Entropy-enthalpy compensation: Role and ramifications in biomolecular ligand recognition and design

Annual Review of Biophysics

Volumn 42, Issue 1, 2013, Pages 121-142

  Chodera, John D ^a   Mobley, David L ^b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

entropy enthalpy compensation; isothermal titration calorimetry; small molecule ligand engineering

Indexed keywords

LIGAND;

ARTICLE; CALORIMETRY; CORRELATION ANALYSIS; DECOMPOSITION; ENTHALPY; ENTROPY; HIGH THROUGHPUT SCREENING; HOMEOSTASIS; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; MEASUREMENT ERROR; MOLECULAR DOCKING; MOLECULAR RECOGNITION; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; THERMODYNAMICS;

CALORIMETRY; ENTROPY; LIGANDS; PROTEIN BINDING; PROTEINS; THERMODYNAMICS;

EID: 84877768087     PISSN: 1936122X     EISSN: 19361238     Source Type: Book Series    
DOI: 10.1146/annurev-biophys-083012-130318     Document Type: Article

References (119)

1. Baranauskiene L, Petrikaite V, Matuliene J, Matulis D. 2009. Titration calorimetry standards and the precision of isothermal titration calorimetry data. Int. J. Mol. Sci. 10:2752-622
2. Baron R, Molinero V. 2012. Water-driven cavity-ligand binding: Comparison of thermodynamic signatures from coarse-grained and atomic-level simulations. J. Chem. Theory Comput. 7:3696-7044
3. Baum B, Muley L, Smolinski M, Heine A, Hangauer D, Klebe G. 2010. Non-additivity of functional group contributions in protein ligand binding: A comprehensive study by crystallography and isothermal titration calorimetry. J. Mol. Biol. 397:1042-544
4. Beasley JR, DoyleDF, Chen L, CohenDS, Fine BR, Pielak GJ. 2002. Searching for quantitative entropyenthalpy compensation among protein variants. Proteins 49:398-4022
5. Bennaim A. 1978. Standard thermodynamics of transfer: Uses and misuses. J. Phys. Chem. 82:792-8033
6. B?ohm H, Klebe G. 1996. What can we learn from molecular recognition in protein-ligand complexes for the design of new drugs? Angew. Chem. Int. Ed. Engl. 35:2588-6144
7. Boresch S, Tettinger F, Leitgeb M, Karplus M. 2005. Absolute binding free energies: A quantitative approach for their calculation. J. Phys. Chem. B 107:9535-511
8. Boyce SE, Mobley DL, Rocklin GJ, Graves AP, Dill KA, Shoichet BK. 2009. Predicting ligand binding affinity with alchemical free energy methods in a polar model binding site. J. Mol. Biol. 394:747-633
9. Brandt T, Holzmann N, Muley L, Khayat M, Wegscheid-Gerlach C, et al. 2011. Congeneric but still distinct: How closely related trypsin ligands exhibit different thermodynamic and structural properties. J. Mol. Biol. 405:1170-877
10. Chang CE, Gilson MK. 2004. Free energy, entropy, and induced fit in host-guest recognition: Calculations with the second-generation mining minima algorithm. J. Am. Chem. Soc. 126:13156-644
11. Chodera JD, Mobley DL, Shirts MR, Dixon RW, Branson K, Pande VS. 2011. Alchemical free energy methods for drug discovery: Progress and challenges. Curr. Opin. Struct. Biol. 21:150-600
12. Christ CD, van Gunsteren WF. 2008. Multiple free energies from a single simulation: Extending enveloping distribution sampling to nonoverlapping phase-space distributions. J. Chem. Phys. 128:1741122
13. ChristensenT,GoodenDM, Kung JE,Toone EJ. 2003. Additivity and the physical basis ofmultivalency effects: A thermodynamic investigation of the calcium EDTA interaction. J. Am. Chem. Soc. 125:7357-666
14. Cooper A. 2011. Microcalorimetry of heat capacity and volumetric changes in biomolecular interactions - the link to solvation? J. Therm. Anal. Calorim. 104:69-733
15. CooperA, Johnson CM,Lakey JH,NöllmannM. 2001. Heat does not come in different colours: Entropyenthalpy compensation, free energy windows, quantum confinement, pressure perturbation calorimetry, solvation and the multiple causes of heat capacity effects in biomolecular interactions. Biophys. Chem. 93:215-300
16. Cornish-Bowden A. 2002. Enthalpy-entropy compensation: A phantom phenomenon. J. Biosci. 27:121- 266
17. de Rivera M, Socorro F. 2005. Baseline changes in an isothermal titration microcalorimeter. J. Therm. Anal. Calorim. 80:769-733
18. Delorbe JE, Clements JH, Whiddon BB, Martin SF. 2010. Thermodynamic and structural effects of macrocyclic constraints in protein-ligand interactions. ACS Med. Chem. Lett. 1:448-522
19. Deng Y, Roux B. 2009. Computations of standard binding free energies with molecular dynamics simulations. J. Phys. Chem. B 113:2234-466
20. Dill KA, Bromberg S. 2003. Molecular Driving Forces: Statistical Thermodynamics in Chemistry and Biology. New York: Garland Science
21. Donnini S, Villa A, GroenhofG,Mark AE, Wierenga RK, Juffer AH. 2009. Inclusion of ionization states of ligands in affinity calculations. Proteins 76:138-500
22. Dunitz JD. 2003. Win some, lose some: Enthalpy-entropy compensation in weak intermolecular interactions. Chem. Biol. 2:709-122
23. Exner O. 1964. Concerning the isokinetic relationship. Nature 201:488-900
24. ExnerO. 1997. How to get wrong results from good experimental data: A survey of incorrect applications of regression. J. Phys. Org. Chem. 10:797-8133
25. Exner O. 2000. Entropy-enthalpy compensation and anticompensation: Solvation and ligand binding. Chem. Commun. 2000:1655-566
26. Fenley AT, Muddana HS, Gilson MK. 2012. Entropy-enthalpy transduction caused by conformational shifts can obscure the forces driving protein-ligand binding. Proc. Natl. Acad. Sci. USA 109:20006-111
27. Ferenczy GG, Keser ?uGM. 2010. Enthalpic efficiency of ligand binding. J. Chem. Inf.Model. 50:1536-411
28. Ferenczy GG, Keser ?uGM. 2010. Thermodynamics guided lead discovery and optimization. Drug Discov. Today 15:919-322
29. FerranteA,Gorski J. 2012. Enthalpy-entropy compensation and cooperativity as thermodynamic epiphenomena of structural flexibility in ligand-receptor interactions. J. Mol. Biol. 417:454-677
30. Ferrari AM, Degliesposti G, Sgobba M, Rastelli G. 2007. Validation of an automated procedure for the prediction of relative free energies of binding on a set of aldose reductase inhibitors. Bioorg. Med. Chem. 15:7865-777
31. Fisher HF. 2012. Detecting "silent" allosteric coupling. Methods Mol. Biol. 796:71-966
32. Ford DM. 2005. Enthalpy-entropy compensation is not a general feature of weak association. J. Am. Chem. Soc. 127:16167-700
33. Forrey C,Douglas JF,Gilson MK. 2012. The fundamental role of flexibility on the strength of molecular binding. Soft Matter 8:6385-922
34. Freire E. 2008. Do enthalpy and entropy distinguish first in class from best in class? Drug Discov. Today 13:869-744
35. Fujitani H, Tanida Y, ItoM, Jayachandran G, Snow C, et al. 2005. Direct calculation of the binding free energies of FKBP ligands. J. Chem. Phys. 123:0841088
36. Gallicchio E, Kubo MM, Levy RM. 1998. Entropy-enthalpy compensation in solvation and ligand binding revisited. J. Am. Chem. Soc. 120:4526-277
37. Gallicchio E, Levy RM. 2011. Advances in all atom sampling methods for modeling protein-ligand binding affinities. Curr. Opin. Struct. Biol. 21:161-666
38. General IJ. 2010. A note on the standard state's binding free energy. J. Chem. Theory Comput. 6:2520-244
39. Gilson MK,Given J, Bush B, McCammon J. 1997. The statistical- thermodynamic basis for computation of binding affinities: A critical review. Biophys. Chem. 72:1047-699
40. Gohlke H, Case DA. 2004. Converging free energy estimates: MM-PB(GB)SA studies on the proteinprotein complex Ras-Raf. J. Comput. Chem. 25:238-500
41. Graves AP, Shivakumar DM, Boyce SE, Jacobson MP, Case DA, Shoichet BK. 2008. Rescoring docking hit lists for model cavity sites: Predictions and experimental testing. J. Mol. Biol. 377:914-344
42. Graziano G. 2012. Molecular driving forces of the pocket-ligand hydrophobic association. Chem. Phys. Lett. 533:95-999
43. Grunwald E, Steel C. 1995. Solvent reorganization and thermodynamic enthalpy-entropy compensation. J. Am. Chem. Soc. 117:5687-922
44. Hansen LD, Fellingham GW, Russell DJ. 2011. Simultaneous determination of equilibrium constants and enthalpy changes by titration calorimetry: Methods, instruments, and uncertainties. Anal. Biochem. 409:220-299
45. Hess B, van der Vegt NFA. 2006. Hydration thermodynamic properties of amino acid analogues: A systematic comparison of biomolecular force fields and water models. J. Phys. Chem. B 110:17616-266
46. Holloway MK, Wai JM, Halgren TA, Fitzgerald PMD, Vacca JP, et al. 1995. A priori prediction of activity for HIV-1 protease inhibitors employing energy minimization in the active site. J. Med. Chem. 38:305-177
47. Hou T, Wang J, Li Y, Wang W. 2011. Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations. J. Chem. Inf. Model. 51:69-822
48. Jorgensen WL. 2009. Progress and issues for computationally guided lead discovery and optimization. In Drug Design: Structure- and Ligand-Based Approaches, ed. KM Merz, D Ringe, CH Reynolds, pp. 1-14. Cambridge, UK: Cambridge Univ. Press
49. King NM, Prabu-Jeyabalan M, Bandaranayake RM, Nalam MNL, Nalivaika EA, et al. 2012. Extreme entropy-enthalpy compensation in a drug-resistant variant ofHIV-1 protease.ACS Chem. Biol. 7:1536-466
50. Klebe G. 2011. On the validity of popular assumptions in computational drug design. J. Cheminform. 3:O188
51. Knight JL, Brooks CL III. 2011. Multisite λ dynamics for simulated structure-activity relationship studies. J. Chem. Theory Comput. 7:2728-399
52. Koch C, Heine A, Klebe G. 2011. Tracing the detail: How mutations affect binding modes and thermodynamic signatures of closely related aldose reductase inhibitors. J. Mol. Biol. 406:700-122
53. Kramer C, Kalliokoski T, Gedeck P, Vulpetti A. 2012. The experimental uncertainty of heterogeneous public Ki data. J. Med. Chem. 55:5165-733
54. Krug RR, HungterWG, Grieger RA. 1976. Statistical interpretation of enthalpy-entropy compensation. Nature 261:566-677
55. Kuntz ID, Chen K, Sharp KA, Kollman PA. 1999. The maximal affinity of ligands. Proc. Natl. Acad. Sci. USA 96:9997-100022
56. Kurioki R,Nitta K, Yutani K. 1992. Thermodynamic changes in the binding of Ca2+ to amutant human lysozyme (D86/92): Enthalpy-entropy compensation observed upon Ca2+ binding to proteins. J. Biol. Chem. 267:24297-3011
57. Ladbury JE, Klebe G, Freire E. 2010. Adding calorimetric data to decision making in lead discovery: A hot tip. Nat. Rev. Drug Discov. 9:23-277
58. Lafont V, Armstrong AA, Ohtaka H, Kiso Y, Mario Amzel L, Freire E. 2007. Compensating enthalpic and entropic changes hinder binding affinity optimization. Chem. Biol. Drug Discov. 69:413-222
59. Lee B. 1991. Solvent reorganization contribution to the transfer thermodynamics of small nonpolar molecules. Biopolymers 31:993-10088
60. Lee B, Graziano G. 1996. A two-state model of hydrophobic hydration that produces compensating enthalpy and entropy changes. J. Am. Chem. Soc. 118:5163-688
61. Leffler JE. 1955. The enthalpy-entropy relationship and its implications for organic chemistry. J. Org. Chem. 20:1202-311
62. Liu T, Lin Y, Wen X, Jorissen RN, Gilson MK. 2007. BindingDB: A web-accessible database of experimentally determined protein-ligand binding affinities. Nucleic Acids Res. 35:D198-2011
63. Lumry R, Rajender S. 1970. Enthalpy-entropy compensation phenomena in water solutions of proteins and small molecules: A ubiquitous property of water. Biopolymers 9:1125-2277
64. Lyubartsev AP, Martsinovski AA, Shevkunov SV, Vorontsov-Velyaminov PN. 1992. New approach to Monte Carlo calculation of the free energy: Method of expanded ensembles. J. Chem. Phys. 96:1776-833
65. Makhatadze GI, Privalov PL. 1994. Hydration effects in protein unfolding. Biophys. Chem. 51:291-3099
66. Martin YC. 2009. Let's not forget tautomers. J. Comput. Aid. Mol. Des. 23:693-7044
67. McGregor R, Milícevíc B. 1966. On the enthalpy-entropy relationship. Nature 211:523-255
68. Mizoue LS, Tellinghuisen J. 2004. The role of backlash in the "first injection anomaly" in isothermal titration calorimetry. Anal. Biochem. 326:125-277
69. Mobley DL. 2012. Let's get honest about sampling. J. Comput. Aid. Mol. Des. 26:93-955
70. Mobley DL,Graves AP, Chodera JD, McReynolds AC, Shoichet BK,Dill KA. 2007. Predicting absolute ligand binding free energies to a simple model site. J. Mol. Biol. 371:1118-344
71. Myszka DG, Abdiche YN, Arisaka F, Byron O, Eisenstein E, et al. 2009. The ABRF-MIRG'02 study: Assembly state, thermodynamic, and kinetic analysis of an enzyme/inhibitor interaction. J. Biomol. Tech. 14:247-699
72. Olsson TSG, Ladbury JE, Pitt WR, Williams MA. 2011. Extent of enthalpy-entropy compensation in protein-ligand interactions. Protein Sci. 20:1607-188
73. Peters WB, Frasca V, Brown RK. 2009. Recent developments in isothermal titration calorimetry label free screening. Comb. Chem. High Throughput Screen. 12:772-900
74. Petersen RC. 1964. Linear relationship between enthalpy and entropy of activation. J. Org. Chem. 29:31333
75. Petersen RC, Markgraf JH, Ross SD. 1961. Solvent effects in decomposition of 1,1-diphenylazoethane and 2,2-azobis-(2-methylpropionitrile). J. Am. Chem. Soc. 83:3819-233
76. Pitera JW, Kollman PA. 2000. Exhaustive mutagenesis in silico:multicoordinate free energy calculations on proteins and peptides. Proteins 41:385-977
77. Qian H. 1998. Entropy-enthalpy compensation: Conformational fluctuation and induced-fit. J. Chem. Phys. 109:10015-177
78. Qian H. 2006. An asymptotic comparative analysis of the thermodynamics of non-covalent association. J. Math. Biol. 52:277-899
79. Qian H, Hopfield JJ. 1996. Entropy-enthalpy compensation: Perturbation and relaxation in thermodynamic systems. J. Chem. Phys. 105:9292-988
80. Rekharsky MV, Mori T, Yang C, Ko YH, Selvapalam N, et al. 2007. A synthetic host-guest system achieves avidin-biotin affinity by overcoming enthalpy-entropy compensation. Proc. Natl. Acad. Sci. USA 104:20737-422
81. Reynolds CH,HollowayMK. 2011. Thermodynamics of ligand binding and efficiency. ACSMed. Chem. Lett. 2:433-377
82. Rudzinski JF, Noid WG. 2011. Coarse-graining entropy, forces, and structures. J. Chem. Phys. 135:2141011
83. Schneider G. 2010. Virtual screening: An endless staircase? Nat. Rev. Drug Discov. 9:273-766
84. Scior T, Bender A, Tresadern G, Medina-Franco JL, Mart́inez-Mayorga K, et al. 2012. Recognizing pitfalls in virtual screening: A critical review. J. Chem. Inf. Model. 52:867-811
85. Searle MS,WestwellMS, WilliamsDH. 1995. Application of a generalised enthalpy-entropy relationship to binding co-operativity and weak associations in solution. J. Chem. Soc. Perkin Trans. 2:141-511
86. Setny P, Baron R, McCammon JA. 2010. How can hydrophobic association be enthalpy driven? J. Chem. Theory Comput. 6:2866-711
87. rfsti Sharp K. 2001. Entropy-enthalpy compensation: Fact or artifact? Protein Sci. 10:661-677
88. ShirtsMR. 2012. Best practices in free energy calculations for drug design. MethodsMol. Biol. 819:425-677
89. Shoichet BK. 2004. Virtual screening of chemical libraries. Nature 432:862-655
90. Singh N, Warshel A. 2010. A comprehensive examination of the contributions to the binding entropy of protein-ligand complexes. Proteins 78:1724-355
91. Snyder PW, Mecinovic J, Moustakas DT, Thomas SW 3rd, Harder M, et al. 2011. Mechanism of the hydrophobic effect in the biomolecular recognition of arylsulfonamides by carbonic anhydrase. Proc. Natl. Acad. Sci. USA 108:17889-944
92. Socorro F, de La Nuez I, Alvarez L, de Rivera M. 2004. Effect of a stirring process in an isothermal titration microcalorimeter. Thermochim. Acta 420:163-677
93. Starikov EB,Nord́en B. 2007. Enthalpy-entropy compensation: A phantom or something useful? J. Phys. Chem. B 111:14431-355
94. Starikov EB, Nord́en B. 2012. Entropy-enthalpy compensation as a fundamental concept and analysis tool for systematical experimental data. Chem. Phys. Lett. 538:118-200
95. Swanson JMJ, Henchman RH, McCammon JA. 2004. Revisiting free energy calculations: A theoretical connection to MM/PBSA and direct calculation of the association free energy. Biophys. Chem. 86:67-744
96. Talhout R, Villa A, Mark AE, Engberts JBFN. 2003. Understanding binding affinity: A combined isothermal titration calorimetry/molecular dynamics study of the binding of a series of hydrophobically modified benzamidinium chloride inhibitors to trypsin. J. Am. Chem. Soc. 125:10570-799
97. Tellinghuisen J. 2003. A study of statistical error in isothermal titration calorimetry. Anal. Biochem. 321:79-888
98. Tellinghuisen J. 2004. Statistical error in isothermal titration calorimetry. Methods Enzymol. 383:245-822
99. Tellinghuisen J. 2004. Volume errors in isothermal titration calorimetry. Anal. Biochem. 333:405-66
100. Tellinghuisen J. 2005. Optimizing experimental parameters in isothermal titration calorimetry. J. Phys. Chem. B 109:20027-355
101. Tellinghuisen J. 2005. Statistical error in isothermal titration calorimetry: Variance function estimation from generalized least squares. Anal. Biochem. 343:106-155
102. Tellinghuisen J. 2006. Van't Hoff analysis of K(T): How good. . .or bad? Biophys. Chem. 120:114-200
103. Tellinghuisen J. 2007. Optimizing experimental parameters in isothermal titration calorimetry: Variable volume procedures. J. Phys. Chem. B 111:11531-377
104. Tellinghuisen J. 2008. Isothermal titration calorimetry at very low c. Anal. Biochem. 373:395-977
105. Tellinghuisen J. 2012. Designing isothermal titration calorimetry experiments for the study of 1:1 binding: Problems with the "standard protocol". Anal. Biochem. 424:211-200
106. Tellinghuisen J, Chodera JD. 2011. Systematic errors in isothermal titration calorimetry: Concentrations and baselines. Anal. Biochem. 414:297-999
107. Tembe BL, McCammon JA. 2001. Ligand receptor interactions. Comput. Chem. 8:281-833
108. Tomlinson E. 1983. Enthalpy-entropy compensation analysis of pharmaceutical, biochemical and biological systems. Int. J. Pharm. 13:115-444
109. Tzeng SR, KalodimosCG. 2012. Protein activity regulation by conformational entropy. Nature 488:236- 400
110. Varadarajan R, Connelly PR, Sturtevant JM, Richards FM. 1992. Heat capacity changes for proteinpeptide interactions in the ribonuclease S system. Biochemistry 31:1421-266
111. Veĺazquez-Campoy A, Freire E. 2006. Isothermal titration calorimetry to determine association constants for high-affinity ligands. Nat. Protoc. 1:186-911
112. Veĺazquez-Campoy A, Ohtaka H, Nezami A,Muzammil S, Freire E. 2004. Isothermal titration calorimetry. Curr. Protoc. Cell Biol. 17.8.1:1-244
113. Ward JM, Gorenstein NM, Tian J, Martin SF, Post CB. 2010. Constraining binding hot spots: NMR andmolecular dynamics simulations provide a structural explanation for enthalpy-entropy compensation in SH2-ligand binding. J. Am. Chem. Soc. 132:11058-700
114. Whitesides GM, Snyder PW, Moustakas DT, Mirica KA. 2008. Designing ligands to bind tightly to proteins. In Physical Biology: From Atoms to Medicine, ed. AH Zewail, pp. 189-215. Singapore: World Scientific
115. Wiseman T,Williston S, Brandts JF, Lin LN. 1989. Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal. Biochem. 179:131-377
116. Wlodawer A, Vondrasek J. 1998. Inhibitors of HIV-1 protease: Amajor success of structure-assisted drug design. Annu. Rev. Biophys. Biomol. Struct. 27:249-844
117. Woo HJ, Roux B. 2005. Calculation of absolute protein-ligand binding free energy from computer simulations. Proc. Natl. Acad. Sci. USA 102:6825-300
118. Zeevaart JG, Wang L, Thakur VV, Leung CS, Tirado-Rives J, et al. 2008. Optimization of azoles as anti-human immunodeficiency virus agents guided by free-energy calculations. J. Am. Chem. Soc. 130:9492-999
119. Zhou HX, Gilson MK. 2009. Theory of free energy and entropy in noncovalent binding. Chem. Rev. 109:4092-1077