The thermodynamics of protein-protein recognition as characterized by a combination of volumetric and calorimetric techniques: The binding of Turkey ovomucoid third domain to α-chymotrypsin

Journal of Molecular Biology

Volumn 326, Issue 4, 2003, Pages 1271-1288

  Filfil, Rana ^a   Chalikian, Tigran V ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Hydration; Protein protein recognition; Thermodynamics; Turkey ovomucoid third domain; chymotrypsin

Indexed keywords

CHYMOTRYPSIN A; OVOMUCOID;

ARTICLE; BINDING AFFINITY; CALORIMETRY; DATA ANALYSIS; ENTHALPY; ENTROPY; HYDRATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; TEMPERATURE DEPENDENCE; THERMODYNAMICS; VOLUMETRY; X RAY CRYSTALLOGRAPHY;

EID: 0037470558     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00022-6     Document Type: Article

References (81)

1. Laskowski M. Jr, Kato I. Protein inhibitors of proteinases. Annu. Rev. Biochem. 49:1980;593-626.
2. Laskowski M. Jr., Tashiro M., Empie M.W., Park S.J., Kato I., Ardelt W., Wieczorek M. Relationship between the amino acid sequence and inhibitory activity of protein inhibitors of proteinases. Katunuma N., Umezawa H., Holzer H. Proteinase Inhibitors: Medical and Biological Aspects. 1983;55-68 Japan Sci. Soc. Press/Springer, Tokyo/Berlin.
3. Read R.J., James M.N.G. Introduction to the protein inhibitors: X-ray crystallography. Barett A.J., Salvesen G. Proteinase Inhibitors. 1986;301-336 Elsevier Science Publishers BV, Amsterdam.
4. Bode W., Huber R. Proteinase-protein inhibitor interaction. Biomed. Biochim. Acta. 50:1991;437-446.
5. Hubbard S.J., Campbell S.F., Thornton J.M. Molecular recognition, conformational analysis of limited proteolytic sites and serine protease protein inhibitors. J. Mol. Biol. 220:1991;507-530.
6. Murphy K.P., Baker B.M., Edgcomb S.P., Horn J.R. Structural energetics of serine protease inhibition. Pure Appl. Chem. 71:1999;1207-1213.
7. Laskowski M. Jr, Qasim M.A. What can the structures of enzyme-inhibitor complexes tell us about the structures of enzyme substrate complexes? Biochim. Biophys. Acta. 1477:2000;324-337.
8. Laskowski M. Jr, Kato I., Ardelt W., Cook J., Denton A., Empie M.W., et al. Ovomucoid third domains from 100 avian species: isolation, sequences, and hypervariability of enzyme-inhibitor contact residues. Biochemistry. 26:1987;202-221.
9. Bode W., Epp O., Huber R., Laskowski M. Jr, Ardelt W. The crystal and molecular structure of the third domain of silver pheasant ovomucoid (OMSVP3). Eur. J. Biochem. 147:1985;387-395.
10. Krezel A.M., Darba P., Robertson A.D., Fejzo J., Macura S., Markley J.L. Solution structure of turkey ovomucoid third domain as determined from nuclear magnetic resonance data. J. Mol. Biol. 242:1994;203-214.
11. Hoogstraten C.G., Choe S., Westler W.M., Markley J.L. Comparison of the accuracy of protein solution structures derived from conventional and network-edited NOESY data. Protein Sci. 4:1995;2289-2299.
12. Read R.J., Fujinaga M., Sielecki A.R., James M.N. Structure of the complex of Streptomyces griseus protease B and the third domain of the turkey ovomucoid inhibitor at 1.8 Å resolution. Biochemistry. 22:1983;4420-4433.
13. Bode W., Wei A.Z., Huber R., Meyer E., Travis J., Neumann S. X-ray crystal structure of the complex of human leukocyte elastase (Pmn elastase) and the third domain of the turkey ovomucoid inhibitor. EMBO J. 5:1986;2453-2458.
14. Fujinaga M., Sielecki A.R., Read R.J., Ardelt W., Laskowski M. Jr, James M.N.G. Crystal and molecular structures of the complex of α-chymotrypsin with inhibitor turkey ovomucoid third domain at 1.8 Å resolution. J. Mol. Biol. 195:1987;397-418.
15. Baker B.M., Murphy K.P. Dissecting the energetics of a protein-protein interaction: the binding of ovomucoid third domain to elastase. J. Mol. Biol. 268:1997;557-569.
16. Schwert G.W. The molecular size and shape of the pancreatic proteases. 1. Sedimentation studies on chymotrypsinogen and on α- and γ-chymotrypsin. J. Biol. Chem. 179:1949;655-664.
17. Timasheff S.N. On the mechanism of α-chymotrypsin dimerization. Arch. Biochem. Biophys. 132:1969;165-169.
18. Shiao D.D.F., Sturtevant J.M. Calorimetric investigations of the binding of inhibitors to α-chymotrypsin. 1. The enthalpy of dilution of α-chymotrypsin and of proflavin, and the enthalpy of binding of indole, N-acetyl-D-tryptophan, and proflavin to α-chymotrypsin. Biochemistry. 8:1969;4910-4917.
19. Tsukada H., Blow D.M. Structure of α-chymotrypsin refined at 1.68 Å resolution. J. Mol. Biol. 184:1985;703-711.
20. Shearwin K.E., Winzor D.J. Effect of sucrose on the dimerization of α-chymotrypsin. Allowance for thermodynamic nonideality arising from the presence of a small inert solute. Biophys. Chem. 31:1988;287-294.
21. Patel C.N., Noble S.M., Weatherly G.T., Tripathy A., Winzor D.J., Pielak G.J. Effect of molecular crowding by saccharides on α-chymotrypsin dimerization. Protein Sci. 11:2002;997-1003.
22. Breslauer K.J. Extracting thermodynamic data from equilibrium melting curves for oligonucleotide order-disorder transitions. Agrawal S. Methods in Molecular Biology. vol. 26:1994;347-372 Humana Press, Totowa, NJ.
23. Crothers D.M. Statistical thermodynamics of nucleic acid melting transitions with coupled binding equilibria. Biopolymers. 10:1971;2147-2160.
24. Privalov P.L., Khechinashvili N.N. Thermodynamic approach to problem of stabilization of globular protein structure - calorimetric study. J. Mol. Biol. 86:1974;665-684.
25. Brandts J.F., Lin L.-N. Study of strong to ultratight protein interactions using differential scanning calorimetry. Biochemistry. 29:1990;6927-6940.
26. Privalov G.P., Privalov P.L. Problems and prospects in microcalorimetry of biological macromolecules. Methods Enzymol. 323:2000;31-62.
27. Gekko K., Noguchi H. Compressibility of globular proteins in water at 25°C. J. Phys. Chem. 83:1979;2706-2714.
28. Gekko K., Hasegawa Y. Compressibility-structure relationship of globular proteins. Biochemistry. 25:1986;6563-6571.
29. Chalikian T.V., Sarvazyan A.P., Breslauer T.V. Hydration and partial compressibility of biological compounds. Biophys. Chem. 51:1994;89-109.
30. Chalikian T.V., Totrov M., Abagyan R., Breslauer K.J. The hydration of globular proteins as derived from volume and compressibility: cross correlating thermodynamic and structural data. J. Mol. Biol. 260:1996;588-603.
31. Lakowicz J.R. Principles of Fluorescence Spectroscopy. 2nd edit. 1999;Kluwer Academic/Plenum Publishers, New York.
32. Baker B.M., Murphy K.P. Evaluation of linked protonation effects in protein binding reactions using isothermal titration calorimetry. Biophys. J. 71:1996;2049-2055.
33. Fukada H., Takahashi K. Enthalpy and heat capacity changes for the proton dissociation of various buffer components in 0.1 M potassium chloride. Proteins: Struct. Funct. Genet. 33:1998;159-166.
34. Frisch C., Schreiber G., Johnson C.M., Fersht A.R. Thermodynamics of the interaction of barnase and barstar: changes in free energy versus changes in enthalpy on mutation. J. Mol. Biol. 267:1997;696-706.
35. Pierce M.N., Raman C.S., Nall B.T. Isothermal titration calorimetry of protein-protein interactions. Methods. 19:1999;213-221.
36. Spolar R.S., Record M.T. Jr. Coupling of local folding to site-specific binding of proteins to DNA. Science. 263:1994;777-784.
37. Luque I., Freire E. Structure-based prediction of binding affinities and molecular design of peptide ligands. Methods Enzymol. 295:1998;100-127.
38. Lazaridis T., Karplus M. Heat capacity and compactness of denatured proteins. Biophys. Chem. 78:1999;207-217.
39. Cooper A. Heat capacity of hydrogen-bonded networks: an alternative view of protein folding thermodynamics. Biophys. Chem. 85:2000;25-39.
40. Empie M.W., Laskowski M. Jr. Thermodynamics and kinetics of single residue replacements in avian ovomucoid third domains: effect on inhibitor interactions with serine proteases. Biochemistry. 21:1982;2274-2284.
41. Høiland H. Pressure dependence of the volumes of ionization of carboxylic acids at 25, 35, and 45°C and 1-1200 bar. J. Chem. Soc. Faraday Trans. 1. 70:1974;1180-1185.
42. Chalikian T.V., Breslauer K.J. On volume changes accompanying conformational transitions of biopolymers. Biopolymers. 39:1996;619-626.
43. Dubins D.N., Filfil R., Macgregor R.B. Jr, Chalikian T.V. The role of water in protein-ligand interactions: volumetric characterizations of the binding of 2′-CMP and 3′-CMP to ribonuclease A. J. Phys. Chem. B. 104:2000;390-401.
44. Chalikian T.V. Volumetric properties of proteins. Annu. Rev. Biophys. Biomol. Struct. 32:2003;207-235.
45. Kharakoz D.P. Partial molar volumes of molecules of arbitrary shape and the effect of hydrogen bonding with water. J. Soln Chem. 21:1992;569-595.
46. Chalikian T.V., Breslauer K.J. Thermodynamic analysis of biomolecules: a volumetric approach. Curr. Opin. Struct. Biol. 8:1998;657-664.
47. Richards F.M. Areas, volumes, packing and protein structure. Annu. Rev. Biophys. Bioeng. 6:1977;151-176.
48. Richards F.M. Calculation of molecular volumes and areas for structures of known geometry. Methods Enzymol. 115:1985;440-464.
49. Connolly M.L. Analytical molecular surface calculation. J. Appl. Crystallog. 16:1983;548-558.
50. Connolly M.L. Solvent-accessible surfaces of proteins and nucleic acids. Science. 221:1983;709-713.
51. Chalikian T.V. Structural thermodynamics of hydration. J. Phys. Chem. ser. B. 105:2001;12566-12578.
52. Taulier N., Chalikian T.V. Compressibility of protein transitions. Biochim. Biophys. Acta. 1595:2002;48-70.
53. Makhatadze G.I., Privalov P.L. Energetics of protein structure. Advan. Protein Chem. 47:1995;307-425.
54. Pickett S.D., Sternberg M.J.E. Empirical scale of side chain conformational entropy in protein folding. J. Mol. Biol. 231:1993;825-839.
55. Thompson J.B., Hansma H.G., Hansma P.K., Plaxco K.W. The backbone conformational entropy of protein folding: experimental measures from atomic force microscopy. J. Mol. Biol. 322:2002;645-652.
56. von Hippel P.H. Protein-DNA recognition: new perspectives and underlying themes. Science. 263:1994;769-770.
57. Poornima C.S., Dean P.M. Hydration in drug design. 1. Multiple hydrogen-bonding features of water molecules in mediating protein-ligand interactions. J. Comput. Aided Mol. Des. 9:1995;500-512.
58. Lemieux R.U. How water provides the impetus for molecular recognition in aqueous solution. Accts Chem. Res. 29:1996;373-380.
59. Lundbäck T., Härd T. Sequence-specific DNA-binding dominated by dehydration. Proc. Natl Acad. Sci. USA. 93:1996;4754-4759.
60. Jen-Jacobson L. Protein-DNA recognition complexes: structure and binding energy in the transition state. Biopolymers. 44:1997;153-180.
61. Reid C., Rand R.P. Probing protein hydration and conformational states in solution. Biophys. J. 72:1997;1022-1030.
62. Schwabe J.W.R. The role of water in protein-DNA interactions. Curr. Opin. Struct. Biol. 7:1997;126-134.
63. Robinson C.R., Sligar S.G. Change in solvation during DNA binding and cleavage are critical to altered specificity of the EcoRI endonuclease. Proc. Natl Acad. Sci. USA. 95:1998;2186-2191.
64. Sidorova N.Y., Rau D.C. Linkage of EcoRI dissociation from its specific DNA recognition site to water activity, salt concentration, and pH: separating their roles in specific and non-specific binding. J. Mol. Biol. 310:2001;801-816.
65. Ladbury J.E. Just add water! The effect of water on the specificity of protein-ligand binding sites and its potential application to drug design. Chem. Biol. 3:1996;973-980.
66. Swint L., Robertson A.D. Thermodynamics of unfolding for turkey ovomucoid third domain: thermal and chemical denaturation. Protein Sci. 2:1993;2037-2049.
67. Kupke D.W. Density and volume change measurements. Leach S.J. Physical Principles and Techniques of Protein Chemistry. 1973;1-75 Academic Press, New York. part C.
68. Eggers F. Ultrasonic velocity and attenuation measurements in liquids with resonator, extending the MHz frequency range. Acustica. 76:1992;231-240.
69. Eggers F., Funck T. Ultrasonic measurements with millilitre liquid samples in the 0.5-100 MHz range. Rev. Sci. Instrum. 44:1973;969-978.
70. Eggers F., Kaatze U. Broad-band ultrasonic measurement techniques for liquids. Meas. Sci. Technol. 7:1996;1-19.
71. Sarvazyan A.P. Development of methods of precise ultrasonic measurements in small volumes of liquids. Ultrasonics. 20:1982;151-154.
72. Chalikian T.V., Gindikin V.S., Breslauer K.J. Volumetric characterizations of the native, molten, and unfolded states of cytochrome c at acidic pH. J. Mol. Biol. 250:1995;291-306.
73. Barnatt S. The velocity of sound in electrolytic solutions. J. Chem. Phys. 20:1952;278-279.
74. Owen B.B., Simons H.L. Standard partial molal compressibilities by ultrasonics. 1. Sodium chloride and potassium chloride at 25°C. J. Phys. Chem. 61:1957;479-482.
75. Breslauer K.J., Freire E., Straume M. Calorimetry: a tool for DNA and ligand-DNA studies. Methods Enzymol. 211:1992;533-567.
76. Berstein F.C., Koetzle T.F., William G.J.B., Meyer E.F., Brice M.D., Rodgers J.R., et al. The Protein Data Bank: a computer-based archival file for macromolecular structure. J. Mol. Biol. 112:1977;535-542.
77. Berman H.M., Westbrook J., Feng Z., Gilliland G., Bhat T.N., Weissig H., et al. The Protein Data Bank. Nucl. Acids Res. 28:2000;235-242.
78. Lee B.K., Richards F.M. The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55:1971;397-400.
79. Gerstein M. A resolution-sensitive procedure for comparing protein surfaces and its application to the comparison of antigen-combining sites. Acta Crystallog. sect. A. 48:1992;271-276.
80. Gerstein M., Tsai J., Levitt M. The volume of atoms on the protein surface: calculated from simulation, using Voronoi polyhedra. J. Mol. Biol. 249:1995;955-966.
81. Harpaz Y., Gerstein M., Chothia C. Volume changes on protein folding. Structure. 2:1994;641-649.