Combining in silico tools and NMR data to validate protein-ligand structural models: Application to matrix metalloproteinases

Journal of Medicinal Chemistry

Volumn 48, Issue 24, 2005, Pages 7544-7559

  Bertini, Ivano ^a   Fragai, Marco ^a   Giachetti, Andrea ^a,b   Luchinat, Claudio ^a   Maletta, Massimiliano ^a   Parigi, Giacomo ^a   Yeo, Kwon Joo ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b ProtEra Srl   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

2 MERCAPTOMETHYL 4 METHYLPENTANOYLPHENYLALANYLALANINAMIDE; ACTINONIN; COLLAGENASE; ILOMASTAT; LIGAND; MACROPHAGE ELASTASE; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE INHIBITOR; N ISOBUTYL N (4 METHYLOXYPHENYLSULFONYL)GLYCYLHYDROXAMIC ACID; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CALCULATION; COMPUTER MODEL; HETERONUCLEAR SINGLE QUANTUM COHERENCE; MACROPHAGE; NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SPECTROSCOPY; STRUCTURE ANALYSIS; VALIDATION PROCESS; X RAY;

ALANINE; BINDING SITES; DIPEPTIDES; GLYCINE; HUMANS; HYDROXAMIC ACIDS; LIGANDS; MAGNETIC RESONANCE SPECTROSCOPY; MATRIX METALLOPROTEINASE 1; MATRIX METALLOPROTEINASE 12; MATRIX METALLOPROTEINASES; METALLOENDOPEPTIDASES; MODELS, MOLECULAR; MOLECULAR CONFORMATION; PROLINE;

EID: 28144451811     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm050574k     Document Type: Article

References (58)

1. Anderson A. C. The Process of Structure-Based Drug Design. Chem. Biol. 2003, 10, 787-797.
2. Blundell, T. L.; Jhoti, H.; Abell, C. High-throughput crystallography for lead discovery in drug design. Mit. Rev. Drug Discovery 2002, 1, 45-54.
3. Lepre, C. A.; Moore, J. M.; Peng, J. W. Theory and Applications of NMR-Based Screening in Pharmaceutical Research. Chem. Rev. 2004, 104, 3641-3675.
4. Pellecchia, M.; Becattini, B.; Crowell, K. J.; Fattorusso, R.; Forino, M.; Fragai, M.; Jung, D.; Mustelin, T.; Tautz L. NMR-based techniques in the hit identification and optimisation processes. Exp. Opin. Ther. Targets 2004, 6, 597-611.
5. Shuker, S. B.; Hajduk, P. J.; Meadows, R. P.; Fesik, S. W. Discovering high-affinity ligands for proteins: SAR by NMR. Science 1996, 274, 1531-1534.
6. Bertini, I.; Calderone, V.; Cosenza, M.; Fragai, M.; Lee, Y.-M.; Luchinat, C.; Mangani, S.; Terni, B.; Turano, P. Conformational variability of MMPs: beyond a single 3D structure. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 5334-5339.
7. Stahl, M.; Rarey, M. Detailed Analysis of Scoring Functions for Virtual Screening. J. Med. Chem. 2001, 44, 1035-1042.
8. Cummings, M. D.; DesJarlais, R. L.; Gibbs, A. C.; Mohan, V.; Jaeger, E. P. Comparison of Automated Docking Programs as Virtual Screening Tools. J. Med. Chem. 2005, 48, 962-976.
9. Trosset, J.-Y.; Scheraga, H. A. Reaching the global minimum in docking simulations: A Monte Carlo energy minimization approach using Bezier splines. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 8011-8015.
10. McCoy, M. A.; Wyss, D. F. Spatial localization of ligand binding sites from electron current density surfaces calculated from NMR chemical shift perturbations. J. Am. Chem. Soc. 2002, 124, 11758-11763.
11. Lugovskoy, A. A.; Degterev, A. I.; Fahmy, A. F.; Zhou, P.; Gross, J. D.; Yuan, J.; Wagner, G. A Novel Approach for Characterizing Protein Ligand Complexes: Molecular Basis for Specificity of Small-Molecule BcI-2 Inhibitors. J. Am. Chem. Soc. 2002, 124, 1234-1240.
12. Pellecchia, M.; Meininger, D.; Dong, Q.; Chang, E.; Jack, R.; Sem, D. S. NMR-based structural characterization of large protein-ligand interactions. J. Biomol. NMR 2002, 22, 165-173.
13. Schieborr, U.; Vogtherr, M.; Elshorst, B.; Betz, M.; Grimme, S.; Pescatore, B.; Langer, T.; Saxena, K.; Schwalbe, H. How much NMR-Data are required for the Determination of a Protein-Ligand Complex? ChemBioChem 2005, 6, 1891-1898.
14. Woessner, J. F., Jr. Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J. 1991, 5, 2145-2154.
15. Yu, A. E.; Hewitt, R. E.; Connor, E. W.; Stetler-Stevenson, W. G. Matrix metalloproteinases: novel targets for directed cancer therapy. Drugs Aging 1997, 11, 229-244.
16. Whittaker, M.; Floyd, C. D.; Brown, P.; Gearing, A. J. Design and Therapeutic Application of Matrix Metalloproteinase Inhibitors. Chem. Rev. 1999, 99, 2735-2776.
17. Clendeninn, N. J.; Appelt, K. Metalloproteinase Inhibitors in Cancer Therapy; Humana Press: Totowa, NJ, 2001.
18. Maeda, A.; Sobel, R. A. Matrix metalloproteinases in the normal human nervous system, microglial nodules, and multiple sclerosis lesions. J. Neuropathol. Exp. Neurol. 1996, 55, 300-309.
19. Mitton-Fry, R. M.; Anderson, E. M.; Hughes, T. R.; Lundblad, V.; Wuttke, D. S. Conserved Structure for Single-Stranded Telomeric DNA Recognition. Science 2002, 296, 145-147.
20. Clore, G. M.; Schwieters, C. D. Docking of Protein-Protein Complexes on the Basis of Highly Ambiguous Intermolecular Distance Restraints Derived from 1HN/15N Chemical Shift Mapping and Backbone 15N-1H Residual Dipolar Couplings Using Conjoined Rigid Body/Torsion Angle Dynamics. J. Am. Chem. Soc. 2003, 125, 2902-2912.
21. Hu, X.; Shelver, W. H. Docking studies of matrix metalloproteinase inhibitors: zinc parameter optimization to improve the binding free energy prediction. J. Mol. Graphics Modell. 2003, 22, 115-126.
22. MacPherson, L. J.; Bayburt, E. K.; Capparelli, M. P.; Carroll, B. J.; Goldstein, R.; Justice, M. R.; Zhu, L.; Hu, S.; Melton, R. A.; Fryer, L.; Goldberg, R. L.; Doughty, J. R.; Spirito, S.; Blancuzzi, V.; Wilson, D.; O'Byrne, E. M.; Ganu, V.; Parker, D. T. Discovery of CGS 27023A, a nonpeptidic, potent, and orally active stromelysin inhibitor that blocks cartilage degradation in rabbits. J. Med. Chem. 1997, 40, 2525-2532.
23. Bertini, I.; Calderone, V.; Fragai, M.; Luchinat, C.; Mangani, S.; Terni, B. X-ray structures of ternary enzyme-product-inhibitor complexes of MMP. Angew. Chem., Int. Ed. 2003, 42, 2673-2676.
24. Lovejoy, B.; Hassell, A. M.; Luther, M. A.; Weigl, D.; Jordan, S. R. Crystal Structures of Recombinant 19-kDa Human Fibroblast Collagenase Complexed to Itself. Biochemistry 1994, 33, 8207-8217.
25. Chen, D. Z.; Patel, D. V.; Hackbarth, C. J.; Wang, W.; Dreyer, G.; Young, D. C.; Margolis, P. S.; Wu, C.; Ni, Z.-J.; Trias, J.; White, R. J.; Yuan, Z. Actiononin, a Naturally Occurring Antibacterial Agent, Is a Potent Deformylase Inhibitor. Biochemistry 2000, 39, 1256-1262.
26. BIOMOL Research Laboratories data (www.biomol.com), 2005.
27. Yamamoto, M.; Tsujishita, H.; Hori, N.; Ohishi, Y.; Inoue, S.; Ikeda, S.; Okada, Y. Inhibition of Membrane-Type 1 Matrix Matalloproteinase by Hydroxamate Inhibitors: An Examination of the subsite pocket. J. Med. Chem. 1998, 41, 1209-1217.
28. van Dijk, A. D. J.; Boelens, R.; and Bonvin, A. M. J. J. Data-driven docking for the study of biomolecular complexes. FEBS J. 2005, 272, 293-312.
29. Fradera, X.; Mestres, J. Guided Docking Approaches to Structure-Based Design and Screening. Curr. Top. Med. Chem. 2004, 4, 687-700.
30. Ota, N.; Agard, D. A. Binding Mode Prediction for a Flexible Ligand in a Flexible Pocket using Multi-Conformation Simulated Annealing Pseudo Crystallographic Refinement. J. Mol. Biol. 2001, 314, 607-617.
31. Taylor, R. D.; Jewsbury, P. J.; Essex, J. W. A review of protein-small molecule docking methods. J. Comput.-Aided Mol. Des. 2002, 16, 151-166.
32. Perola, E.; Walters, W. P.; Charifson, P. S. A detailed comparison of current docking and scoring methods on systems of pharmaceutical relevance. Proteins 2004, 56, 235-249.
33. Kellenberger, E.; Rodrigo, J.; Muller, P.; Rognan, D. Comparative evaluation of eight docking tools for docking and virtual screening accuracy. Proteins 2004, 57, 225-242.
34. Carlson, H. A. Protein flexibility and drug design: how to hit a moving target. Curr. Opin. Chem. Biol. 2002, 6, 447-452.
35. Gervasio, F. L.; Laio, A.; Parrinello, M. Flexible docking in solution using metadynamics. J. Am. Chem. Soc. 2005, 127, 2600-2607.
36. Maurer, M. C.; Trosset, J. Y.; Lester, C. C.; DiBella, E. E.; Scheraga, H. A. New general approach for determining the solution structure of a ligand bound weakly to a receptor: structure of a fibrinogen Aα-like peptide bound to thrombin-(S195A) obtained using NOE distance constraints and an ECEPP/3 flexible docking program. Proteins: Struct., Funct., Genet. 1999, 34, 29-48.
37. Vogtherr, M.; Fiebig, K. NMR-based screening methods for lead discovery. EXS 2003, 93, 183-202.
38. Zabell, A. P. Z.; Post, C. B. Docking multiple conformations of a flexible ligand into a protein binding site using NMR restraints. Proteins: Struct., Funct., Genet. 2002, 46, 295-307.
39. Hajduk, P. J.; Mack, J. C.; Olejniczak, E. T.; Park, C.; Dandliker, P. J.; Beutel, B. A. SOS-NMR: A saturation transfer NMR-based method for determining the structures of protein-ligand complexes. J. Am. Chem. Soc. 2004, 126, 2390-2398.
40. Hu, X.; Balaz, S.; Shelver, W. H. A practical approach to docking of zinc metalloproteinase inhibitors. J. Mol. Graphics Modell. 2004, 22, 293-307.
41. Moy, F. J.; Pisano, M. R.; Chanda, P. K.; Urbano, C.; Killar, L. M1; Sung, M. L.; Powers, R. Asseignments, secondary structure and dynamics of the inhibitor-free catalytic fragment of human fibroblast collagenase. J. Biomol. NMR 1997, 10, 9-19.
42. Moy, F. J.; Chanda, P. K.; Chen, J. M.; Cosmi, S.; Edris, W.; Skotnicki, J. S.; Wilhelm, J.; Powers, R. NMR Solution Structure of the Catalytic Fragment of Human Fibroblast Collagenase Complexed with a Sulfonamide Derivative of a Hydroxamic Acid Compound. Biochemistry 1999, 38, 7085-7096.
43. Wasserman, Z. R. Making a New Turn in Matrix Metalloprotease Inhibition. Chem. Biol. 2005, 12, 143-148.
44. Clore, G. M. Accurate and rapid docking of protein-protein complexes on the basis of intermolecular nuclear overhauser enhancement data and dipolar couplings by rigid body minimization. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 9021-9025.
45. Clore, G. M.; Bewley, C. A. Using Conjoined Rigid Body/Torsion Angle Simulated Annealing to Determine the Relative Orientation of Covalently Linked Protein Domains from Dipolar Couplings. J. Magn. Reson. 2002, 154, 329-335.
46. Jain, N. U.; Wyckoff, T. J. O.; Raetz, C. R. H.; Prestegard, J. H. Rapid Analysis of Large Protein-Protein Complexes Using NMR-derived Orientational Constraints: The 95 kDa Complex of LpxA with Acyl Carrier Protein. J. Mol. Biol. 2004, 343, 1379-1389.
47. Crowley, P. B.; Otting, G.; Schlarb-Ridley, B.; Canters, G. W.; Ubbink, M. Hydrophobic interactions in a cyanobacterial plastocyanin-cytochrome f complex. J. Am. Chem. Soc. 2001, 123, 10444-10453.
48. Banci, L.; Bertini, I.; Cavallaro, G.; Giachetti, A.; Luchinat, C.; Parigi, G. Paramagnetism-based restraints for Xplor-NIH. J. Biomol. NMR 2004, 28, 249-261.
49. Palmer, A. G., III; Cavanagh, J.; Wright, P. E.; Rance, M. J. Magn. Reson. 1991, 93, 151-170.
50. Schleucher, J.; Schwendinger, M.; Sattler, M.; Schmidt, P.; Schedletzky, O.; Glaser, S. J.; Sørensen, O. W.; Griesinger, C. A general enhancement scheme in heteronuclear multidimensional NMR employing pulsed field gradients. J. Biomol. NMR 1994, 4, 301-306.
51. Bartels, C.; Xia, T. H.; Billeter, M.; Güntert, P.; Wüthrich, K. The program XEASY for computer-supported NMR. J. Biomol. NMR 1995, 5, 1-10.
52. Morris, G. M.; Goodsell, D. S.; Halliday, R. S.; Huey, R.; Hart, W. E.; Belew, R. K.; Olson, A. J. Automated docking using a lamarckian genetic algorithm and empirical binding free energy function. J. Comput. Chem. 1998, 19, 1639-1662.
53. Dewar, M. J. S.; Zoebisch, E. G.; Healy, E. F.; Stewart, J. J. P. AMI: a new general purpose quantum mechanical molecular model. J. Am. Chem. Soc. 1985, 107, 3902-3909.
54. Gasteiger, J.; Marsili, M. Iterative Partial Equalization of Orbital Electronegativity-A Rapid Access to Atomic Charges. Tetrahedron 1980, 36, 3219-3228.
55. Schwieters, C. D.; Kuszewski, J.; Tjandra, N.; Clore, G. M. The Xplor-NIH NMR molecular structure determination package. J. Magn. Reson. 2003, 160, 65-73.
56. Schwieters, C. D.; Clore, G. M. Internal Coordinates for Molecular Dynamics and Minimization in Structure Determination and Refinement. J. Magn. Reson. 2001, 152, 288-302.
57. Kleywegt, G. J.; Jones, T. A. Methods Enzymol. 1997, 277, 208-230.
58. MacKerell, A. D., Jr.; Wiòrkiewicz-Kuczera, J.; Karplus, M. An All-Atom Empirical Energy Function for the simulation of Nucleic Acids. J. Am. Chem. Soc. 1995, 117, 11946-11975.