motion in barrier crossing. Nat Chem Biol 5: 551-558.
18. Caratzoulas S, Mincer J. S, Schwartz S. D, (2002) Identification of a protein-promoting vibration in the reaction catalyzed by horse liver alcohol dehydrogenase. J Am Chem Soc 124: 3270-3276.
19. Smiley R. D, Hammes G. G, (2006) Single molecule studies of enzyme mechanisms. Chem Rev 106: 3080-3094.
20. Eisenmesser E. Z, Bosco D. A, Akke M, Kern D, (2002) Enzyme dynamics during catalysis. Science 295: 1520-1523.
21. Fraser J. S, Clarkson M. W, Degnan S. C, Erion R, Kern D, et al. (2009) Hidden alternative structures of proline isomerase essential for catalysis. Nature 462: 669-673.
22. Schnell J. R, Dyson H. J, Wright P. E, (2004) Effect of cofactor binding and loop conformation on side chain methyl dynamics in dihydrofolate reductase. Biochemistry 43: 374-383.
23. Boehr D. D, McElheny D, Dyson H. J, Wright P. E, (2006) The dynamic energy landscape of dihydrofolate reductase catalysis. Science 313: 1638-1642.
24. Antikainen N. M, Smiley R. D, Benkovic S. J, Hammes G. G, (2005) Conformation coupled enzyme catalysis: single-molecule and transient kinetics investigation of dihydrofolate reductase. Biochemistry 44: 16835-16843.
25. Agarwal P. K, Geist A, Gorin A, (2004) Protein dynamics and enzymatic catalysis: investigating the peptidyl-prolyl cis-trans isomerization activity of cyclophilin A. Biochemistry 43: 10605-10618.
26. Agarwal P. K, (2005) Role of protein dynamics in reaction rate enhancement by enzymes. J Am Chem Soc 127: 15248-15256.
27. Benkovic S. J, Hammes-Schiffer S, (2003) A perspective on enzyme catalysis. Science 301: 1196-1202.
28. Hammes G. G, Zhang Z. Q, Rajagopalan P. T, (2003) Conformational changes in enzyme catalysis: single-molecule and ensemble kinetics of dihydrofollate reductase. Biochemistry 42: 8651-8652.
29. Agarwal P. K, Billeter S. R, Hammes-Schiffer S, (2002) Nuclear quantum effects and enzyme dynamics in dihydrofolate reductase catalysis. J Phys Chem B 106: 3283-3293.
30. Rod T. H, Radkiewicz J. L, Brooks C. L 3rd, (2003) Correlated motion and the effect of distal mutations in dihydrofolate reductase. Proc Natl Acad Sci U S A 100: 6980-6985.
31. Tousignant A, Pelletier J. N, (2004) Protein motions promote catalysis. Chem & Biol 11: 1037-1042.
32. Garcia-Viloca M, Gao J, Karplus M, Truhlar D. G, (2004) How enzymes work: analysis by modern rate theory and computer simulations. Science 303: 186-195.
33. Pineda J. R, Antoniou D, Schwartz S. D, (2010) Slow conformational motions that favor sub-picosecond motions important for catalysis. J Phys Chem B 114: 15985-15990.
34. Wong K. F, Selzer T, Benkovic S. J, Hammes-Schiffer S, (2004) Impact of distal mutations on the network of coupled motions correlated to hydride transfer in dihydrofolate reductase. Proc Natl Acad Sci U S A 102: 6807-6812.
35. Boehr D. D, McElheny D, Dyson H. J, 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.
36. Eisenmesser E. Z, Millet O, Labeikovsky W, Korzhnev D. M, Wolf-Watz M, et al. (2005) Intrinsic dynamics of an enzyme underlies catalysis. Nature 438: 117-121.
37. Fenimore P. W, Frauenfelder H, McMahon B. H, Young R. D, (2004) Bulk-solvent and hydration-shell fluctuations, similar to alpha- and beta-fluctuations in glasses, control protein motions and functions. Proc Natl Acad Sci U S A 101: 14408-14413.
38. Warshel A, Sharma P. K, Chu Z. T, Aqvist J, (2007) Electrostatic contributions to binding of transition state analogues can be very different from the corresponding contributions to catalysis: phenolates binding to the oxyanion hole of ketosteroid isomerase. Biochemistry 46: 1466-1476.
39. Warshel A, Sharma P. K, Kato M, Xiang Y, Liu H. B, et al. (2006) Electrostatic basis for enzyme catalysis. Chem Rev 106: 3210-3235.
40. Bruice T. C, Benkovic S. J, (2000) Chemical basis for enzyme catalysis. Biochemistry 39: 6267-6274.
41. Gerlt J. A, Babbitt P. C, (2001) Divergent evolution of enzymatic function: mechanistically diverse superfamilies and functionally distinct suprafamilies. Annu Rev Biochem 70: 209-246.
42. Glasner M. E, Gerlt J. A, Babbitt P. C, (2006) Evolution of enzyme superfamilies. Curr Opin Chem Biol 10: 492-497.
43. Jencks W. P, (1975) Binding-energy, specificity, and enzymic catalysis- circe effect. Adv Enzymol Relat Areas Mol Biol 43: 219-410.
44. Kraut J, (1988) How do enzymes work. Science 242: 533-540.
45. Carnevale V, Raugei S, Micheletti C, Carloni P, (2006) Convergent dynamics in the protease enzymatic superfamily. J Am Chem Soc 128: 9766-9772.
46. Keskin O, Jernigan R. L, Bahar I, (2000) Proteins with similar architecture exhibit similar large-scale dynamic behavior. Biophys J 78: 2093-2106.
47. Maguid S, Fernandez-Alberti S, Echave J, (2008) Evolutionary conservation of protein vibrational dynamics. Gene 422: 7-13.
48. Zen A, Carnevale V, Lesk A. M, Micheletti C, (2008) Correspondences between low-energy modes in enzymes: dynamics-based alignment of enzymatic functional families. Protein Sci 17: 918-929.
49. Fanghanel J, Fischer G, (2004) Insights into the catalytic mechanism of peptidyl prolyl cis/trans isomerases. Front Biosci 9: 3453-3478.
50. Howard B. R, Vajdos F. F, Li S, Sundquist W. I, Hill C. P, (2003) Structural insights into the catalytic mechanism of cyclophilin A. Nat Struct Biol 10: 475-481.
51. Li G. H, Cui Q, (2003) What is so special about Arg 55 in the catalysis of cyclophilin A? Insights from hybrid QM/MM simulations. J Am Chem Soc 125: 15028-15038.
52. Hess B, (2000) Similarities between principal components of protein dynamics and random diffusion. Phys Rev E 62: 8438-8448.
53. Ranganathan R, Lu K. P, Hunter T, Noel J. P, (1997) Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent. Cell 89: 875-886.
54. Labeikovsky W, Eisenmesser E. Z, Bosco D. A, Kern D, (2007) Structure and dynamics of Pin1 during catalysis by NMR. J Mol Biol 367: 1370-1381.
55. Behrsin C. D, Bailey M. L, Bateman K. S, Hamilton K. S, Wahl L. M, et al. (2007) Functionally important residues in the peptidyl-prolyl isomerase Pin1 revealed by unigenic evolution. J Mol Biol 365: 1143-1162.
56. Sawaya M. R, Kraut J, (1997) Loop and subdomain movements in the mechanism of Escherichia coli dihydrofolate reductase: crystallographic evidence. Biochemistry 36: 586-603.
57. Garcia-Viloca M, Truhlar D. G, Gao J, (2003) Reaction-path energetics and kinetics of the hydride transfer reaction catalyzed by dihydrofolate reductase. Biochemistry 42: 13558-13575.
58. Wang L, Goodey N. M, Benkovic S. J, Kohen A, (2006) Coordinated effects of distal mutations on environmentally coupled tunneling in dihydrofolate reductase. Proc Natl Acad Sci U S A 103: 15753-15758.
59. Hammes G. G, (2002) Multiple conformational changes in enzyme catalysis. Biochemistry 41: 8221-8228.
60. Howell E. E, (2005) Searching sequence space: two different approaches to dihydrofolate reductase catalysis. ChemBioChem 6: 590-600.
61. Krahn J, Jackson M, DeRose E. F, Howell E. E, London R. E, (2007) Structure of a type ii dihydrofolate reductase ternary complex: use of identical binding sites for unrelated ligands. Biochemistry 46: 14878-14888.
62. Kamath G, Howell E. E, Agarwal P. K, (2010) The tail wagging the dog: insights into catalysis in R67 dihydrofolate reductase. Biochemistry 49: 9078-9088.
63. Almarsson O. B, Thomas C, (1993) Evaluation of the factors influencing reactivity and stereospecificity in NAD(P)H dependent dehydrogenase enzymes. J Am Chem Soc 115: 2125-2138.
64. Cole R, Loria J. P, (2002) Evidence for flexibility in the function of ribonuclease A. Biochemistry 41: 6072-6081.
65. Leonidas D. D, Shapiro R, Allen S. C, Subbarao G. V, Veluraja K, et al. (1999) Refined crystal structures of native human angiogenin and two active site variants: implications for the unique functional properties of an enzyme involved in neovascularisation during tumour growth. J Mol Biol 285: 1209-1233.
66. Formoso E, Matxain J. M, Lopez X, York D. M, (2010) Molecular dynamics simulation of bovine pancreatic ribonuclease A-CpA and transition state-like complexes. J Phys Chem B.
67. Kovrigin E. L, Loria J. P, (2006) Enzyme dynamics along the reaction coordinate: critical role of a conserved residue. Biochemistry 45: 2636-2647.
68. Lockless S. W, Ranganathan R, (1999) Evolutionarily conserved pathways of energetic connectivity in protein families. Science 286: 295-299.
69. Ramanathan A, Savol A. J, Langmead C. J, Agarwal P. K, Chennubhotla C. S, (2011) Discovering conformational sub-states relevant to protein function. PLoS ONE 6 (1): e15827.
70. Thorpe I. F, Brooks C. L, (2003) Barriers to hydride transfer in wild type and mutant dihydrofolate reductase from E-coli. J Phys Chem B 107: 14042-14051.
71. Hicks S. N, Smiley R. D, Stinnett L. G, Minor K. H, Howell E. E, (2004) Role of Lys-32 residues in R67 dihydrofolate reductase probed by asymmetric mutations. J Biol Chem 279: 46995-47002.
72. Lee J, Natarajan M, Nashine V. C, Socolich M, Vo T, et al. (2008) Surface sites for engineering allosteric control in proteins. Science 322: 438-442.
73. Wang L, Tharp S, Selzer T, Benkovic S. J, Kohen A, (2006) Effects of a distal mutation on active site chemistry. Biochemistry 45: 1383-1392.
74. Watt E. D, Shimada H, Kovrigin E. L, Loria J. P, (2007) The mechanism of rate-limiting motions in enzyme function. Proc Natl Acad Sci U S A 104: 11981-11986.
75. Sergi A, Watney J. B, Wong K. F, Hammes-Schiffer S, (2006) Freezing a single distal motion in dihydrofolate reductase. J Phys Chem B 110: 2435-2441.
76. Thorpe I. F, Brooks C. L, (2005) Conformational substates modulate hydride transfer in dihydrofolate reductase. J Am Chem Soc 127: 12997-13006.
77. Case D. A, Cheatham T. E 3rd, Darden T, Gohlke H, Luo R, et al. (2005) The Amber biomolecular simulation programs. J Comput Chem 26: 1668-1688.
78. Agarwal P. K, (2004) Cis/trans isomerization in HIV-1 capsid protein catalyzed by cyclophilin A: insights from computational and theoretical studies. Proteins: Struct Funct Bioinf 56: 449-463.
79. Warshel A, (1984) Dynamics of enzymatic-reactions. Proc Natl Acad Sci U S A 81: 444-448.
80. Warshel A, (1991) Computer modeling of chemical reactions in enzymes and solutions. New York Wiley-Interscience.
81. Levy R. M, Karplus M, Kushick J, Perahia D, (1984) Evaluation of the configurational entropy for proteins- application to molecular-dynamics simulations of an alpha-helix. Macromolecules 17: 1370-1374.
82. Ramanathan A, Agarwal P. K, Kurnikova M, Langmead C. J, (2010) An online approach for mining collective behaviors from molecular dynamics simulations. J Comput Biol 17: 309-324.
83. Ramanathan A, Agarwal P. K, (2009) Computational identification of slow conformational fluctuations in proteins. J Phys Chem B 113: 16669-16680.
84. Thompson J. D, Higgins D. G, Gibson T. J, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
85. PyMOL: The PyMOL Molecular Graphics System, version 1.0 (http://www.pymol.org/).
86. Lange O. F, Grubmuller H, de Groot B. L, (2005) Molecular dynamics simulations of protein G challenge NMR-derived correlated backbone motions. Angew Chem Int Ed Engl 44: 3394-3399.
87. Smith L. J, Daura X, van Gunsteren W. F, (2002) Assessing equilibration and convergence in biomolecular simulations. Proteins: Struct Funct Bioinf 48: 487-496.
88. Schnell J. R, Dyson H. J, Wright P. E, (2004) Effect of cofactor binding and loop conformation on side chain methyl dynamics in dihydrofolate reductase. Biochemistry 43: 374-383.