1932

Abstract

Biomolecular recognition can be stubborn; changes in the structures of associating molecules, or the environments in which they associate, often yield compensating changes in enthalpies and entropies of binding and no net change in affinities. This phenomenon—termed enthalpy/entropy (H/S) compensation—hinders efforts in biomolecular design, and its incidence—often a surprise to experimentalists—makes interactions between biomolecules difficult to predict. Although characterizing H/S compensation requires experimental care, it is unquestionably a real phenomenon that has, from an engineering perspective, useful physical origins. Studying H/S compensation can help illuminate the still-murky roles of water and dynamics in biomolecular recognition and self-assembly. This review summarizes known sources of H/ compensation (real and perceived) and lays out a conceptual framework for understanding and dissecting—and, perhaps, avoiding or exploiting—this phenomenon in biophysical systems.

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2018-05-20
2024-10-12
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Literature Cited

  1. 1.  Adhikary R, Yu W, Oda M, Zimmermann J, Romesberg FE 2012. Protein dynamics and the diversity of an antibody response. J. Biol. Chem. 287:3227139–47
    [Google Scholar]
  2. 2.  Ahmad M, Helms V, Lengauer T, Kalinina OV 2015. Enthalpy–entropy compensation upon molecular conformational changes. J. Chem. Theory Comput. 11:41410–18
    [Google Scholar]
  3. 3.  Akke M. 2002. NMR methods for characterizing microsecond to millisecond dynamics in recognition and catalysis. Curr. Opin. Struct. Biol. 12:5642–47
    [Google Scholar]
  4. 4.  Ali A, Bandaranayake RM, Cai Y, King NM, Kolli M et al. 2010. Molecular basis for drug resistance in HIV-1 protease. Viruses 2:112509–35
    [Google Scholar]
  5. 5.  Aramini JM, Vorobiev SM, Tuberty LM, Janjua H, Campbell ET et al. 2015. The RAS-binding domain of human BRAF protein serine/threonine kinase exhibits allosteric conformational changes upon binding HRAS. Structure 23:81382–93
    [Google Scholar]
  6. 6.  Bale JB, Gonen S, Liu Y, Sheffler W, Ellis D et al. 2016. Accurate design of megadalton-scale two-component icosahedral protein complexes. Science 353:6297389–94
    [Google Scholar]
  7. 7.  Ball P. 2008. Water as an active constituent in cell biology. Chem. Rev. 108:74–108
    [Google Scholar]
  8. 8.  Baron R, McCammon JA 2013. Molecular recognition and ligand association. Annu. Rev. Phys. Chem. 64:151–75
    [Google Scholar]
  9. 9.  Barratt E, Bingham RJ, Warner DJ, Laughton CA, Phillips SEV, Homans SW 2005. Van der Waals interactions dominate ligand–protein association in a protein binding site occluded from solvent water. J. Am. Chem. Soc. 127:11827–34
    [Google Scholar]
  10. 10.  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. 397:41042–54
    [Google Scholar]
  11. 11.  Betz M, Wulsdorf T, Krimmer SG, Klebe G 2016. Impact of surface water layers on protein–ligand binding: How well are experimental data reproduced by molecular dynamics simulations in a thermolysin test case. ? J. Chem. Inf. Model. 56:1223–33
    [Google Scholar]
  12. 12.  Biela A, Nasief NN, Betz M, Heine A, Hangauer D, 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. 52:1822–28
    [Google Scholar]
  13. 13.  Biela A, Sielaff F, Terwesten F, Heine A, Steinmetzer T, Klebe G 2012. Ligand binding stepwise disrupts water network in thrombin: Enthalpic and entropic changes reveal classical hydrophobic effect. J. Med. Chem. 55:6094–110
    [Google Scholar]
  14. 14.  Bingham RJ, Findlay JBC, Hsieh S-Y, Kalverda AP, Kjellberg A et al. 2004. Thermodynamics of binding of 2-methoxy-3-isopropylpyrazine and 2-methoxy-3-isobutylpyrazine to the major urinary protein. J. Am. Chem. Soc. 126:1675–81
    [Google Scholar]
  15. 15.  Blasie CA, Berg JM 2004. Entropy–enthalpy compensation in ionic interactions probed in a zinc finger peptide. Biochemistry 43:3210600–4
    [Google Scholar]
  16. 16.  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. 405:51170–87
    [Google Scholar]
  17. 17.  Breiten B, Lockett MR, Sherman W, Fujita S, Al-Sayah M et al. 2013. Water networks contribute to enthalpy/entropy compensation in protein–ligand binding. J. Am. Chem. Soc. 135:15579–84
    [Google Scholar]
  18. 18.  Carter M, Voth AR, Scholfield MR, Rummel B, Sowers LC, Ho PS 2013. Enthalpy–entropy compensation in biomolecular halogen bonds measured in DNA junctions. Biochemistry 52:294891–903
    [Google Scholar]
  19. 19.  Chang C-a, Chen W, Gilson MK 2007. Ligand configurational entropy and protein binding. PNAS 104:51534–39
    [Google Scholar]
  20. 20.  Chen D, Oezguen N, Urvil P, Ferguson C, Dann SM, Savidge TC 2016. Regulation of protein-ligand binding affinity by hydrogen bond pairing. Sci. Adv. 2:3e1501240
    [Google Scholar]
  21. 21.  Chodera JD, Mobley DL 2013. Entropy-enthalpy compensation: role and ramifications in biomolecular ligand recognition and design. Annu. Rev. Biophys. 42:121–42
    [Google Scholar]
  22. 22.  Christianson DW, Fierke CA 1996. Carbonic anhydrase: evolution of the zinc binding site by nature and by design. Acc. Chem. Res. 29:331–39
    [Google Scholar]
  23. 23.  Cooper A, Johnson CM, Lakey JH, Nöllmann M 2011. 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. 93:2–3215–30
    [Google Scholar]
  24. 24.  Cornish-Bowden A. 2002. Enthalpy–entropy compensation: a phantom phenomenon. J. Biosci. 27:2121–26
    [Google Scholar]
  25. 25.  De Vivo M, Masetti M, Bottegoni G, Cavalli A 2016. Role of molecular dynamics and related methods in drug discovery. J. Med. Chem. 59:94035–61
    [Google Scholar]
  26. 26.  Dunitz JD. 1995. Win some, lose some: enthalpy–entropy compensation in weak intermolecular interactions. Chem. Biol. 2:709–12
    [Google Scholar]
  27. 27.  Elliott JR, Lira CT 2012. Introductory Chemical Engineering Thermodynamics Prentice Hall Int. Ser. Phys. Chem. Eng. Sci Upper Saddle River, NJ: Pearson, 2nd ed..
    [Google Scholar]
  28. 28.  Englert L, Biela A, Zayed M, Heine A, Hangauer D, Klebe G 2010. Displacement of disordered water molecules from hydrophobic pocket creates enthalpic signature: binding of phosphonamidate to the S1′-pocket of thermolysin. Biochim. Biophys. Acta Gen. Subj. 1800:1192–202
    [Google Scholar]
  29. 29.  Eriksson AE, Kylsten PM, Jones TA, Liljas A 1988. Crystallographic studies of inhibitor binding sites in human carbonic anhydrase II: a pentacoordinated binding of the SCN ion to the zinc at high pH. Proteins 4:283–93
    [Google Scholar]
  30. 30.  Feig M, Brooks CL III 2004. Recent advances in the development and application of implicit solvent models in biomolecule simulations. Curr. Opin. Struct. Biol. 14:2217–24
    [Google Scholar]
  31. 31.  Fenley AT, Muddana HS, Gilson MK 2012. Entropy–enthalpy transduction caused by conformational shifts can obscure the forces driving protein–ligand binding. PNAS 109:4920006–11
    [Google Scholar]
  32. 32.  Fisher SZ, Kovalevsky AY, Domsic JF, Mustyakimov M, McKenna R et al. 2010. Neutron structure of human carbonic anhydrase II: implications for proton transfer. Biochemistry 49:3415–21
    [Google Scholar]
  33. 33.  Fisher SZ, Kovalevsky AY, Domsic JF, Mustyakimov M, Silverman DN et al. 2009. Preliminary joint neutron and x-ray crystallographic study of human carbonic anhydrase II. Acta Crystallogr. F 65:5495–98
    [Google Scholar]
  34. 34.  Foulkes-Murzycki JE, Rosi C, Kurt Yilmaz N, Shafer RW, Schiffer CA 2013. Cooperative effects of drug-resistance mutations in the flap region of HIV-1 protease. ACS Chem. Biol. 8:3513–18
    [Google Scholar]
  35. 35.  Fox JM, Kang K, Sastry M, Sherman W, Sankaran B et al. 2017. Water-restructuring mutations can reverse the thermodynamic signature of ligand binding to human carbonic anhydrase. Angew. Chem. Int. Ed. 56:143833–37
    [Google Scholar]
  36. 36.  Fox JM, Kang K, Sherman W, Héroux A, Sastry G et al. 2015. Interactions between Hofmeister anions and the binding pocket of a protein. J. Am. Chem. Soc. 137:113859–66
    [Google Scholar]
  37. 37.  Frank HS, Evans MW 1945. Free volume and entropy in condensed systems III. Entropy in binary liquid mixtures; partial molal entropy in dilute solutions; structure and thermodynamics in aqueous electrolytes. J. Chem. Phys. 13:11507–32
    [Google Scholar]
  38. 38.  Frauenfelder H, Sligar SG, Wolynes PG 1991. The energy landscapes and motions of proteins. Science 254:50381598–603
    [Google Scholar]
  39. 39.  Frederick KK, Marlow MS, Valentine KG, Wand AJ 2007. Conformational entropy in molecular recognition by proteins. Nature 448:7151325–29
    [Google Scholar]
  40. 40.  Furuhashi M, Hotamisligil GS 2008. Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets. Nat. Rev. Drug Discov. 7:6489–503
    [Google Scholar]
  41. 41.  Gerstein M, Levitt M 1998. Simulating water and the molecules of life. Sci. Am. 279:5100–105
    [Google Scholar]
  42. 42.  Gray JJ, Moughon S, Wang C, Schueler-Furman O, Kuhlman B et al. 2003. Protein–protein docking with simultaneous optimization of rigid-body displacement and side-chain conformations. J. Mol. Biol. 331:1281–99
    [Google Scholar]
  43. 43.  Hanhoff T, Lücke C, Spener F 2002. Insights into binding of fatty acids by fatty acid binding proteins. Mol. Cell. Biochem. 239:1–245–54
    [Google Scholar]
  44. 44.  Hann MM, Keserü GM 2012. Finding the sweet spot: the role of nature and nurture in medicinal chemistry. Nat. Rev. Drug Discov. 11:5355–65
    [Google Scholar]
  45. 45.  Homans SW. 2007. Water, water everywhere—except where it matters. ? Drug Discov. Today 12:534–39
    [Google Scholar]
  46. 46.  Hornak V, Okur A, Rizzo RC, Simmerling C 2006. HIV-1 protease flaps spontaneously open and reclose in molecular dynamics simulations. PNAS 103:4915–20
    [Google Scholar]
  47. 47.  Huang Y, Liu Z 2013. Do intrinsically disordered proteins possess high specificity in protein–protein interactions. ? Chem. Eur. J. 19:144462–67
    [Google Scholar]
  48. 48.  Jorgensen WL. 1991. Rusting of the lock and key model for protein-ligand binding. Science 254:5034954–55
    [Google Scholar]
  49. 49.  Kamath P, Huntington JA, Krishnaswamy S 2010. Ligand binding shuttles thrombin along a continuum of zymogen- and proteinase-like states. J. Biol. Chem. 285:3728651–58
    [Google Scholar]
  50. 50.  Kandeel M, Kitade Y 2010. Substrate specificity and nucleotides binding properties of NM23H2/nucleoside diphosphate kinase homolog from plasmodium falciparum. J. Bioenerg. Biomembr. 42:5361–69
    [Google Scholar]
  51. 51.  Kandeel M, Kitade Y 2011. Binding dynamics and energetic insight into the molecular forces driving nucleotide binding by guanylate kinase. J. Mol. Recognit. 24:2322–32
    [Google Scholar]
  52. 52.  Kauzmann W. 1959. Some factors in the interpretation of protein denaturation. Adv. Protein Chem. 14:1–63
    [Google Scholar]
  53. 53.  King NM, Prabu-Jeyabalan M, Bandaranayake RM, Nalam MNL, Nalivaika EA et al. 2012. Extreme entropy–enthalpy compensation in a drug-resistant variant of HIV-1 protease. ACS Chem. Biol. 7:91536–46
    [Google Scholar]
  54. 54.  Klebe G. 2015. Applying thermodynamic profiling in lead finding and optimization. Nat. Rev. Drug Discov. 14:295–110
    [Google Scholar]
  55. 55.  Korth M. 2013. A quantum chemical view of enthalpy–entropy compensation. MedChemComm 4:61025
    [Google Scholar]
  56. 56.  Krimmer SG, Betz M, Heine A, Klebe G 2014. Methyl, ethyl, propyl, butyl: futile but not for water, as the correlation of structure and thermodynamic signature shows in a congeneric series of thermolysin inhibitors. Chem. Med. Chem. 9:4833–46
    [Google Scholar]
  57. 57.  Krimmer SG, Cramer J, Betz M, Fridh V, Karlsson R et al. 2016. Rational design of thermodynamic and kinetic binding profiles by optimizing surface water networks coating protein-bound ligands. J. Med. Chem. 59:2310530–48
    [Google Scholar]
  58. 58.  Krintel C, Francotte P, Pickering DS, Juknaite L, Pohlsgaard J et al. 2016. Enthalpy-entropy compensation in the binding of modulators at ionotropic glutamate receptor GluA2. Biophys. J. 110:112397–406
    [Google Scholar]
  59. 59.  Krishnamurthy VM, Bohall BR, Semetey V, Whitesides GM 2006. The paradoxical thermodynamic basis for the interaction of ethylene glycol, glycine, and sarcosine chains with bovine carbonic anhydrase II: an unexpected manifestation of enthalpy/entropy compensation. J. Am. Chem. Soc. 128:175802–12
    [Google Scholar]
  60. 60.  Krishnamurthy VM, Kaufman GK, Urbach AR, Gitlin I, Gudiksen KL et al. 2008. Carbonic anhydrase as a model for biophysical and physical-organic studies of proteins and protein–ligand binding. Chem. Rev. 108:946–1051
    [Google Scholar]
  61. 61.  Laage D, Stirnemann G, Hynes JT 2009. Why water reorientation slows without iceberg formation around hydrophobic solutes. J. Phys. Chem. B. 113:82428–35
    [Google Scholar]
  62. 62.  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 Des. 69:6413–22
    [Google Scholar]
  63. 63.  Lai B, Nagy G, Garate JA, Oostenbrink C 2014. Entropic and enthalpic contributions to stereospecific ligand binding from enhanced sampling methods. J. Chem. Inf. Model. 54:1151–58
    [Google Scholar]
  64. 64.  Lam SY, Yeung RCY, Yu T-H, Sze K-H, Wong K-B 2011. A rigidifying salt-bridge favors the activity of thermophilic enzyme at high temperatures at the expense of low-temperature activity. PLOS Biol 9:3e1001027
    [Google Scholar]
  65. 65.  Levy Y, Onuchic JN 2006. Water mediation in protein folding and molecular recognition. Annu. Rev. Biophys. Biomol. Struct. 35:389–415
    [Google Scholar]
  66. 66.  Li M, Schlesiger S, Knauer SK, Schmuck C 2016. Introduction of a tailor made anion receptor into the side chain of small peptides allows fine-tuning the thermodynamic signature of peptide–DNA binding. Org. Biomol. Chem. 14:8800–3
    [Google Scholar]
  67. 67.  Liebschner D, Dauter M, Brzuszkiewicz A, Dauter Z 2013. On the reproducibility of protein crystal structures: five atomic resolution structures of trypsin. Acta Crystallogr. D 69:81447–62
    [Google Scholar]
  68. 68.  Lim S, Chen B, Kariolis MS, Dimov IK, Baer TM, Cochran JR 2017. Engineering high affinity protein–protein interactions using a high-throughput microcapillary array platform. ACS Chem. Biol. 12:2336–41
    [Google Scholar]
  69. 69.  Link KH, Breaker RR 2009. Engineering ligand-responsive gene-control elements: lessons learned from natural riboswitches. Gene Ther 16:101189–201
    [Google Scholar]
  70. 70.  Liu L, Guo Q-X 2001. Isokinetic relationship, isoequilibrium relationship, and enthalpy−entropy compensation. Chem. Rev. 101:3673–96
    [Google Scholar]
  71. 71.  Liu Z, Wang Y, Brunzelle J, Kovari IA, Kovari LC 2011. Nine crystal structures determine the substrate envelope of the MDR HIV-1 protease. Protein J 30:3173–83
    [Google Scholar]
  72. 72.  Lockett MR, Lange H, Breiten B, Heroux A, Sherman W et al. 2013. The binding of benzoarylsulfonamide ligands to human carbonic anhydrase is insensitive to formal fluorination of the ligand. Angew. Chem. Int. Ed. 52:307714–17
    [Google Scholar]
  73. 73.  Lonhienne T, Gerday C, Feller G 2000. Psychrophilic enzymes: revisiting the thermodynamic parameters of activation may explain local flexibility. Biochim. Biophys. Acta Protein Struct. Mol. Enzymol. 1543:11–10
    [Google Scholar]
  74. 74.  Lv Z, Chu Y, Wang Y 2015. HIV protease inhibitors: a review of molecular selectivity and toxicity. HIV/AIDS 7:95–104
    [Google Scholar]
  75. 75.  Mantz YA, Chen B, Martyna GJ 2005. Temperature-dependent water structure: ab initio and empirical model predictions. Chem. Phys. Lett. 405:4–6294–99
    [Google Scholar]
  76. 76.  Matsuoka S, Sugiyama S, Matsuoka D, Hirose M, Lethu S et al. 2015. Water-mediated recognition of simple alkyl chains by heart-type fatty-acid-binding protein. Angew. Chem. Int. Ed. 54:51508–11
    [Google Scholar]
  77. 77.  McQuarrie DA, Simon JD 1997. Physical Chemistry: A Molecular Approach, Vol. 1 Sausalito, CA: Univ. Sci. Books
    [Google Scholar]
  78. 78.  Mecinović J, Snyder PW, Mirica KA, Bai S, Mack ET et al. 2011. Fluoroalkyl and alkyl chains have similar hydrophobicities in binding to the “hydrophobic wall” of carbonic anhydrase. J. Am. Chem. Soc. 133:3514017–26
    [Google Scholar]
  79. 79.  Mitkevich VA, Ermakov A, Kulikova AA, Tankov S, Shyp V et al. 2010. Thermodynamic characterization of ppGpp binding to EF-g or IF2 and of initiator tRNA binding to free IF2 in the presence of GDP, GTP, or ppGpp. J. Mol. Biol. 402:5838–46
    [Google Scholar]
  80. 80.  Mittermaier A, Kay LE 2006. New tools provide new insights in NMR studies of protein dynamics. Science 312:5771224–28
    [Google Scholar]
  81. 81.  Movileanu L, Schiff EA 2013. Entropy–enthalpy compensation of biomolecular systems in aqueous phase: a dry perspective. Monatshefte Chem. Chem. Mon. 144:159–65
    [Google Scholar]
  82. 82.  Myszka DG, Abdiche YN, Arisaka F, Byron O, Eisenstein E et al. 2003. The ABRF-MIRG'02 study: assembly state, thermodynamic, and kinetic analysis of an enzyme/inhibitor interaction. J. Biomol. Tech. 14:4247–69
    [Google Scholar]
  83. 83.  Nalam MNL, Ali A, Altman MD, Reddy GSKK, Chellappan S et al. 2010. Evaluating the substrate-envelope hypothesis: structural analysis of novel HIV-1 protease inhibitors designed to be robust against drug resistance. J. Virol. 84:105368–78
    [Google Scholar]
  84. 84.  Nicholson LK, Yamazaki T, Torchia DA, Grzesiek S, Bax A et al. 1995. Flexibility and function in HIV-1 protease. Nat. Struct. Biol. 2:4274–80
    [Google Scholar]
  85. 85.  Olsson TSG, Ladbury JE, Pitt WR, Williams MA 2011. Extent of enthalpy–entropy compensation in protein–ligand interactions. Protein Sci 20:91607–18
    [Google Scholar]
  86. 86.  Olsson U, Wolf-Watz M 2010. Overlap between folding and functional energy landscapes for adenylate kinase conformational change. Nat. Commun. 1:111
    [Google Scholar]
  87. 87.  Portman K, Long J, Carr S, Briand L 2014. Enthalpy/entropy compensation effects from cavity desolvation underpin broad ligand binding selectivity for rat odorant binding protein 3. Biochemistry 3:142371–79
    [Google Scholar]
  88. 88.  Prabu-Jeyabalan M, Nalivaika E, Schiffer CA 2002. Substrate shape determines specificity of recognition for HIV-1 protease: analysis of crystal structures of six substrate complexes. Structure 10:3369–81
    [Google Scholar]
  89. 89.  Reichmann D, Rahat O, Albeck S, Meged R, Dym O, Schreiber G 2005. The modular architecture of protein–protein binding interfaces. PNAS 102:157–62
    [Google Scholar]
  90. 90.  Reynolds CH, Holloway MK 2011. Thermodynamics of ligand binding and efficiency. ACS Med. Chem. Lett. 2:6433–37
    [Google Scholar]
  91. 91.  Rhodes G. 2006. Crystallography Made Crystal Clear New York: Elsevier Inc, 3rd ed..
    [Google Scholar]
  92. 92.  Ruehmann E, Betz M, Heine A, Klebe G 2015. Fragments can bind either more enthalpy or entropy-driven: crystal structures and residual hydration pattern suggest why. J. Med. Chem. 58:6960–71
    [Google Scholar]
  93. 93.  Ryde U. 2014. A fundamental view of enthalpy–entropy compensation. MedChemComm 5:91324
    [Google Scholar]
  94. 94.  Sacco C, Skowronsky RA, Gade S, Kenney JM, Spuches AM 2012. Calorimetric investigation of copper(II) binding to Aβ peptides: thermodynamics of coordination plasticity. J. Biol. Inorg. Chem. 17:4531–41
    [Google Scholar]
  95. 95.  Saito K, Hamano K, Nakagawa M, Yugawa K, Muraoka J et al. 2011. Conformational analysis of human serum albumin and its non-enzymatic glycation products using monoclonal antibodies. J. Biochem. 149:5569–80
    [Google Scholar]
  96. 96.  Sandler SI. 2006. Chemical, Biochemical, and Engineering Thermodynamics Hoboken, NJ: John Wiley & Sons, 4th ed..
    [Google Scholar]
  97. 97.  Searle MS, Westwell MS, Williams DH 1995. Application of a generalised enthalpy–entropy relationship to binding co-operativity and weak associations in solution. J. Chem. Soc. Perkin Trans 1:141–51
    [Google Scholar]
  98. 98.  Sharp K. 2001. Entropy–enthalpy compensation: fact or artifact. ? Protein Sci 10:661–67
    [Google Scholar]
  99. 99.  Siddiqui KS, Cavicchioli R 2006. Cold-adapted enzymes. Annu. Rev. Biochem. 75:403–33
    [Google Scholar]
  100. 100.  Snyder PW, Lockett MR, Moustakas DT, Whitesides GM 2013. Is it the shape of the cavity, or the shape of the water in the cavity. ? Eur. Phys. J. Spec. Top. 223:5853–91
    [Google Scholar]
  101. 101.  Snyder PW, Mecinovic J, Moustakas DT, Thomas SW III, Harder M et al. 2011. Mechanism of the hydrophobic effect in the biomolecular recognition of arylsulfonamides by carbonic anhydrase. PNAS 108:4417889–94
    [Google Scholar]
  102. 102.  Starikov EB, Nordén B 2007. Enthalpy–entropy compensation: a phantom or something useful. ? J. Phys. Chem. B 111:5114431–35
    [Google Scholar]
  103. 103.  Storch J, McDermott L 2009. Structural and functional analysis of fatty acid-binding proteins. J. Lipid Res. 50:Suppl.S126–31
    [Google Scholar]
  104. 104.  Syme NR, Dennis C, Phillips SEV, Homans SW 2007. Origin of heat capacity changes in a “nonclassical” hydrophobic interaction. ChemBioChem 8:131509–11
    [Google Scholar]
  105. 105.  Tanford C. 1979. Interfacial free energy and the hydrophobic effect. PNAS 76:94175–76
    [Google Scholar]
  106. 106.  Tellinghuisen J, Chodera JD 2011. Systematic errors in isothermal titration calorimetry: concentrations and baselines. Anal. Biochem. 414:2297–99
    [Google Scholar]
  107. 107.  Thomas K, Haapalainen AM, Burgos ES, Evans GB, Tyler PC et al. 2012. Femtomolar inhibitors bind to 5′-methylthioadenosine nucleosidases with favorable enthalpy and entropy. Biochemistry 51:387541–50
    [Google Scholar]
  108. 108.  Trbovic N, Cho JH, Abel R, Friesner RA, Rance M, Palmer AG 2009. Protein side-chain dynamics and residual conformational entropy. J. Am. Chem. Soc. 131:2615–22
    [Google Scholar]
  109. 109.  Treuheit NA, Beach MA, Komives EA 2011. Thermodynamic compensation upon binding to exosite 1 and the active site of thrombin. Biochemistry 50:214590–96
    [Google Scholar]
  110. 110.  Tzeng S-R, Kalodimos CG 2012. Protein activity regulation by conformational entropy. Nature 488:7410236–40
    [Google Scholar]
  111. 111.  Wand AJ, Moorman VR, Harpole KW 2013. A surprising role for conformational entropy in protein function. Top. Curr. Chem. 337:69–94
    [Google Scholar]
  112. 112.  Watson JD, Baker TA, Bell SP, Gann A, Levine M, Losick R 2003. Molecular Biology of the Gene Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press
    [Google Scholar]
  113. 113.  Whitesides GM. 2016. Physical-organic chemistry: a Swiss Army knife. Isr. J. Chem. 56:66–82
    [Google Scholar]
  114. 114.  Whitesides GM, Krishnamurthy VM 2005. Designing ligands to bind proteins. Q. Rev. Biophys. 38:385–95
    [Google Scholar]
  115. 115.  Williams PA, Cosme J, Sridhar V, Johnson EF, McRee DE 2000. Mammalian microsomal cytochrome p450 monooxygenase: structural adaptations for membrane binding and functional diversity. Mol. Cell 5:1121–31
    [Google Scholar]
  116. 116.  Zhang J, Jones CP, Ferré-D'Amaré AR 2014. Global analysis of riboswitches by small-angle X-ray scattering and calorimetry. Biochim. Biophys. Acta 1839:101020–29
    [Google Scholar]
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