Characterization of binding interactions by isothermal titration calorimetry

Current Opinion in Biotechnology

Volumn 8, Issue 1, 1997, Pages 31-35

  Doyle, Michael L ^a  

^a GLAXOSMITHKLINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING AFFINITY; CALORIMETRY; DRUG DESIGN; ENTHALPY; MICROCALORIMETRY; MOLECULAR INTERACTION; PRIORITY JOURNAL; REVIEW; STOICHIOMETRY; THERMODYNAMICS; TITRIMETRY;

EID: 0031027122     PISSN: 09581669     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0958-1669(97)80154-1     Document Type: Article

References (55)

1. 1. Murphy KP, Freire E, Paterson Y: Configurational effects in antibody-antigen interactions studied by microcalorimetry. Proteins 1995, 21:83-90. A focused analysis of binding thermodynamics for two monoclonal antibodies (mAbs). It demonstrates two distinct antigen-binding mechanisms that have similar affinity. In one case, thermodynamic analysis revealed that conformational changes are coupled to binding. The extent of conformational change, solvent release, and amount of water-accessible surface area buried in the reaction were estimated from thermodynamics.
2. 2. Schwarz FP, Tello D, Goldbaum FA, Mariuzza RA, Poljak RJ: Thermodynamics of antigen-antibody binding using specific anti-lysozyme antibodies. Eur J Biochem 1995, 228:388-394. This paper exemplifies the type of rigorous analysis that ITC affords in evaluating the functional chemistries of antigen binding to various mAbs and subfragments. It surveys five different antibodies that exhibit a range of thermodynamics.
3. 3. Tsumoto K, Ogasahara K, Ueda Y, Watanabe K, Yutani K, Kumagai I: Role of tyr residues in the contact region of anti-lysozyme monoclonal antibody hyhel10 for antigen binding. J Biol Chem 1995, 270:18551-18557.
4. 4. Raman CS, Allen MJ, Nall BT: Enthalpy of antibody-cytochrome c binding. Biochemistry 1995, 34:5831-5838. Different binding mechanisms of two anti-cytochrome c mAbs were demonstrated from the analysis of thermodynamics. In one case, ITC data showed protonation was coupled to binding.
5. 5. Kelley RF, O'Connell MP: Thermodynamic analysis of an antibody functional epitope. Biochemistry 1993, 32:6828-6835.
6. 6. Gomez J, Freire E: Thermodynamic mapping of the inhibitor site of the aspartic protease endothiapepsin. J Mol Biol 1995, 252:337-350. A comprehensive thermodynamic study that dissected the individual contributions of amino acids to a peptide-protein binding interaction. This paper points out the specific properties of protein-ligand interactions (e.g. coupled protonation events and conformational entropies for amino acid sidechains) that must be taken into account when using thermodynamic approaches to structure-based drug design.
7. 7. Mandiyan V, O'Brien R, Zhou M, Margolis B, Lemmon MA, Sturtevant JM, Schlessinger J: Thermodynamic studies of SHC phosphotyrosine interaction domain recognition of the NPXpY motif. J Biol Chem 1996, 271:4770-4775.
8. 8. Rolf B, Oudenampsen-Kruger E, Borchers T, Faergeman NJ, Knodsen J, Lezius A, Spener F: Analysis of the ligand binding properties of recombinant bovine liver-type fatty acid binding protein. Biochim Biophys Acta 1995, 1259:245-253.
9. 9. Terzi E, Holzemann G, Seelig J: Self-association of beta-amyloid peptide (1-40) in solution and binding to lipid membranes. J Mol Biol 1995, 252:633-642.
10. 10. Seelig A, Alt T, Lotz S, Holzemann G: Binding of substance P agonists to lipid membranes and to the neurokinin-1 receptor. Biochemistry 1996, 35:4365-4374.
11. 11. Evans LJA, Cooper A, Lakey JH: Direct measurement of the association of a protein with a family of membrane receptors. J Mol Biol 1996, 255:559-563. The authors measured the affinities and stoichiometries for colicin N binding to three membrane receptors by ITC. Although the affinities were all very similar, the underlying thermodynamics were divergent and demonstrated different molecular binding mechanisms.
12. 12. Lin LN, Li J, Brandts JF, Weiss RM: The serine receptor of bacterial chemotaxis exhibits half-site saturation for serine binding. Biochemistry 1994, 33:6564-6570.
13. 13. Johanson K, Appelbaum E, Doyle M, Hensley P, Zhao B, Abdel-Meguid SS, Young P, Cook R, Carr S, Matico R et al.: Binding interactions of human interleukin-5 with its receptor alpha subunit. J Biol Chem 1995, 270:9459-9471.
14. 14. Pantoliano MW, Horlick RA, Springer BA, Van Dyk DE, Tobery T, Wetmore DR, Lear JD, Nahapetian AT, Bradley JD, Sisk WR: Multivalent ligand-receptor binding interactions in the fibroblast growth factor system produces a cooperative growth factor and heparin mechanism for receptor dimerization. Biochemistry 1994, 33:10229-10248.
15. 15. Pearce KH, Ultsch MH, Kelley RF, De Vos AM, Wells JA: Structural and mutational analysis of affinity-inert contact residues at the growth hormone-receptor interface. Biochemistry 1996, 35:10300-10307. Results showed that for certain alanine mutants, the affinity, kinetics and global structure were not affected, but large compensating enthalpy-entropy effects indicated the presence of local structure changes.
16. 16. Brummell DA, Sharma VP, Anand NN, Bilous D, Dubuc G, Michniewicz J, MacKenzie CR, Sadowska J, Sigurskjold BW, Sinnott B et al.: Probing the combining site of an anti-carbohydrate antibody by saturation-mutagenesis: role of the heavy-chain CDR3 residues. Biochemistry 1993, 32:1180-1187.
17. 17. Evans SV, Sigurskjold BW, Jennings HJ, Brisson JR, To R, Tse WC, Altman E, Frosch M, Weisgerber C, Kratzin HD et al.: Evidence for the extended helical nature of polysaccharide epitopes. The 2.8 Å resolution structure and thermodynamics of ligand binding of an antigen binding fragment specific for a-(2-8)-polysialic acid. Biochemistry 1995, 34:6737-6744.
18. 18. Schwarz FP, Misquith S, Surolia A: Effect of substituent on the thermodynamics of d-glucopyranoside binding to concanavalin a, pea (Pisum sativum) lectin and lentil (Lens culinaris) lectin. Biochem J 1996, 316:123-129.
19. 19. Berland CR, Sigurskjold BW, Stoffer B, Frandsen TP, Svensson B: Thermodynamics of inhibitor binding to mutant forms of glucoamylase from Aspergillus niger determined by isothermal titration calorimetry. Biochemistry 1995, 34:10153-10161.
20. 20. Lundback T, Hard T: Sequence-specific DNA-binding dominated by dehydration. Proc Natl Acad Sci USA 1996, 93:4754-4759.
21. 21. Plum GR, Breslauer KJ: Calorimetry of proteins and nucleic acids. Curr Opin Struct Biol 1995, 5:682-690. A recent review that focuses on the calorimetric analysis of protein-nucleic acid interactions.
22. 22. Lohman TM, Overman LB, Ferrari ME, Kozlov AG: A highly salt-dependent enthalpy change for Escherichia coli SSB protein-nucleic acid binding due to ion-protein interactions. Biochemistry 1996, 35:5272-5279. This paper reports the large effects that specific salts can have on the thermodynamics of protein-nucleic acid interactions. It indicates that an accurate understanding of structure-thermodynamic relationships in binding specificity will require the characterization of salt effects.
23. 23. Ladbury JE, Wright JG, Sturtevant JM, Sigler PB: A thermodynamic study of the trp repressor-operator interaction. J Mol Biol 1994, 238:669-681.
24. 24. Reedstrom RJ, Royer CA: Evidence for coupling of folding and function in trp repressor: physical characterization of the superrepressor mutant AV77. J Mol Biol 1995, 253:266-276. It was demonstrated from the analysis of binding thermodynamics and other biophysical methods that conformational changes are coupled to tryptophan (trp) binding to trp repressor and that the extent of conformational change is diminished in the AV77 mutant.
25. 25. Merabet E, Ackers GK: Calorimetric analysis of lambda cl repressor binding to DNA operator sites. Biochemistry 1995, 34:8554-8563. The analysis of cl-DNA binding thermodynamics for various combinations of the three operator binding sites demonstrated that sequence-dependent structural changes play a role in the mechanism of cl binding and cooperativity.
26. 26. Kresheck GC, Vitello LB, Erman JE: Calorimetric studies on the interaction of horse ferricytochrome c and yeast cytochrome c peroxidase. Biochemistry 1995, 34:8398-8405.
27. 27. Lin Z, Schwarz FP, Eisenstein E: The hydrophobic nature of GroEL-substrate binding. J Biol Chem 1995, 270:1011-1014. The binding mechanism of GroEL to two different proteins is implicated to be dominated by hydrophobic forces based on the thermodynamic signature of the binding interactions, particularly the large negative heat capacity change.
28. 28. Wu ML, Morgan WT: Thermodynamics of heme-induced conformational changes in hemopexin: role of domain-domain interactions. Protein Sci 1995, 4:29-34.
29. 29. Li J, Swanson RV, Simon MI, Weiss RM: The response regulators CheB and CheY exhibit competitive binding to the kinase CheA. Biochemistry 1995, 34:14626-14636.
30. 30. Wu J, Li J, Li G, Long DG, Weiss RM: The receptor binding site for the methyltransferase of bacterial chemotaxis is distinct from the sites of methylation. Biochemistry 1996, 35:4984-4993. ITC was used to localize the methyltransferase binding site on the receptor to the last five amino acids of the cytoplasmic domain. Moreover, they found that the pentapeptide had affinity and thermodynamics that were very similar to the full-length receptor. The results guided structural modeling of the mechanism of receptor methylation.
31. 31. Connelly PR, Aldape RA, Bruzzese FJ, Chambers SP, Fitzgibbon MJ, Fleming MA, Itoh S, Livingston DJ, Navia MA, Thomson JA, Wilson KP: Enthalpy of hydrogen bond formation in a protein-ligand binding reaction. Proc Natl Acad Sci USA 1994, 91:1964-1968.
32. 32. Weber PC, Pantoliano MW, Simmons DM, Salemme FR: Structure-based design of synthetic azobenzene ligands for streptavidin. J Am Chem Soc 1994, 116:2717-2724.
33. 33. Morton A, Baase WA, Matthews BW: Energetic origins of specificity of ligand binding in an interior nonpolar cavity of T4 lysozyme. Biochemistry 1995, 34:8564-8575.
34. 34. Garcia-Fuentes L, Reche P, Lopez-Mayorga O, Santi DV, Gonzalez-Pacanowska D, Baron C: Thermodynamic analysis of the binding of 5-fluoro-2′-deoxyuridine 5′-monophosphate to thymidylate synthetase over a range of temperatures. Eur J Biochem 1995, 232:641-645. Analysis of the thermodynamics for FdUMP (5-fluoro-2′-deoxyuridine 5′-monophosphate) binding to thymidylate synthase suggests that coupled conformational changes are minimal and that binding is coupled to protonation. Molecular interpretation of the thermodynamics is presented in the light of crystallographic structural information.
35. 35. Xu Y, Johnson CR, Beckett D: Thermodynamic analysis of small ligand binding to the Escherichia coli repressor of biotin synthesis. Biochemistry 1996, 35:5509-5517. This study provides a thermodynamic analysis of the mechanistic differences between the ligands biotin and bio-5′-AMP binding to the biotin synthesis repressor. Analysis of the thermodynamics portrays the nature of the molecular structural origins for the different regulatory roles of these ligands.
36. 36. Gormley NA, Orphanides G, Meyer A, Cullis PM, Maxwell A: The interaction of coumarin antibiotics with fragments of the DNA gyrase b protein. Biochemistry 1996, 35:5083-5092.
37. 37. Marzabadi MR, Gruys KJ, Pansegrau PD, Walker MC, Yuen HK, Sikorski JA: An EPSP synthetase inhibitor joining shikimate 3-phosphate with glyphosate: synthesis and ligand binding studies. Biochemistry 1996, 35:4199-4210. Analysis of binding thermodynamics reveals the mode of binding for a novel EPSP (5-enolpyruvoylshikimate) inhibitor.
38. 38. Fisher HF, Singh N: Calorimetric methods for interpreting protein-ligand interactions. Methods Enzymol 1995, 259:194-221. A comprehensive review of the mechanics and practical issues involved in conducting ITC experiments. Includes discussion on data analysis and deconvolution of linked protons.
39. 39. Wiseman T, Williston S, Brandts JF, Lin LN: Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal Biochem 1989, 179:131-137.
40. 40. Wadso I: Isothermal microcalorimetry for the characterization of interactions between drugs and biological materials. Thermochim Acta 1995, 267:45-59.
41. 41. Bhatnagar RS, Gordon JI: Thermodynamic studies of myristoyl-CoA-protein n-myristoyltransferase using isothermal titration calorimetry. Methods Enzymol 1995, 250:467-486. Reviews practical aspects of ITC, including experimental design for tight/weak binding interactions.
42. 42. Bundle DR, Sigurskjold BW: Determination of accurate thermodynamics of binding by titration microcalorimetry. Methods Enzymol 1994, 247:288-304.
43. 43. Doyle ML, Myszka DG, Chaiken IW: Molecular interaction analysis in ligand design using mass transport, kinetic and thermodynamic methods. J Mol Recognit 1996, 9:65-74.
44. 44. Doyle ML, Louie G, Dal Monte PR, Sokoloski TD: Tight binding affinities determined from thermodynamic linkage to protons by titration calorimetry. Methods Enzymol 1995, 259:183-194.
45. 45. Privalov PL, Gill SJ: Stability of protein structure and hydrophobic interaction. In Advances in Protein Chemistry. New York: Academic Press; 1988:191-234.
46. 46. Wyman J, Gill SJ: Physical binding phenomena. In Binding and Linkage: Functional Chemistry of Biological Macromolecules. Mill Valley, CA: University Science Books; 1990:168-235.
47. 47. Liu Y, Sturtevant JM: Significant discrepancies between van't Hoff and calorimetric enthalpies II. Protein Sci 1995, 4:2559-2561. Exemplifies the remarkable high-precision capability of ITC instrumentation.
48. 48. Doyle ML, Hensley P: Experimental dissection of protein-protein interactions in solution. Adv Mol Cell Biol 1997, 21:in press. Describes the synergism of combining ITC experiments with other bioanalytical methods to rigorously characterize the binding interactions of proteins. Practical issues involved in using common solution biophysical methods are discussed.
49. 49. Eftink MR: Use of multiple spectroscopic methods to monitor equilibrium unfolding of proteins. Methods Enzymol 1995, 259:487-512.
50. 50. Baker BM, Murphy KP: Evaluation of linked protonation effects in protein binding reactions using isothermal titration calorimetry. Biophys J 1996, 71:2049-2055. A comprehensive treatise on the use of ITC to characterize protonation reactions that are coupled to ligand binding.
51. 51. Spolar RS, Record MT Jr: Coupling of local folding to site-specific binding of proteins to DNA. Science 1994, 263:777-784.
52. 52. Luque I, Mayorga OL, Freire E: Structure-based thermodynamic scale of alpha-helix propensities in amino acids. Biochemistry 1996, 35:13681-13688. Reports an accurate thermodynamic method for calculating protein folding energetics from structure. The method is shown to be predictive for calculating α-helix propensities. The method is also applicable to structure-based calculation of protein-peptide binding affinity.
53. 53. Ohyama T, Cowan JA: Calorimetric studies of metal binding to tetracycline. Role of solvent structure in defining the selectivity of metal ion-drug interactions. Inorg Chem 1995, 34:3083-3086. This model compound study reveals the utility of thermodynamics in deconvoluting specific hydration effects in binding interactions involving metals.
54. 54. Ladbury J, Peters R: Turning up the heat on rational drug design. Bio-Technology 1994, 12:1083-1085.
55. 55. Murphy KP, Freire E: Thermodynamic strategies for rational protein and drug design. Pharm Biotechnol 1995, 7:219-241.