Further studies on the role of water in R67 dihydrofolate reductase

Biochemistry

Volumn 52, Issue 12, 2013, Pages 2118-2127

  Timson, Mary Jane ^a   Duff, Michael R ^a   Dickey, Greyson ^a   Saxton, Arnold M ^a   Reyes De Corcuera, José I ^b   Howell, Elizabeth E ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION VOLUME; COFACTOR BINDING; DIHYDROFOLATE REDUCTASE; FLUORESCENCE MEASUREMENTS; HIGH HYDROSTATIC PRESSURE; ISOTHERMAL TITRATION CALORIMETRY; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATES; R67 DIHYDROFOLATE REDUCTASE;

ENZYME ACTIVITY; HYDROSTATIC PRESSURE; OSMOSIS;

EXPERIMENTS;

DIHYDROFOLATE REDUCTASE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; WATER;

ARTICLE; ENZYME ACTIVITY; HYDROSTATIC PRESSURE; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; NUCLEAR MAGNETIC RESONANCE; OSMOTIC PRESSURE; OSMOTIC STRESS; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEOMICS;

BINDING SITES; DEUTERIUM EXCHANGE MEASUREMENT; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDROSTATIC PRESSURE; KINETICS; MODELS, MOLECULAR; NADP; OSMOTIC PRESSURE; PROTEIN STRUCTURE, QUATERNARY; SPECTROMETRY, FLUORESCENCE; SUBSTRATE SPECIFICITY; TETRAHYDROFOLATE DEHYDROGENASE; THERMODYNAMICS; WATER;

EID: 84875643738     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi301544k     Document Type: Article

References (69)

1. Whitesides, G. M. and Krishnamurthy, V. M. (2005) Designing ligands to bind proteins Q. Rev. Biophys. 38, 385-395
2. Munos, B. (2009) Lessons from 60 years of pharmaceutical innovation Nat. Rev. Drug Discovery 8, 959-968
3. Petsko, G. A. (2010) When failure should be the option BMC Biol. 8, 61-64
4. Silva, J. L., Foguel, D., and Royer, C. A. (2001) Pressure provides new insights into protein folding, dynamics and structure Trends Biochem. Sci. 26, 612-618
5. Northrop, D. B. (2006) Unusual origins of isotope effects in enzyme-catalysed reactions Philos. Trans. R. Soc., B 361, 1341-1349
6. Robinson, C. R. and Sligar, S. G. (1995) Hydrostatic and osmotic pressure as tools to study macromolecular recognition Methods Enzymol. 259, 395-427
7. Kornblatt, J. A. and Kornblatt, M. J. (2002) The effects of osmotic and hydrostatic pressures on macromolecular systems Biochim. Biophys. Acta 1595, 30-47
8. Kornblatt, J. A. and Kornblatt, M. J. (2002) Water as it applies to the function of enzymes Int. Rev. Cytol. 215, 49-73
9. Robinson, C. R. and Sligar, S. G. (1994) Hydrostatic pressure reverses osmotic pressure effects on the specificity of EcoRI-DNA interactions Biochemistry 33, 3787-3793
10. Chopra, S., Dooling, R., Horner, C. G., and Howell, E. E. (2008) A balancing act: Net uptake of water during dihydrofolate binding and net release of water upon NADPH binding in R67 dihydrofolate reductase J. Biol. Chem. 283, 4690-4698
11. Fried, M. G., Stickle, D. F., Smirnakis, K. V., Adams, C., MacDonald, D., and Lu, P. (2002) Role of hydration in the binding of lac repressor to DNA J. Biol. Chem. 277, 50676-50682
12. LiCata, V. J. and Allewell, N. M. (1997) Functionally linked hydration changes in Escherichia coli aspartate transcarbamylase and its catalytic subunit Biochemistry 36, 10161-10167
13. Reid, C. and Rand, R. P. (1997) Probing protein hydration and conformational states in solution Biophys. J. 72, 1022-1030
14. Grubbs, J., Rahmanian, S., Deluca, A., Padmashali, C., Jackson, M., Duff, M. R., and Howell, E. E. (2011) Thermodynamics and solvent effects on substrate and cofactor binding in Escherichia coli chromosomal dihydrofolate reductase Biochemistry 50, 3673-3685
15. Duff, M. R., Jr., Grubbs, J., Serpersu, E., and Howell, E. E. (2012) Weak interactions between folate and osmolytes in solution Biochemistry 51, 2309-2318
16. Chervenak, M. C. and Toone, E. J. (1994) A direct measure of the contribution of solvent reorganization to the enthalpy of binding J. Am. Chem. Soc. 116, 10533-10539
17. Krahn, J., Jackson, M., DeRose, E. F., Howell, E. E., and 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
18. Howell, E. E. (2005) Searching sequence space: Two different approaches to dihydrofolate reductase catalysis ChemBioChem 6, 590-600
19. 2 symmetric protein Biochemistry 35, 11414-11424
20. Strader, M. B., Chopra, S., Jackson, M., Smiley, R. D., Stinnett, L., Wu, J., and Howell, E. E. (2004) Defining the binding site of homotetrameric R67 dihydrofolate reductase and correlating binding enthalpy with catalysis Biochemistry 43, 7403-7412
21. Amyes, S. G. and Smith, J. T. (1976) The purification and properties of the trimethoprim-resistant dihydrofolate reductase mediated by the R-factor, R388 Eur. J. Biochem. 61, 597-603
22. Stone, D. and Smith, S. L. (1979) The amino acid sequence of the trimethoprim-resistant dihydrofolate reductase specified in Escherichia coli by R-plasmid R67 J. Biol. Chem. 254, 10857-10861
23. Narayana, N., Matthews, D. A., Howell, E. E., and Nguyen-huu, X. (1995) A plasmid-encoded dihydrofolate reductase from trimethoprim-resistant bacteria has a novel D2-symmetric active site Nat. Struct. Biol. 2, 1018-1025
24. Reece, L. J., Nichols, R., Ogden, R. C., and Howell, E. E. (1991) Construction of a synthetic gene for an R-plasmid-encoded dihydrofolate reductase and studies on the role of the N-terminus in the protein Biochemistry 30, 10895-10904
25. Eisenmenger, M. J. and Reyes-De-Corcuera, J. I. (2009) High hydrostatic pressure increased stability and activity of immobilized lipase in hexane Enzyme Microb. Technol. 45, 118-125
26. Quinlan, R. J. and Reinhart, G. D. (2005) Baroresistant buffer mixtures for biochemical analyses Anal. Biochem. 341, 69-76
27. Dunn, S. M., Lanigan, T. M., and Howell, E. E. (1990) Dihydrofolate reductase from Escherichia coli: Probing the role of aspartate-27 and phenylalanine-137 in enzyme conformation and the binding of NADPH Biochemistry 29, 8569-8576
28. Blakley, R. L. (1960) Crystalline dihydropteroylglutamic acid Nature 188, 231-232
29. Horecker, B. L. and Kornberg, A. (1948) The extinction coefficients of the reduced band of pyridine nucleotides J. Biol. Chem. 175, 385-390
30. Baccanari, D., Phillips, A., Smith, S., Sinski, D., and Burchall, J. (1975) Purification and properties of Escherichia coli dihydrofolate reductase Biochemistry 14, 5267-5273
31. Ohmae, E., Tatsuta, M., Abe, F., Kato, C., Tanaka, N., Kunugi, S., and Gekko, K. (2008) Effects of pressure on enzyme function in Esherichia coli dihydrofolate reductase Biochim. Biophys. Acta 1784, 1115-1121
32. Wiseman, T., Williston, S., Brandts, J. F., and Lin, L. N. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter Anal. Biochem. 179, 131-137
33. Hutchins, R. A., Crenshaw, J. M., Graves, D. E., and Denny, W. A. (2003) Influence of substituent modifications on DNA binding energetics of acridine-based anticancer agents Biochemistry 42, 13754-13761
34. Cook, P. (1991) Enzyme Mechanism from Isotope Effect, CRC Press, Boca Raton, FL.
35. Quinn, D. M. and Sutton, L. D. (2000) Theoretical basis and mechanistic utility of solvent isotope effects. In Enzyme Mechanism from Isotope Effects (Cook, P., Ed.) pp 73-126, CRC Press, Boca Raton, FL.
36. Houtman, J. C., Brown, P. H., Bowden, B., Yamaguchi, H., Appella, E., Samelson, L. E., and Schuck, P. (2007) Studying multisite binary and ternary protein interactions by global analysis of isothermal titration calorimetry data in SEDPHAT: Application to adaptor protein complexes in cell signaling Protein Sci. 16, 30-42
37. Herve, G., Tobe, S., Heams, T., Vergne, J., and Maurel, M. C. (2006) Hydrostatic and osmotic pressure study of the hairpin ribozyme Biochim. Biophys. Acta 1764, 573-577
38. Hay, S., Sutcliffe, M. J., and Scrutton, N. S. (2007) Promoting motions in enzyme catalysis probed by pressure studies of kinetic isotope effects Proc. Natl. Acad. Sci. U.S.A. 104, 507-512
39. Tobe, S., Heams, T., Vergne, J., Herve, G., and Maurel, M. C. (2005) The catalytic mechanism of hairpin ribozyme studied by hydrostatic pressure Nucleic Acids Res. 33, 2557-2564
40. Hicks, S. N., Smiley, R. D., Hamilton, J. B., and Howell, E. E. (2003) Role of ionic interactions in ligand binding and catalysis of R67 dihydrofolate reductase Biochemistry 42, 10569-10578
41. Lin, L. N., Brandts, J. F., Brandts, J. M., and Plotnikov, V. (2002) Determination of the volumetric properties of proteins and other solutes using pressure perturbation calorimetry Anal. Biochem. 302, 144-160
42. Cooper, A., Johnson, C. M., Lakey, J. H., and Nollmann, M. (2001) Heat does not come in different colours: Entropy-enthalpy compensation, free energy windows, quantum confinement, pressure perturbation calorimetry, solvation and the multiple causes of heat capacity effects in biomolecular interactions Biophys. Chem. 93, 215-230
43. Cameron, D. L., Jakus, J., Pauleta, S. R., Pettigrew, G. W., and Cooper, A. (2010) Pressure perturbation calorimetry and the thermodynamics of noncovalent interactions in water: Comparison of protein-protein, protein-ligand, and cyclodextrin-adamantane complexes J. Phys. Chem. B 114, 16228-16235
44. Marcus, Y. and Ben-Naim, A. (1985) A study of the structure of water and its dependence on solutes, based on the isotope effects on solvation thermodynamics in water J. Chem. Phys. 83, 4744-4759
45. Muller, N. (1991) Model-calculations of changes of thermodynamic variables for the transfer of nonpolar solutes from water to water-D2 J. Solution Chem. 20, 669-680
46. Nemethy, G. and Scheraga, H. A. (1964) Structure of water + hydrophobic bonding in proteins. 4. Thermodynamic properties of liquid deuterium oxide J. Chem. Phys. 41, 680-689
47. Ozen, C., Norris, A. L., Land, M. L., Tjioe, E., and Serpersu, E. H. (2008) Detection of specific solvent rearrangement regions of an enzyme: NMR and ITC studies with aminoglycoside phosphotransferase(3′)-IIIa Biochemistry 47, 40-49
48. Sobhany, M., Dong, J., and Negishi, M. (2005) Two-step mechanism that determines the donor binding specificity of human UDP-N- acetylhexosaminyltransferase J. Biol. Chem. 280, 23441-23445
49. Castillo, R., Andres, J., and Moliner, V. (1999) Catalytic mechanism of dihydrofolate reductase enzyme. A combined quantum-mechanical/molecular- mechanical characterizaton of transition state structure for the hydride transfer step J. Am. Chem. Soc. 121, 12140-12147
50. Li, D., Levy, L. A., Gabel, S. A., Lebetkin, M. S., DeRose, E. F., Wall, M. J., Howell, E. E., and London, R. E. (2001) Interligand Overhauser effects in type II dihydrofolate reductase Biochemistry 40, 4242-4252
51. Kamath, G., Howell, E. E., and Agarwal, P. K. (2010) The tail wagging the dog: Insights into catalysis in R67 dihydrofolate reductase Biochemistry 49, 9078-9088
52. Strader, M. B. (2003) Identifying the catalytic and ligand binding roles of active site residues in homotetrameric R67 dihydrofolate reductase. Ph.D. Thesis, University of Tennessee, Knoxville, TN.
53. Jackson, M., Chopra, S., Smiley, R. D., Maynord, P. O., Rosowsky, A., London, R. E., Levy, L., Kalman, T. I., and Howell, E. E. (2005) Calorimetric studies of ligand binding in R67 dihydrofolate reductase Biochemistry 44, 12420-12433
54. + complex reveals a novel cofactor binding mode Protein Sci. 16, 1063-1068
55. Feng, J., Goswami, S., and Howell, E. E. (2008) R67, the other dihydrofolate reductase: Rational design of an alternate active site configuration Biochemistry 47, 555-565
56. Chandler, D. (2005) Interfaces and the driving force of hydrophobic assembly Nature 437, 640-647
57. LeBard, D. N. and Matyushova, D. V. (2008) Redox entropy of plastocyanin: Developing a microscopic view of mesoscopic polar solvation J. Chem. Phys. 128, 155106-155116
58. Gilman-Politi, R. and Harries, D. (2011) Unraveling the Molecular Mechanism of Enthalpy Driven Peptide Folding by Polyol Osmolytes J. Chem. Theory Comput. 7, 3816-3828
59. Muller, N. (1990) Search for a realistic view of hydrophobic effects Acc. Chem. Res. 23, 23-28
60. Tanaka, H. (2000) General view of a liquid-liquid phase transition Phys. Rev. E: Stat. Phys., Plasmas, Fluids, Relat. Interdiscip. Top. 62, 6968-6976
61. Ball, P. (2008) Water: An enduring mystery Nature 452, 291-292
62. Ball, P. (2008) Water as an active constituent in cell biology Chem. Rev. 108, 74-108
63. Huang, C., Wikfeldt, K. T., Tokushima, T., Nordlund, D., Harada, Y., Bergmann, U., Niebuhr, M., Weiss, T. M., Horikawa, Y., Leetmaa, M., Ljungberg, M. P., Takahashi, O., Lenz, A., Ojamae, L., Lyubartsev, A. P., Shin, S., Pettersson, L. G., and Nilsson, A. (2009) The inhomogeneous structure of water at ambient conditions Proc. Natl. Acad. Sci. U.S.A. 106, 15214-15218
64. Mallamace, F. (2009) The liquid water polymorphism Proc. Natl. Acad. Sci. U.S.A. 106, 15097-15098
65. Major, R. C., Houston, J. E., McGrath, M. J., Siepmann, J. I., and Zhu, X.-Y. (2006) Viscous Water Meniscus under Nanoconfinement Phys. Rev. Lett. 96, 177803
66. Li, T.-D., Gao, J., Szoszkiewicz, R., Landman, U., and Riedo, E. (2007) Structured and viscous water in sub-nanometer gaps Phys. Rev. B 75, 115415
67. Ball, P. (2008) Water as a biomolecule ChemPhysChem 9, 2677-2685
68. Baron, R., Setny, P., and McCammon, J. A. (2010) Water in cavity-ligand recognition J. Am. Chem. Soc. 132, 12091-12097
69. Biela, A., Nasief, N. N., Betz, M., Heine, A., Hangauer, D., and Klebe, G. (2013) Dissecting the hydrophobic effect on the molecular level: The role of water, enthalpy, and entropy in ligand binding to thermolysin Angew. Chem., Int. Ed. 52, 1822-1828