Thermodynamics and solvent effects on substrate and cofactor binding in escherichia coli chromosomal dihydrofolate reductase

Biochemistry

Volumn 50, Issue 18, 2011, Pages 3673-3685

  Grubbs, Jordan ^a   Rahmanian, Sharghi ^a   Deluca, Alexa ^a   Padmashali, Chetan ^a   Jackson, Michael ^a   Duff, Michael R ^a   Howell, Elizabeth E ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; COFACTOR BINDING; COFACTORS; CONFORMATIONAL TRANSITIONS; COSOLVENT EFFECTS; DIFFERENT EFFECTS; DIHYDROFOLATE; DIHYDROFOLATE REDUCTASE; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; NON-ADDITIVE; OSMOLYTES; PROTON RELEASE; R67 DIHYDROFOLATE REDUCTASE; ROLE OF WATER; SOLVENT EFFECTS; STOPPED FLOW EXPERIMENTS; TETRAHYDROFOLATES; TETRAMERIC STRUCTURES; THERMODYNAMIC CYCLE; TYPE II; WATER MOLECULE; WATER UPTAKE;

CHROMOSOMES; ESCHERICHIA COLI; PROTONS; THERMODYNAMIC PROPERTIES;

ENZYMES;

APOENZYME; DIHYDROFOLATE REDUCTASE; FOLIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SOLVENT;

ARTICLE; BACTERIAL CHROMOSOME; ENTHALPY; ENZYME CONFORMATION; ESCHERICHIA COLI; IONIZATION; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTON TRANSPORT; THERMODYNAMICS; WATER TRANSPORT;

BINDING SITES; CALORIMETRY; CHROMOSOMES; ESCHERICHIA COLI; KINETICS; LIGANDS; NADP; PROTEIN BINDING; PROTEIN CONFORMATION; SOLVENTS; TETRAHYDROFOLATE DEHYDROGENASE; THERMODYNAMICS; WATER;

ESCHERICHIA COLI;

EID: 79955586889     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi2002373     Document Type: Article

References (102)

1. 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 (Pubitemid 38829954)
2. Rajagopalan, P. T. and Benkovic, S. J. (2002) Preorganization and protein dynamics in enzyme catalysis Chem. Rec. 2, 24-36 (Pubitemid 44127757)
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 (Pubitemid 27057006)
4. Subramanian, S. and Kaufman, B. T. (1978) Interaction of methotrexate, folates, and pyridine nucleotides with dihydrofolate reductase: Calorimetric and spectroscopic binding studies Proc. Natl. Acad. Sci. U.S.A. 75, 3201-3205 (Pubitemid 8395147)
5. Gilli, R. M., Sari, J. C., Sica, L. M., and Briand, C. M. (1988) Thermodynamic study of the influence of NADPH on the binding of methotrexate and its metabolites to a mammalian dihydrofolate reductase Biochim. Biophys. Acta 964, 53-60 (Pubitemid 18020739)
6. Sica, L., Gilli, R., Briand, C., and Sari, J. C. (1987) A flow microcalorimetric method for enzyme activity measurements: Application to dihydrofolate reductase Anal. Biochem. 165, 341-348
7. Todd, M. J. and Gomez, J. (2001) Enzyme kinetics determined using calorimetry: A general assay for enzyme activity? Anal. Biochem. 296, 179-187 (Pubitemid 32868499)
8. 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
9. Bolin, J., Filman, D., Matthews, D., Hamlin, R., and Kraut, J. (1982) Crystal structures of Escherichia coli and Lactobacillus casei dihydrofolate reductase refined at 1.7 Å resolution. I. General features and binding of methotrexate J. Biol. Chem. 257, 13650
10. 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
11. 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 (Pubitemid 44414038)
12. 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
13. Venkitakrishnan, R. P., Zaborowski, E., McElheny, D., Benkovic, S. J., Dyson, H. J., and Wright, P. E. (2004) Conformational changes in the active site loops of dihydrofolate reductase during the catalytic cycle Biochemistry 43, 16046-16055 (Pubitemid 40041018)
14. 2 symmetric protein Biochemistry 35, 11414-11424 (Pubitemid 26299316)
15. Park, H., Bradrick, T. D., and Howell, E. E. (1997) A glutamine 67 to histidine mutation in homotetrameric R67 dihydrofolate reductase results in four mutations per single active site pore and causes substantial substrate and cofactor inhibition Protein Eng., Des. Sel. 10, 1415-1424 (Pubitemid 28116181)
16. Pitcher, W. H., III, DeRose, E. F., Mueller, G. A., Howell, E. E., and London, R. E. (2003) NMR studies of the interaction of a type II dihydrofolate reductase with pyridine nucleotides reveal unexpected phosphatase and reductase activity Biochemistry 42, 11150-11160 (Pubitemid 37158882)
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 (Pubitemid 350308879)
18. 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
19. Howell, E. E. (2005) Searching sequence space: Two different approaches to dihydrofolate reductase catalysis ChemBioChem 6, 590-600 (Pubitemid 40873755)
20. Fierke, C. A., Kuchta, R. D., Johnson, K. A., and Benkovic, S. J. (1987) Implications for enzymic catalysis from free-energy reaction coordinate profiles Cold Spring Harbor Symp. Quant. Biol. 52, 631-638 (Pubitemid 18262375)
21. Alonso, H. and Gready, J. E. (2006) Integron-sequestered dihydrofolate reductase: A recently redeployed enzyme Trends Microbiol. 14, 236-242 (Pubitemid 44255607)
22. Yahashiri, A., Howell, E. E., and Kohen, A. (2008) Tuning of the H-Transfer Coordinate in Primitive versus Well-Evolved Enzymes ChemPhysChem 9, 980-982
23. 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 (Pubitemid 36042229)
24. Arakawa, T. and Timasheff, S. N. (1985) The stabilization of proteins by osmolytes Biophys. J. 47, 411-414
25. Timasheff, S. N. (1993) The control of protein stability and association by weak interactions with water: How do solvents affect these processes? Annu. Rev. Biophys. Biomol. Struct. 22, 67-97 (Pubitemid 23180317)
26. Street, T. O., Bolen, D. W., and Rose, G. D. (2006) A molecular mechanism for osmolyte-induced protein stability Proc. Natl. Acad. Sci. U.S.A. 103, 13997-14002 (Pubitemid 44488414)
27. Reid, C. and Rand, R. P. (1997) Probing protein hydration and conformational states in solution Biophys. J. 72, 1022-1030 (Pubitemid 27113630)
28. 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 (Pubitemid 27357726)
29. Flensburg, J. and Skold, O. (1987) Massive overproduction of dihydrofolate reductase in bacteria as a response to the use of trimethoprim Eur. J. Biochem. 162, 473-476 (Pubitemid 17023099)
30. Baccanari, D. P., Stone, D., and Kuyper, L. (1981) Effect of a single amino acid substitution on Escherichia coli dihydrofolate reductase catalysis and ligand binding J. Biol. Chem. 256, 1738-1747 (Pubitemid 11100048)
31. Ellis, K. J. and Morrison, J. F. (1982) Buffers of constant ionic strength for studying pH-dependent processes Methods Enzymol. 87, 405-426
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 (Pubitemid 19149635)
33. 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 (Pubitemid 46036496)
34. Fukada, H. and Takahashi, K. (1998) Enthalpy and heat capacity changes for the proton dissociation of various buffer components in 0.1 M potassium chloride Proteins 33, 159-166 (Pubitemid 28457970)
35. + reductase and the role of water at the complex interface Biochemistry 33, 13321-13328 (Pubitemid 24373247)
36. Sweeney, T. E. and Beuchat, C. A. (1993) Limitations of methods of osmometry: Measuring the osmolality of biological fluids Am. J. Physiol. 264, R469-R480
37. Wyman, J., Jr. (1964) Linked functions and reciprocal effects in hemoglobin: A second look Adv. Protein Chem. 19, 223-286
38. Fierke, C. A., Johnson, K. A., and Benkovic, S. J. (1987) Construction and evaluation of the kinetic scheme associated with dihydrofolate reductase from Escherichia coli Biochemistry 26, 4085-4092
39. Maharaj, G., Selinsky, B. S., Appleman, J. R., Perlman, M., London, R. E., and Blakley, R. L. (1990) Dissociation constants for dihydrofolic acid and dihydrobiopterin and implications for mechanistic models for dihydrofolate reductase Biochemistry 29, 4554-4560 (Pubitemid 20172670)
40. Cayley, P. J., Dunn, S. M., and King, R. W. (1981) Kinetics of substrate, coenzyme, and inhibitor binding to Escherichia coli dihydrofolate reductase Biochemistry 20, 874-879 (Pubitemid 11097550)
41. Fersht, A. (1999) Structure and Mechanism in Protein Science, W. H. Freeman and Co., New York.
42. Posner, B. A., Li, L., Bethell, R., Tsuji, T., and Benkovic, S. J. (1996) Engineering specificity for folate into dihydrofolate reductase from Escherichia coli Biochemistry 35, 1653-1663 (Pubitemid 26055300)
43. a of N5 of dihydrofolate bound to dihydrofolate reductase: Mechanistic implications Biochemistry 33, 7021-7026 (Pubitemid 24208735)
44. Deng, H. and Callender, R. (1998) Structure of dihydrofolate when bound to DHFR J. Am. Chem. Soc. 120, 7730-7737 (Pubitemid 28392054)
45. Cannon, W., Garrison, B., and Benkovic, S. (1997) Electrostatic characterization of enzyme complexes: Evaluation of the mechanism of catalysis of dihydrofolate reductase J. Am. Chem. Soc. 119, 2386-2395 (Pubitemid 27167855)
46. Rod, T. H. and Brooks, C. L., III (2003) How dihydrofolate reductase facilitates protonation of dihydrofolate J. Am. Chem. Soc. 125, 8718-8719 (Pubitemid 36886197)
47. Ferrer, S., Silla, E., Tunon, I., Marti, S., and Moliner, V. (2003) Catalytic mechanism of dihydrofolate reductase enzyme. A combined quantum mechanical/molecular-mechanical characterization of the N5 protonation step J. Phys. Chem. B 107, 14036-14041
48. Shrimpton, P. and Allemann, R. K. (2002) Role of water in the catalytic cycle of E. coli dihydrofolate reductase Protein Sci. 11, 1442-1451 (Pubitemid 34547216)
49. Chen, Y. Q., Kraut, J., and Callender, R. (1997) pH-dependent conformational changes in Escherichia coli dihydrofolate reductase revealed by Raman difference spectroscopy Biophys. J. 72, 936-941 (Pubitemid 27044897)
50. Cummins, P. L. and Gready, J. E. (2001) Energetically most likely substrate and active-site protonation sites and pathways in the catalytic mechanism of dihydrofolate reductase J. Am. Chem. Soc. 123, 3418-3428 (Pubitemid 32884575)
51. + binding to L. casei dihydrofolate reductase Nature 257, 564-566
52. Parsegian, V. A., Rand, R. P., and Rau, D. C. (1995) Macromolecules and water: Probing with osmotic stress Methods Enzymol. 259, 43-94
53. LiCata, V. J. and Allewell, N. M. (1998) Measuring hydration changes of proteins in solution: Applications of osmotic stress and structure-based calculations Methods Enzymol. 295, 42-62 (Pubitemid 29349908)
54. Robinson, C. R. and Sligar, S. G. (1995) Hydrostatic and osmotic pressure as tools to study macromolecular recognition Methods Enzymol. 259, 395-427
55. Kornblatt, J. A. and Kornblatt, M. J. (2002) The effects of osmotic and hydrostatic pressures on macromolecular systems Biochim. Biophys. Acta 1595, 30-47 (Pubitemid 34442634)
56. Edsall, J. (1943) Dielectric constants and dipole moments of dipolar ions. In Proteins, Amino Acids and Peptides as Ions and Dipolar Ions (Cohn, E. and Edsall, J., Eds.) pp 140-154, Reinhold, New York.
57. Kiser, J. R., Monk, R. W., Smalls, R. L., and Petty, J. T. (2005) Hydration changes in the association of Hoechst 33258 with DNA Biochemistry 44, 16988-16997 (Pubitemid 43007227)
58. Timasheff, S. N. (2002) Protein-solvent preferential interactions, protein hydration, and the modulation of biochemical reactions by solvent components Proc. Natl. Acad. Sci. U.S.A. 99, 9721-9726 (Pubitemid 34831114)
59. Parsegian, V. A., Rand, R. P., and Rau, D. C. (2000) Osmotic stress, crowding, preferential hydration, and binding: A comparison of perspectives Proc. Natl. Acad. Sci. U.S.A. 97, 3987-3992 (Pubitemid 30226074)
60. Vossen, K. M., Wolz, R., Daugherty, M. A., and Fried, M. G. (1997) Role of macromolecular hydration in the binding of the Escherichia coli cyclic AMP receptor to DNA Biochemistry 36, 11640-11647 (Pubitemid 27424088)
61. Sidorova, N. Y., Muradymov, S., and Rau, D. C. (2006) Differences in hydration coupled to specific and nonspecific competitive binding and to specific DNA binding of the restriction endonuclease BamHI J. Biol. Chem. 281, 35656-35666 (Pubitemid 46041296)
62. Courtenay, E. S., Capp, M. W., Anderson, C. F., and Record, M. T., Jr. (2000) Vapor pressure osmometry studies of osmolyte-protein interactions: Implications for the action of osmoprotectants in vivo and for the interpretation of "osmotic stress" experiments in vitro Biochemistry 39, 4455-4471 (Pubitemid 30212662)
63. Schellman, J. A. (2003) Protein stability in mixed solvents: A balance of contact interaction and excluded volume Biophys. J. 85, 108-125 (Pubitemid 36753621)
64. Schurr, J. M., Rangel, D. P., and Aragon, S. R. (2005) A contribution to the theory of preferential interaction coefficients Biophys. J. 89, 2258-2276 (Pubitemid 41401018)
65. Minton, A. P. (1981) Excluded volume as a determinant of macromolecular structure and reactivity Biopolymers 20, 2093-2120
66. Garner, M. M. and Rau, D. C. (1995) Water release associated with specific binding of gal repressor EMBO J. 14, 1257-1263
67. Sidorova, N. and Rau, D. C. (2004) The role of water in the EcoRI-DNA binding Nucleic Acids Mol. Biol. 14, 319-337
68. Hultgren, A. and Rau, D. C. (2004) Exclusion of alcohols from spermidine-DNA assemblies: Probing the physical basis of preferential hydration Biochemistry 43, 8272-8280 (Pubitemid 38808283)
69. Davis-Searles, P. R., Morar, A. S., Saunders, A. J., Erie, D. A., and Pielak, G. J. (1998) Sugar-induced molten-globule model Biochemistry 37, 17048-17053 (Pubitemid 28566784)
70. Saunders, A. J., Davis-Searles, P. R., Allen, D. L., Pielak, G. J., and Erie, D. A. (2000) Osmolyte-induced changes in protein conformational equilibria Biopolymers 53, 293-307 (Pubitemid 30230020)
71. Gulotta, M., Qiu, L., Desamero, R., Rosgen, J., Bolen, D. W., and Callender, R. (2007) Effects of cell volume regulating osmolytes on glycerol 3-phosphate binding to triosephosphate isomerase Biochemistry 46, 10055-10062 (Pubitemid 47378597)
72. Auton, M. and Bolen, D. W. (2005) Predicting the energetics of osmolyte-induced protein folding/unfolding Proc. Natl. Acad. Sci. U.S.A. 102, 15065-15068 (Pubitemid 41513335)
73. Chik, J., Mizrahi, S., Chi, S., Parsegian, V. A., and Rau, D. C. (2005) Hydration forces underlie the exclusion of salts and of neutral polar solutes from hydroxypropylcellulose J. Phys. Chem. B 109, 9111-9118 (Pubitemid 40750948)
74. Stanley, C. and Rau, D. C. (2006) Preferential hydration of DNA: The magnitude and distance dependence of alcohol and polyol interactions Biophys. J. 91, 912-920 (Pubitemid 44161923)
75. Chervenak, M. C. T. and Eric, J. (1994) A direct measure of the contribution of solvent reorganization to the enthalpy of binding J. Am. Chem. Soc. 116, 10533-10539
76. Dunitz, J. D. (1995) Win some, lose some: Enthalpy-entropy compensation in weak intermolecular interactions Chem. Biol. 2, 709-712
77. Frisch, C., Schreiber, G., Johnson, C. M., and Fersht, A. R. (1997) Thermodynamics of the interaction of barnase and barstar: Changes in free energy versus changes in enthalpy on mutation J. Mol. Biol. 267, 696-706 (Pubitemid 27170691)
78. Harries, D., Rau, D. C., and Parsegian, V. A. (2005) Solutes probe hydration in specific association of cyclodextrin and adamantane J. Am. Chem. Soc. 127, 2184-2190 (Pubitemid 40270522)
79. 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 (Pubitemid 20302746)
80. Appleman, J. R., Howell, E. E., Kraut, J., and Blakley, R. L. (1990) Role of aspartate 27 of dihydrofolate reductase from Escherichia coli in interconversion of active and inactive enzyme conformers and binding of NADPH J. Biol. Chem. 265, 5579-5584
81. Adams, J., Johnson, K. A., Matthews, C. R., and Benkovic, S. J. (1989) Effects of distal point-site mutations on the binding and catalysis of dihydrofolate reductase from Escherichia coli Biochemistry 28, 6611-6618 (Pubitemid 19208310)
82. Loveridge, E. J., Tey, L. H., and Allemann, R. K. (2010) Solvent effects on catalysis by Escherichia coli dihydrofolate reductase J. Am. Chem. Soc. 132, 1137-1143
83. 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 (Pubitemid 41324334)
84. Ortiz-Salmeron, E., Yassin, Z., Clemente-Jimenez, M. J., Las Heras-Vazquez, F. J., Rodriguez-Vico, F., Baron, C., and Garcia-Fuentes, L. (2001) Thermodynamic analysis of the binding of glutathione to glutathione S-transferase over a range of temperatures Eur. J. Biochem. 268, 4307-4314 (Pubitemid 32862892)
85. Miyagi, M., Wan, Q., Ahmad, M. F., Gokulrangan, G., Tomechko, S. E., Bennett, B., and Dealwis, C. (2011) Histidine hydrogen-deuterium exchange mass spectrometry for probing the microenvironment of histidine residues in dihydrofolate reductase PLoS One 6, e17055
86. Appleman, J. R., Howell, E. E., Kraut, J., Kuhl, M., and Blakley, R. L. (1988) Role of aspartate 27 in the binding of methotrexate to dihydrofolate reductase from Escherichia coli J. Biol. Chem. 263, 9187-9198
87. Boehr, D. D., Dyson, H. J., and Wright, P. E. (2006) An NMR perspective on enzyme dynamics Chem. Rev. 106, 3055-3079 (Pubitemid 44376926)
88. Boehr, D. D., Dyson, H. J., and Wright, P. E. (2008) Conformational relaxation following hydride transfer plays a limiting role in dihydrofolate reductase catalysis Biochemistry 47, 9227-9233
89. Heaslet, H., Harris, M., Fahnoe, K., Sarver, R., Putz, H., Chang, J., Subramanyam, C., Barreiro, G., and Miller, J. R. (2009) Structural comparison of chromosomal and exogenous dihydrofolate reductase from Staphylococcus aureus in complex with the potent inhibitor trimethoprim Proteins 76, 706-717
90. Cody, V., Pace, J., and Rosowsky, A. (2008) 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. D64, 977-984
91. Dzingeleski, G. D. and Wolfenden, R. (1993) Hypersensitivity of an enzyme reaction to solvent water Biochemistry 32, 9143-9147 (Pubitemid 24186236)
92. Furukawa, Y. and Morishima, I. (2001) The role of water molecules in the association of cytochrome P450cam with putidaredoxin. An osmotic pressure study J. Biol. Chem. 276, 12983-12990
93. Xavier, K. A., Shick, K. A., Smith-Gil, S. J., and Willson, R. C. (1997) Involvement of water molecules in the association of monoclonal antibody HyHEL-5 with bobwhite quail lysozyme Biophys. J. 73, 2116-2125 (Pubitemid 27425742)
94. Poe, M. (1973) Proton magnetic resonance studies of folate, dihydrofolate, and methotrexate. Evidence from pH and concentration studies for dimerization J. Biol. Chem. 248, 7025-7032
95. Carlson, J. C., Kanter, A., Thuduppathy, G. R., Cody, V., Pineda, P. E., McIvor, R. S., and Wagner, C. R. (2003) Designing protein dimerizers: The importance of ligand conformational equilibria J. Am. Chem. Soc. 125, 1501-1507 (Pubitemid 36206230)
96. Lu, W., Kwon, Y. K., and Rabinowitz, J. D. (2007) Isotope ratio-based profiling of microbial folates J. Am. Soc. Mass Spectrom. 18, 898-909 (Pubitemid 46617285)
97. Fernandes-Costa, F. and Metz, J. (1979) Role of serum folate binders in the delivery of folate to tissues and to the fetus Br. J. Haematol. 41, 335-342 (Pubitemid 9109597)
98. De Wit, R. and Bulgakov, R. (1985) Guanine nucleotides modulate the ligand binding properties of cell surface folate receptors in Dictyostelium discoideum FEBS Lett. 179, 257-261
99. Corrocher, R., De Sandre, G., Ambrosetti, A., Pachor, M. L., Bambara, L. M., and Hoffbrand, A. V. (1978) Specific and non-specific folate binding protein in normal and malignant human tissues J. Clin. Pathol. 31, 659-665 (Pubitemid 8379772)
100. Arnone, A., Rogers, P. H., Benesch, R. E., Benesch, R., and Kwong, S. (1986) The interaction of folylpolyglutamates with deoxyhemoglobin. Identification of the binding site J. Biol. Chem. 261, 5853-5857
101. Capp, M. W., Pegram, L. M., Saecker, R. M., Kratz, M., Riccardi, D., Wendorff, T., Cannon, J. G., and Record, M. T., Jr. (2009) Interactions of the osmolyte glycine betaine with molecular surfaces in water: Thermodynamics, structural interpretation, and prediction of m-values Biochemistry 48, 10372-10379
102. Norris, A. L. and Serpersu, E. (2010) Interactions of coenzyme A with the aminoglycoside acetyltransferase (3)-IIIb and thermodynamics of a ternary system Biochemistry 49, 4036-4042