Thermodynamic profiling for fragment-based lead discovery and optimization

References

• Ferenczy GG, Keserű GM. Enthalpic efficiency of ligand binding. J Chem Inf Model. 2010;50:1536–1541.
   PubMed Web of Science ®Google Scholar
• Todd MJ, Luque I, Velázquez-Campoy A, et al. Thermodynamic basis of resistance to HIV-1 protease inhibition: calorimetric analysis of the V82F/I84V active site resistant mutant. Biochemistry. 2000;39:11876–11883.
   PubMed Web of Science ®Google Scholar
• Velazquez-Campoy A, Todd MJ, Freire E. HIV-1 protease inhibitors: enthalpic versus entropic optimization of the binding affinity. Biochemistry. 2000;39:2201–2207.
   PubMed Web of Science ®Google Scholar
• Carbonell T, Freire E. Binding thermodynamics of statins to HMG-CoA reductase. Biochemistry. 2005;44:11741–11748.
   PubMed Web of Science ®Google Scholar
• Freire E. Do enthalpy and entropy distinguish first in class from best in class? Drug Discov Today. 2008;13:869–874.
   PubMed Web of Science ®Google Scholar
• Ladbury JE, Klebe G, Freire E. Adding calorimetric data to decision making in lead discovery: a hot tip. Nat Rev Drug Discov. 2010;9:23–27.
   PubMed Web of Science ®Google Scholar
• Ferenczy GG, Keserű GM. Thermodynamics guided lead discovery and optimization. Drug Discov Today. 2010;15:919–932.
   PubMed Web of Science ®Google Scholar
• Freyer MW, Lewis EA. Isothermal titration calorimetry: experimental design, data analysis, and probing macromolecule/ligand binding and kinetic interactions. Methods Cell Biol. 2008;84:79–113.
   PubMed Web of Science ®Google Scholar
• Falconer RJ. Applications of isothermal titration calorimetry - the research and technical developments from 2011 to 2015. J Mol Recognit. 2016;29:504–515.
   PubMed Web of Science ®Google Scholar
• Tellinghuisen J. Van’t Hoff analysis of K° (T): how good … or bad? Biophys Chem. 2006;120:114–120.
   PubMed Web of Science ®Google Scholar
• Torres FE, Kuhn P, De Bruyker D, et al. Enthalpy arrays. Proc Natl Acad Sci. 2004;101:9517–9522.
   PubMed Web of Science ®Google Scholar
• Recht MI, Sridhar V, Badger J, et al. Identification and optimization of PDE10A inhibitors using fragment-based screening by nanocalorimetry and X-ray crystallography. J Biomol Screen. 2014;19:497–507.
   PubMedGoogle Scholar
• Rajarathnam K, Rösgen J. Isothermal titration calorimetry of membrane proteins — progress and challenges. Biochim Biophys Acta - Biomembr. 2014;1838:69–77.
   Web of Science ®Google Scholar
• Paketurytė V, Zubrienė A, Ladbury JE, et al. Intrinsic thermodynamics of protein-ligand binding by isothermal titration calorimetry as aid to drug design. In: Ennifar E, editor. Microcalorim. Biol. Mol. Methods Mol Biol. Humana Press, New York, NY. 2019;1964:61–74.
   PubMedGoogle Scholar
• Chodera JD, Mobley DL. Entropy-enthalpy compensation: role and ramifications in biomolecular ligand recognition and design. Annu Rev Biophys. 2013;42:121–142.
   PubMed Web of Science ®Google Scholar
• Cabani S, Gianni P, Mollica V, et al. Group contributions to the thermodynamic properties of non-ionic organic solutes in dilute aqueous solution. J Solution Chem. 1981;10:563–595.
   Web of Science ®Google Scholar
• Olsson TSG, Williams MA, Pitt WR, et al. The thermodynamics of protein-ligand interaction and solvation: insights for ligand design. J Mol Biol. 2008;384:1002–1017.
   PubMed Web of Science ®Google Scholar
• Eisenhaber F. Hydrophobic regions on protein surfaces. Derivation of the solvation energy from their area distribution in crystallographic protein structures. Protein Sci. 1996;5:1676–1686.
   PubMed Web of Science ®Google Scholar
• Walther KA, Gräter F, Dougan F, et al. Signatures of hydrophobic collapse in extended proteins captured with force spectroscopy. Proc Natl Acad Sci. 2007;104:7916–7921.
   PubMed Web of Science ®Google Scholar
• Nicholls A, Sharp KA, Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins Struct Funct Bioinforma. 1991;11:281–296.
   PubMed Web of Science ®Google Scholar
• Robertson AD, Murphy KP. Protein structure and the energetics of protein stability. Chem Rev. 2002;97:1251–1268.
   Google Scholar
• Searle MS, Williams DH. The cost of conformational order: entropy changes in molecular associations. J Am Chem Soc. 1992;114:10690–10697.
   Web of Science ®Google Scholar
• Murray CW, Verdonk ML. The consequences of translational and rotational entropy lost by small molecules on binding to proteins. J Comput Aided Mol Des. 2002;16:741–753.
   PubMed Web of Science ®Google Scholar
• Mobley DL, Gilson MK. Predicting Binding Free Energies: frontiers and Benchmarks. Annu Rev Biophys. 2017;46:531–558.
   PubMed Web of Science ®Google Scholar
• Abel R, Wang L, Mobley DL, et al. A critical review of validation, blind testing, and real- world use of alchemical protein-ligand binding free energy calculations. Curr Top Med Chem. 2017;17:2577–2585.
   PubMed Web of Science ®Google Scholar
• Wang L, Berne BJ, Friesner RA. Ligand binding to protein-binding pockets with wet and dry regions. Proc Natl Acad Sci U S A. 2011;108:1326–1330.
   PubMed Web of Science ®Google Scholar
• Lazaridis T. Inhomogeneous fluid approach to solvation thermodynamics. 1. Theory. J Phys Chem B. 1998;102:3531–3541.
   Web of Science ®Google Scholar
• Baroni M, Cruciani G, Sciabola S, et al. A common reference framework for analyzing/comparing proteins and ligands. Fingerprints for Ligands and Proteins (FLAP): theory and application. J Chem Inf Model. 2007;47:279–294.
   PubMed Web of Science ®Google Scholar
• Goodford PJ. A computational procedure for determining energetically favorable binding sites on biologically important macromolecules. J Med Chem. 1985;28:849–857.
   PubMed Web of Science ®Google Scholar
• Mason JS, Bortolato A, Weiss DR, et al. High end GPCR design: crafted ligand design and druggability analysis using protein structure, lipophilic hotspots and explicit water networks. Silico Pharmacol. 2013;1:23.
   Google Scholar
• Kamps JJAG, Huang J, Poater J, et al. Chemical basis for the recognition of trimethyllysine by epigenetic reader proteins. Nat Commun. 2015;6:8911.
   PubMed Web of Science ®Google Scholar
• Christopher JA, Orgován Z, Congreve M, et al. Structure-based optimization strategies for G Protein-Coupled Receptor (GPCR) allosteric modulators: a case study from analyses of new metabotropic glutamate receptor 5 (mGlu 5) X-ray structures. J Med Chem. 2019;62:207–222.
   PubMed Web of Science ®Google Scholar
• Biela A, Sielaff F, Terwesten F, et al. Ligand binding stepwise disrupts water network in thrombin: enthalpic and entropic changes reveal classical hydrophobic effect. J Med Chem. 2012;55:6094–6110.
   PubMed Web of Science ®Google Scholar
• Shimokhina N, Bronowska A, Homans SW. Contribution of ligand desolvation to binding thermodynamics in a ligand-protein interaction. Angew Chemie Int Ed. 2006;45:6374–6376.
   PubMed Web of Science ®Google Scholar
• Biela A, Khayat M, Tan H, et al. Impact of ligand and protein desolvation on ligand binding to the S1 pocket of thrombin. J Mol Biol. 2012;418:350–366.
   PubMed Web of Science ®Google Scholar
• Snyder PW, Mecinovic J, Moustakas DT, et al. Mechanism of the hydrophobic effect in the biomolecular recognition of arylsulfonamides by carbonic anhydrase. Proc Natl Acad Sci. 2011;108:17889–17894.
   PubMed Web of Science ®Google Scholar
• Baum B, Muley L, Smolinski M, et al. Non-additivity of functional group contributions in protein-ligand binding: A comprehensive study by crystallography and isothermal titration calorimetry. J Mol Biol. 2010;397:1042–1054.
   PubMed Web of Science ®Google Scholar
• Kazlauskas E, Petrikaitė V, Michailovienė V, et al. Thermodynamics of aryl-dihydroxyphenyl-thiadiazole binding to human Hsp90. Vertessy BG, editor. PLoS One. 2012;7:e36899.
   PubMed Web of Science ®Google Scholar
• Kišonaitė M, Zubrienė A, Čapkauskaitė E, et al. Intrinsic thermodynamics and structure correlation of benzenesulfonamides with a pyrimidine moiety binding to carbonic anhydrases I, II, VII, XII, and XIII. Khodarahmi R, editor. PLoS One. 2014;9:e114106.
   PubMed Web of Science ®Google Scholar
• Wienen-Schmidt B, Wulsdorf T, Jonker HRA, et al. On the implication of water on fragment-to-ligand growth in kinase binding thermodynamics. Chem Med Chem. 2018;13:1988–1996.
   Google Scholar
• Biela A, Nasief NN, Betz M, et al. Dissecting the hydrophobic effect on the molecular level: the role of water, enthalpy, and entropy in ligand binding to thermolysin. Angew Chemie Int Ed. 2013;52:1822–1828.
   PubMed Web of Science ®Google Scholar
• Scott AD, Phillips C, Alex A, et al. Thermodynamic optimisation in drug discovery: A case study using carbonic anhydrase inhibitors. Chem Med Chem. 2009;4:1985–1989.
   Google Scholar
• Geschwindner S, Ulander J, Johansson P. Ligand binding thermodynamics in drug discovery: still a hot tip? J Med Chem. 2015;58:6321–6335.
   PubMed Web of Science ®Google Scholar
• Klebe G. Applying thermodynamic profiling in lead finding and optimization. Nat Rev Drug Discov. 2015;14:95–110.
   PubMed Web of Science ®Google Scholar
• Teague SJ, Davis AM, Leeson PD, et al. The Design of Leadlike Combinatorial Libraries. Angew Chemie Int Ed. 1999;38:3743–3748.
   PubMed Web of Science ®Google Scholar
• Morphy R. The influence of target family and functional activity on the physicochemical properties of pre-clinical compounds. J Med Chem. 2006;49:2969–2978.
   PubMed Web of Science ®Google Scholar
• Hann MM, Leach AR, Harper G. Molecular complexity and its impact on the probability of finding leads for drug discovery. J Chem Inf Comput Sci. 2001;41:856–864.
   PubMedGoogle Scholar
• Tyrchan C, Blomberg N, Engkvist O, et al. Physicochemical property profiles of marketed drugs, clinical candidates and bioactive compounds. Bioorg Med Chem Lett. 2009;19:6943–6947.
   PubMed Web of Science ®Google Scholar
• Oprea TI, Davis AM, Teague SJ, et al. Is there a difference between leads and drugs? A historical perspective. J Chem Inf Comput Sci. 2001;41:1308–1315.
   PubMedGoogle Scholar
• Leeson PD, Springthorpe B. The influence of drug-like concepts on decision-making in medicinal chemistry. Nat Rev Drug Discov. 2007;6:881–890.
   PubMed Web of Science ®Google Scholar
• Ferenczy GG, Keser GM. The impact of binding thermodynamics on medicinal chemistry optimizations. Future Med Chem. 2015;7:1285–1303.
   Web of Science ®Google Scholar
• Kuntz ID, Chen K, Sharp KA, et al. The maximal affinity of ligands. Proc Natl Acad Sci. 1999;96:9997–10002.
   PubMed Web of Science ®Google Scholar
• Gleeson MP, Hersey A, Montanari D, et al. Probing the links between in vitro potency, ADMET and physicochemical parameters. Nat Rev Drug Discov. 2011;10:197–208.
   PubMed Web of Science ®Google Scholar
• Hann MM, Keserü GM. Finding the sweet spot: the role of nature and nurture in medicinal chemistry. Nat Rev Drug Discov. 2012;11:355–365.
   PubMed Web of Science ®Google Scholar
• Erlanson DA, Fesik SW, Hubbard RE, et al. Twenty years on: the impact of fragments on drug discovery. Nat Rev Drug Discov. 2016;15:605–619.
   PubMed Web of Science ®Google Scholar
• Lamoree B, Hubbard RE. Current perspectives in fragment-based lead discovery (FBLD). Essays Biochem. 2017;61:453–464.
   PubMed Web of Science ®Google Scholar
• Jacquemard C, Kellenberger E. A bright future for fragment-based drug discovery: what does it hold? Expert Opin Drug Discov. 2019;14:413–416.
   PubMed Web of Science ®Google Scholar
• Leach AR, Hann MM. Molecular complexity and fragment-based drug discovery: ten years on. Curr Opin Chem Biol. 2011;15:489–496.
   PubMed Web of Science ®Google Scholar
• Ferenczy GGG, Keserű GM, Keseru GM. Thermodynamics of fragment binding. J Chem Inf Model. 2012;52:1039–1045.
   PubMed Web of Science ®Google Scholar
• Giordanetto F, Jin C, Willmore L, et al. Fragment hits: what do they look like and how do they bind? J Med Chem. 2019;62:3381–3394.
   PubMed Web of Science ®Google Scholar
• Ferenczy GG, Keserű GM. On the enthalpic preference of fragment binding. Medchemcomm. 2016;7:332–337.
   Web of Science ®Google Scholar
• Williams G, Ferenczy GG, Ulander J, et al. Binding thermodynamics discriminates fragments from druglike compounds: a thermodynamic description of fragment-based drug discovery. Drug Discov Today. 2017;22:681–689.
   PubMed Web of Science ®Google Scholar
• Murray CW, Rees DC. Opportunity knocks: organic chemistry for fragment-based drug discovery (FBDD). Angew Chemie Int Ed. 2016;55:488–492.
   PubMed Web of Science ®Google Scholar
• O’Reilly M, Cleasby A, Davies TG, et al. Crystallographic screening using ultra-low-molecular-weight ligands to guide drug design. Drug Discov Today. 2019;24:1081–1086.
   PubMed Web of Science ®Google Scholar
• Ferenczy GG, Keserű GM. How are fragments optimized? A retrospective analysis of 145 fragment optimizations. J Med Chem. 2013;56:2478–2486.
   Web of Science ®Google Scholar
• Steuber H, Heine A, Podjarny A, et al. Merging the binding sites of aldose and aldehyde reductase for detection of inhibitor selectivity-determining features. J Mol Biol. 2008;379:991–1016.
   PubMed Web of Science ®Google Scholar
• Gloster TM, Macdonald JM, Tarling CA, et al. Structural, thermodynamic, and kinetic analyses of tetrahydrooxazine- derived inhibitors bound to β-glucosidases. J Biol Chem. 2004;279:49236–49242.
   PubMed Web of Science ®Google Scholar
• Mecinović J, Snyder PW, Mirica KA, et al. Fluoroalkyl and alkyl chains have similar hydrophobicities in binding to the “Hydrophobic Wall” of carbonic anhydrase. J Am Chem Soc. 2011;133:14017–14026.
   PubMed Web of Science ®Google Scholar
• Krishnamurthy VM, Kaufman GK, Urbach AR, et al. Carbonic anhydrase as a model for biophysical and physical-organic studies of proteins and protein-ligand binding. Chem Rev. 2008;108:946–1051.
   PubMed Web of Science ®Google Scholar
• Binford JS, Lindskog S, Wadsö I. A calorimetric study of the binding of sulfonamides and cyanate to carbonic anhydrase. BBA - Enzymol. 1974;341:345–356.
   PubMed Web of Science ®Google Scholar
• Protasevich II, Brouillette CG, Snow ME, et al. Role of inhibitor aliphatic chain in the thermodynamics of inhibitor binding to Escherichia coli enoyl-ACP reductase and the Phe203Leu mutant: A proposed mechanism for drug resistance. Biochemistry. 2004;43:13380–13389.
   PubMed Web of Science ®Google Scholar
• Dunford JE, Kwaasi AA, Rogers MJ, et al. Structure-activity relationships among the nitrogen containing bisphosphonates in clinical use and other analogues: time-dependent inhibition of human farnesyl pyrophosphate synthase. J Med Chem. 2008;51:2187–2195.
   PubMed Web of Science ®Google Scholar
• Balendiran GK, Schnütgen F, Scapin G, et al. Crystal structure and thermodynamic analysis of human brain fatty acid-binding protein. J Biol Chem. 2000;275:27045–27054.
   PubMed Web of Science ®Google Scholar
• Bingham RJ, Findlay JBC, Hsieh SY, et al. Thermodynamics of Binding of 2-Methoxy-3-isopropylpyrazine and 2-Methoxy-3-isobutylpyrazine to the major urinary protein. J Am Chem Soc. 2004;126:1675–1681.
   PubMed Web of Science ®Google Scholar
• Malham R, Johnstone S, Bingham RJ, et al. Strong solute-solute dispersive interactions in a protein-ligand complex. J Am Chem Soc. 2005;127:17061–17067.
   PubMed Web of Science ®Google Scholar
• Barratt E, Bronowska A, Vondrášek J, et al. Thermodynamic penalty arising from burial of a ligand polar group within a hydrophobic pocket of a protein receptor. J Mol Biol. 2006;362:994–1003.
   PubMed Web of Science ®Google Scholar
• Sharrow SD, Novotny MV, Stone MJ. Thermodynamic analysis of binding between mouse major urinary protein-I and the pheromone 2-sec-butyl-4,5-dihydrothiazole. Biochemistry. 2003;42:6302–6309.
   PubMed Web of Science ®Google Scholar
• Neumann L, Von Knig K, Ullmann D. HTS Reporter displacement assay for fragment screening and fragment evolution toward leads with optimized binding kinetics, binding selectivity, and thermodynamic signature. In: Kuo LC, editor. Methods Enzymol. Academic Press. 2011. vol. 493, p. 299–320.
   Google Scholar
• Papalia GA, Giannetti AM, Arora N, et al. Thermodynamic characterization of pyrazole and azaindole derivatives binding to p38 mitogen-activated protein kinase using Biacore T100 technology and van’t Hoff analysis. Anal Biochem. 2008;383:255–264.
   PubMed Web of Science ®Google Scholar
• Silvestre HL, Blundell TL, Abell C, et al. Integrated biophysical approach to fragment screening and validation for fragment-based lead discovery. Proc Natl Acad Sci U S A. 2013;110:12984–12989.
   PubMed Web of Science ®Google Scholar
• Scott DE, Dawes GJ, Ando M, et al. A fragment-based approach to probing adenosine recognition sites by using dynamic combinatorial chemistry. ChemBioChem. 2009;10:2772–2779.
   PubMed Web of Science ®Google Scholar
• Bullock AN, Debreczeni JÉ, Fedorov OY, et al. Structural basis of inhibitor specificity of the human protooncogene proviral insertion site in moloney murine leukemia virus (PIM-1) kinase. J Med Chem. 2005;48:7604–7614.
   PubMed Web of Science ®Google Scholar
• Dai R, Geders TW, Liu F, et al. Fragment-based exploration of binding site flexibility in mycobacterium tuberculosis BioA. J Med Chem. 2015;58:5208–5217.
   PubMed Web of Science ®Google Scholar
• Poget SF, Legge GB, Proctor MR, et al. The structure of a tunicate C-type lectin from Polyandrocarpa misakiensis complexed with D-galactose. J Mol Biol. 1999;290:867–879.
   PubMed Web of Science ®Google Scholar
• Calamini B, Santarsiero BD, Boutin JA, et al. Kinetic, thermodynamic and X-ray structural insights into the interaction of melatonin and analogues with quinone reductase 2. Biochem J. 2008;413:81–91.
   PubMed Web of Science ®Google Scholar
• Fisher BM. Coulombic effects of remote subsites on the active site of ribonuclease A. Biochemistry. 1998;37:17386–17401.
   PubMed Web of Science ®Google Scholar
• Weber PC, Pantoliano MW, Simons DM, et al. Structure-based design of synthetic azobenzene ligands for streptavidin. J Am Chem Soc. 1994;116:2717–2724.
   Web of Science ®Google Scholar
• Rühmann E, Betz M, Fricke M, et al. Thermodynamic signatures of fragment binding: validation of direct versus displacement ITC titrations. Biochim Biophys Acta Gen Subj. 2015;1850:647–656.
   Web of Science ®Google Scholar
• Perozzo R, Jelesarov I, Bosshard HR, et al. Compulsory order of substrate binding to herpes simplex virus type 1 thymidine kinase: A calorimetric study. J Biol Chem. 2000;275:16139–16145.
   PubMed Web of Science ®Google Scholar
• Terán W, Krell T, Ramos JL, et al. Effector-repressor interactions, binding of a single effector molecule to the operator-bound TtgR homodimer mediates derepression. J Biol Chem. 2006;281:7102–7109.
   PubMed Web of Science ®Google Scholar
• Dolezal O, Doughty L, Hattarki MK, et al. Fragment Screening for the Modelling Community: SPR, ITC, and Crystallography. Aust J Chem. 2013;66:1507.
   Web of Science ®Google Scholar
• Talhout R, Engberts JBFN. Thermodynamic analysis of binding of p-substituted benzamidines to trypsin. Eur J Biochem. 2001;268:1554–1560.
   PubMedGoogle Scholar
• Bertini I, Calderone V, Fragai M, et al. Exploring the subtleties of drug-receptor interactions: the case of matrix metalloproteinases. J Am Chem Soc. 2007;129:2466–2475.
   PubMed Web of Science ®Google Scholar
• Ferenczy GG, Keserű GM. Thermodynamics of Ligand Binding. Luque J, Barril X, editors. Physico-Chemical Comput. Approaches to drug discov. RSC Drug Discov. Ser. Cambridge: Royal Society of Chemistry; 2012. p. 23–79.
   Google Scholar
• Murray CW, Carr MG, Callaghan O, et al. Fragment-based drug discovery applied to hsp90. discovery of two lead series with high ligand efficiency. J Med Chem. 2010;53:5942–5955.
   PubMed Web of Science ®Google Scholar
• Torres FE, Recht MI, Coyle JE, et al. Higher throughput calorimetry: opportunities, approaches and challenges. Curr Opin Struct Biol. 2010;20:598–605.
   PubMed Web of Science ®Google Scholar