Congeneric but still distinct: How closely related trypsin ligands exhibit different thermodynamic and structural properties

Journal of Molecular Biology

Volumn 405, Issue 5, 2011, Pages 1170-1187

  Brandt, Tobias ^a   Holzmann, Nicole ^a   Muley, Laveena ^b   Khayat, Maan ^b   Wegscheid Gerlach, Christof ^a   Baum, Bernhard ^a   Heine, Andreas ^a   Hangauer, David ^b   Klebe, Gerhard ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

Compensation; crystal structure analysis; enthalpy entropy; isothermal titrationcalorimetry; molecular dynamics simulations; protein ligand interactions

Indexed keywords

LIGAND; TRYPSIN; TRYPSIN INHIBITOR;

ARTICLE; COMPLEX FORMATION; CRYSTAL STRUCTURE; CRYSTALLIZATION; DISSOCIATION CONSTANT; ENTHALPY; ENTROPY; HYDROGEN BOND; HYDROPHOBICITY; INHIBITION KINETICS; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE; STOICHIOMETRY; STRUCTURE ANALYSIS; THERMODYNAMICS;

EID: 78751580378     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.11.038     Document Type: Article

References (33)

1. Bilello J.A. The agony and ecstasy of "OMIC" technologies in drug development Curr. Mol. Med. 5 2005 39 52
2. Vidalin O., Muslmani M., Estienne C., Echchakir H., and Abina A.M. In vivo target validation using gene invalidation, RNA interference and protein functional knockout models: it is the time to combine Curr. Opin. Pharmacol. 9 2009 669 676
3. Bode W., Mayr I., Baumann U., Huber R., Stone S.R., and Hofsteenge J. The refined 1.9 Å crystal structure of human alpha-thrombin: interaction with d-Phe-Pro-Arg chloromethylketone and significance of the Tyr-Pro-Pro-Trp insertion segment EMBO J. 8 1989 3467 3475
4. Ladbury J.E., Klebe G., and Freire E. Adding calorimetric data to decision making in lead discovery: a hot tip Nat. Rev. Drug Discov. 9 2010 23 27
5. Böhm H.J., Klebe G., and Kubinyi H. Wirkstoffdesign der Weg zum Arzneimittel 1996 Spektrum Akademischer Verlag Heidelberg, Germany
6. Krishnamurthy V.M., Bohall B.R., Semetey V., and Whitesides G.M. 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 2006 5802 5812
7. Copeland R.A., Pompliano D.L., and Meek T.D. Drug-target residence time and its implications for lead optimization Nat. Rev. Drug Discov. 5 2006 730 739
8. Fischer E. Einfluss der Configuration auf die Wirkung der Enzyme Ber. Dtsch. Chem. Ges. 27 1894 2985 2993
9. Koshland D.E. Application of a theory of enzyme specificity to protein synthesis Proc. Natl Acad. Sci. USA 44 1958 98 104
10. Bode W. Activation, activity and inhibition of bovine trypsin Naturwissenschaften 66 1979 251 258
11. Wang Y., Luo W., and Reiser G. Trypsin and trypsin-like proteases in the brain: proteolysis and cellular functions Cell. Mol. Life Sci. 65 2008 237 252
12. Hedstrom L. Serine protease mechanism and specificity Chem. Rev. 102 2002 4501 4524
13. Andrews P.R., Craik D.J., and Martin J.L. Functional group contributions to drug-receptor interactions J. Med. Chem. 27 1984 1648 1657
14. Kuntz I.D., Chen K., Sharp K.A., and Kollman P.A. The maximal affinity of ligands Proc. Natl Acad. Sci. USA 96 1999 9997 10002
15. Dunitz J.D. Win some, lose some: enthalpy-entropy compensation in weak intermolecular interactions Chem. Biol. 2 1995 709 712
16. Baum B., Muley L., Smolinski M., Heine A., Hangauer D., and Klebe G. Non-additivity of functional group contributions in protein-ligand binding: a comprehensive study by crystallography and isothermal titration calorimetry J. Mol. Biol. 397 2010 1042 1054
17. Leiros H.K., McSweeney S.M., and Smalas A.O. Atomic resolution structures of trypsin provide insight into structural radiation damage Acta Crystallogr. Sect. D 57 2001 488 497
18. Gerlach C., Smolinski M., Steuber H., Sotriffer C.A., Heine A., Hangauer D.G., and Klebe G. Thermodynamic inhibition profile of a cyclopentyl and a cyclohexyl derivative towards thrombin: the same but for different reasons Angew. Chem. Int. Ed. Engl. 46 2007 8511 8514
19. Sturzebecher J., Sturzebecher U., Vieweg H., Wagner G., Hauptmann J., and Markwardt F. Synthetic inhibitors of bovine factor Xa and thrombin comparison of their anticoagulant efficiency Thromb. Res. 54 1989 245 252
20. i Biochem. J. 129 1972 197 202
21. Wiseman T., Williston S., Brandts J.F., and Lin L.N. Rapid measurement of binding constants and heats of binding using a new titration calorimeter Anal. Biochem. 179 1989 131 137
22. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
23. McCoy A.J., Grosse-Kunstleve R.W., Adams P.D., Winn M.D., Storoni L.C., and Read R.J. Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674
24. Katz B.A., Elrod K., Luong C., Rice M.J., Mackman R.L., and Sprengeler P.A. A novel serine protease inhibition motif involving a multi-centered short hydrogen bonding network at the active site J. Mol. Biol. 307 2001 1451 1486
25. Dullweber F., Stubbs M.T., Musil D., Sturzebecher J., and Klebe G. Factorising ligand affinity: a combined thermodynamic and crystallographic study of trypsin and thrombin inhibition J. Mol. Biol. 313 2001 593 614
26. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., and Grosse-Kunstleve R.W. Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallogr. Sect. D 54 1998 905 921
27. Sheldrick G.M., and Schneider T.R. SHELXL: high-resolution refinement Methods Enzymol. 277 1997 319 343
28. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics Acta Crystallogr. Sect. D 60 2004 2126 2132
29. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr. Sect. D 50 1994 760 763
30. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26 1993 283 291
31. Kleywegt, G. J., Zou, J. Y., Kjeldgaard, M. & Jones, T. A. (2001). Around O. In International Tables for Crystallography: Vol. F. Crystallography of Biological Macromolecules (Rossmann, M. G., & Arnold, E., eds), vol. F, pp. 353-356, 366-367, Kluwer Academic Publishers, Dordrecht, The Netherlands.
32. McDowell L.M., McCarrick M.A., Studelska D.R., Guilford W.J., Arnaiz D., and Dallas J.L. Conformations of trypsin-bound amidine inhibitors of blood coagulant factor Xa by double REDOR NMR and MD simulations J. Med. Chem. 42 1999 3910 3918
33. Humphrey, W., Dalke, A. & Schulten, K. (1996). VMD: Visual Molecular Dynamics. J. Mol. Graphics, 14, 33-38, 27-28.