3D QSAR selectivity analyses of carbonic anhydrase inhibitors: Insights for the design of isozyme selective inhibitors

Journal of Chemical Information and Modeling

Volumn 46, Issue 6, 2006, Pages 2737-2760

  Weber, Alexander ^a,d   Böhm, Markus ^c   Supuran, Claudiu T ^e   Scozzafava, Andrea ^b   Sotriffer, Christoph A ^a   Klebe, Gerhard ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b UNIVERSITY OF FLORENCE   (Italy)

^c PFIZER GLOBAL RESEARCH AND DEVELOPMENT   (United States)

^d ALTANA PHARMA AG   (Germany)

^e NONE

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CRYSTAL STRUCTURE; DATABASE SYSTEMS; MATHEMATICAL MODELS; OPTIMIZATION; PATHOLOGY;

BINDING POCKETS; CARBONIC ANHYDRASE INHIBITORS; ISOZYME SELECTIVE INHIBITORS; QSAR SELECTIVITY;

ENZYME INHIBITION;

CARBONATE DEHYDRATASE; CARBONATE DEHYDRATASE INHIBITOR; ISOENZYME; ISOPROTEIN; LIGAND;

ANIMAL; ARTICLE; BINDING SITE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; DRUG DESIGN; HUMAN; METHODOLOGY; PH; PHARMACEUTICS; PROTEIN BINDING; PROTEIN CONFORMATION; QUANTITATIVE STRUCTURE ACTIVITY RELATION; SYNTHESIS;

ANIMALS; BINDING SITES; CARBONIC ANHYDRASE INHIBITORS; CARBONIC ANHYDRASES; CHEMISTRY, PHARMACEUTICAL; DRUG DESIGN; HUMANS; HYDROGEN-ION CONCENTRATION; ISOENZYMES; LIGANDS; MODELS, CHEMICAL; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN ISOFORMS; QUANTITATIVE STRUCTURE-ACTIVITY RELATIONSHIP; TECHNOLOGY, PHARMACEUTICAL;

EID: 33845742619     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci600298r     Document Type: Article

References (68)

1. Maren, T. H. Relations between structure and biological activity of sulfonamides. Annu. Rev. Pharmacol. Toxicol. 1976, 16, 309-327.
2. Supuran, C. T. Carbonic anhydrase inhibitors and their therapeutical potential. Exp. Opin. Ther. Patents 2000, 10, 575-600.
3. Supuran, C. T.; Scozzafava, A. Carbonic Anhydrase Inhibitors. Curr. Med. Chem.: Immun., Endocr. Metab. Agents 2001, 1, 61-97.
4. Supuran, C. T.; Scozzafava, A. Applications of carbonic anhydrase inhibitors and activators in therapy. Expert Opin. Ther. Pat. 2002, 12, 217-242.
5. Supuran, C. T.; Scozzafava, A.; Casini, A. Carbonic anhydrase inhibitors. Med. Res. Rev. 2003, 23, 146-189.
6. Chegwidden, W. R.; Carter, N. D. Introduction to the carbonic anhydrases. The Carbonic Anhydrases - New Horizons; Birkhäuser Verlag: Basel, 2000; pp 13-28.
7. Maren, T. H. Carbonic anhydrase: chemistry, physiology, and inhibition. Physiol. Rev. 1967, 47, 595-781.
8. Evans, W. O.; Robinson, S. M.; Houstman, D. H.; Jackson, R. E.; Weinkopf, R. B. Amelioration of the symptoms of acute mountain sickness by staging and acetazolamide. Aviat., Space Environ. Med. 1976, 47, 512-516.
9. Forster, P. Methazolamide in acute mountain sickness. Lancet 1982, 1, 1254.
10. Lindskog, S.; Wistrand, P. J. Inhibitors of carbonic anhydrase. Design of Enzyme Inhibitors as Drugs; Oxford University Press: 1989; pp 698-723.
11. Owa, T.; Yoshino, H.; Okauchi, T.; Yoshimatsu, K.; Ozawa, Y. et al. Discovery of novel antitumor sulfonamides targeting G1 phase of the cell cycle. J. Med. Chem. 1999, 42, 3789-3799.
12. Owa, T.; Nagasu, T. Novel sulfonamide derivatives for the treatment of cancer. Expert Opin. Ther. Pat. 2000, 10, 1725-1740.
13. Abbate, F.; Supuran, C. T.; Scozzafava, A.; Orioli, P.; Stubbs, M. T. et al. Nonaromatic sulfonamide group as an ideal anchor for potent human carbonic anhydrase inhibitors: role of hydrogen-bonding networks in ligand binding and drug design. J. Med. Chem. 2002, 45, 3583-3587.
14. Casini, A.; Scozzafava, A.; Mastrolorenzo, A.; Supuran, L. T. Sulfonamides and sulfonylated derivatives as anticancer agents. Curr. Cancer Drug Targets 2002, 2, 55-75.
15. Scozzafava, A.; Owa, T.; Mastrolorenzo, A.; Supuran, C. T. Anticancer and antiviral sulfonamides. Curr. Med. Chem. 2003, 10, 925-953.
16. Supuran, C. T. Indisulam: an anticancer sulfonamide in clinical development. Expert Opin. Invest. Drugs 2003, 12, 283-287.
17. Abbate, F.; Casini, A.; Owa, T.; Scozzafava, A.; Supuran, C. T. Carbonic anhydrase inhibitors: E7070, a sulfonamide anticancer agent, potently inhibits cytosolic isozymes I and II, and transmembrane, tumor-associated isozyme IX. Bioorg. Med. Chem. Lett. 2004, 14, 217-223.
18. Maren, T. H. The Development of Topical Carbonic Anhydrase Inhibitors. J. Glaucoma 1995, 4, 49-62.
19. Lindskog, S. Structure and mechanism of carbonic anhydrase. Pharmacol. Ther. 1997, 74, 1-20.
20. Clare, B. W.; Supuran, C. T. QSAR studies of sulfonamide carbonic anhydrase inhibitors. Carbonic Anhydrase - Its inhibitors and activators; Taylor & Francis: London & New York, 2004; pp 149-182.
21. Gerber, P. R.; Müller, K. MAB, a generally applicable molecular force field for structure modelling in medicinal chemistry. J. Comput.-Aided Mol. Des. 1995, 9, 251-268.
22. Gerber, P. R. Charge distribution from a simple molecular orbital type calculation and nonbonding interaction terms in the force field MAB. J. Comput.-Aided Mol. Des. 1998, 12, 37-51.
23. Böhm, M.; Stürzebecher, J.; Klebe, G. Three-dimensional quantitative structure-activity relationship analyses using comparative molecular field analysis and comparative molecular similarity indices analysis to elucidate selectivity differences of inhibitors binding to trypsin, thrombin, and factor Xa. J. Med. Chem. 1999, 42, 458-477.
24. Matter, H.; Schwab, W.; Barbier, D.; Billen, G.; Haase, B. et al. Quantitative structure-activity relationship of human neutrophil collagenase (MMP-8) inhibitors using comparative molecular field analysis and X-ray structure analysis. J. Med. Chem. 1999, 42, 1908-1920.
25. Matter, H.; Schwab, W. Affinity and selectivity of matrix metalloproteinase inhibitors: a chemometrical study from the perspective of ligands and proteins. J. Med. Chem. 1999, 42, 4506-4523.
26. Morris, G. M.; Goodsell, D. S.; Huey, R.; Olson, A. J. Distributed automated docking of flexible ligands to proteins: parallel applications of AutoDock 2.4. J. Comput.-Aided Mol. Des. 1996, 10, 293-304.
27. Morris, G. M.; Goodsell, D. S.; Halliday, R. S.; Huey, R.; Hart, W. E. et al. Automated Docking Using a Lamarckian Genetic Algorithm and an Empirical Binding Free Energy Function. J. Comput. Chem. 1998, 19, 1639-1662.
28. Antel, J.; Weber, A.; Sotriffer, C. A.; Klebe, G. Multiple binding modes observed in X-ray structures of carbonic anhydrase inhibitor complexes and other systems: consequenses for structure-based drug design. Carbonic Anhydrase - Its inhibitors and activators; Taylor & Francis: London & New York, 2004; pp 45-65.
29. Borras, J.; Scozzafava, A.; Menabuoni, L.; Mincione, F.; Brigand, F. et al. Carbonic anhydrase inhibitors: synthesis of water-soluble, topically effective intraocular pressure lowering aromatic/heterocyclic sulfonamides containing 8-quinoline-sulfonyl moieties: Is the tail more important than the ring? Bioorg. Med. Chem. 1999, 7, 2397-2406.
30. Casini, A.; Scozzafava, A.; Mincione, F.; Menabuoni, L.; Ilies, M. A. et al. Carbonic anhydrase inhibitors: water-soluble 4-sulfamoylphenylthioureas as topical intraocular pressure-lowering agents with longlasting effects. J. Med. Chem. 2000, 43, 4884-4892.
31. Ilies, M.; Supuran, C. T.; Scozzafava, A.; Casini, A.; Mincione, F. et al. Carbonic anhydrase inhibitors: sulfonamides incorporating furan-, thiophene- and pyrrole-carboxamido groups possess strong topical intraocular pressure lowering properties as aqueous suspensions. Bioorg. Med. Chem. 2000, 8, 2145-2155.
32. Scozzafava, A.; Briganti, F.; Mincione, G.; Menabuoni, L.; Mincione, F. et al. Carbonic anhydrase inhibitors: synthesis of water-soluble, aminoacyl/dipeptidyl sulfonamides possessing long-lasting intraocular pressure-lowering properties via the topical route. J. Med. Chem. 1999, 42, 3690-3700.
33. Scozzafava, A.; Menabuoni, L.; Mincione, F.; Briganti, F.; Mincione, G. et al. Carbonic anhydrase inhibitors. Synthesis of water-soluble, topically effective, intraocular pressure-lowering aromatic/heterocyclic sulfonamides containing cationic or anionic moieties: is the tail more important than the ring? J. Med. Chem. 1999, 42, 2641-2650.
34. Scozzafava, A.; Supuran, C. T. Carbonic anhydrase and matrix metalloproteinase inhibitors: sulfonylated amino acid hydroxamates with MMP inhibitory properties act as efficient inhibitors of CA isozymes I, II, and IV, and N- hydroxysulfonamides inhibit both these zinc enzymes. J. Med. Chem. 2000, 43, 3677-3687.
35. Scozzafava, A. Carbonic Anhydrase Inhibitors: Synthsis of N-Morpholyl-thiocarbonylsulfenylamino Aromatic/Heterocyclic Sulfonamides and their Interaction with Isozymes I, II and IV. Bioorg. Med. Chem. Lett. 2000, 10, 1117-1120.
36. Scozzafava, A.; Menabuoni, L.; Mincione, F.; Briganti, F.; Mincione, G. et al. Carbonic anhydrase inhibitors: perfluoroalkyl/aryl-substituted derivatives of aromatic/heterocyclic sulfonamides as topical intraocular pressure-lowering agents with prolonged duration of action. J. Med. Chem. 2000, 43, 4542-4551.
37. Supuran, C. T. Carbonic anhydrase inhibitors - part 70. Synthesis and ocular pharmacology of a new class of water-soluble, topically effective intraocular pressure lowering agents derived from nicotinic acid and aromatic/heterocyclic sulfonamides. Eur. J. Med. Chem. 1999, 34, 799-808.
38. Supuran, C. T.; Scozzafava, A. Carbonic anhydrase inhibitors - Part 94. 1,3,4-thiadiazole-2- sulfonamidederivatives as antitumor agents? Eur. J. Med. Chem. 2000, 35, 867-874.
39. Supuran, C. T.; Briganti, F.; Tilli, S.; Chegwidden, W. R.; Scozzafava, A. Carbonic anhydrase inhibitors: sulfonamides as antitumor agents? Bioorg. Med. Chem. 2001, 9, 703-714.
40. Thibaut, U.; Folkers, G.; Klebe, G.; Kubinyi, H.; Merz, A. et al. Recommendations for CoMFA Studies and 3D QSAR Publications. 3D QSAR in Drug Design: Theory Methods and Applications; ESCOM: Leiden, 1993; pp 711-716.
41. Berman, H. M.; Battistuz, T.; Bhat, T. N.; Bluhm, W. F.; Bourne, P. E. et al. The Protein Data Bank. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2002, 58, 899-907.
42. Berman, H. M.; Bourne, P. E.; Westbrook, J. The Protein Data Bank: A Case Study in Management of Community Data. Curr. Proteomics 2004, 1, 49-57.
43. Berman, H. M.; Westbrook, J.; Feng, Z.; Gilliland, G.; Bhat, T. N. et al. The Protein Data Bank. Nucleic Acids Res. 2000, 28, 235-242.
44. Hendlich, M.; Bergner, A.; Günther, J.; Klebe, G. Relibase: Design and Development of a Database for Comprehensive Analysis of Protein-Ligand Interactions dagger. J. Mol. Biol. 2003, 326, 607-620.
45. Günther, J.; Bergner, A.; Hendlich, M.; Klebe, G. Utilising structural knowledge in drug design strategies: applications using Relibase. J. Mol. Biol. 2003, 326, 621-636.
46. Duda, D.; Tu, C.; Qian, M.; Laipis, P.; Agbandje-McKenna, M. et al. Structural and kinetic analysis of the chemical rescue of the protontransfer function of carbonic anhydrase II. Biochemistry 2001, 40, 1741-1748.
47. Duda, D.; Govindasamy, L.; Agbandje-McKenna, M.; Tu, C.; Silverman, D. N. et al. The refined atomic structure of carbonic anhydrase II at 1.05 A resolution: implications of chemical rescue of proton transfer. Acta Crvstallogr., Sect. D: Biol. Crystallaqr. 2003, 59, 93-104.
48. Christianson, D. W.; Cox, J. D. Catalysis by metal-activated hydroxide in zinc and manganese metalloenzymes. Annu. Rev. Biochem. 1999, 68, 33-57.
49. Scolnick, L. R. Novel Binding Mode of Hydroxamate Inhibitors to Human Carbonic Anhydrase II. J. Am. Chem. Soc. 1997, 119, 850-851.
50. Cramer, R. D., III.; Patterson, D. E.; Bunce, J. D. Comparative Molecular Field Analysis (CoMFA). 1. Effect of Shape on Binding of Steroids to Carrier Proteins. J. Am. Chem. Soc. 1988, 110, 5959-5967.
51. Klebe, G. Comparative Molecular Similarity Indices Analysis: CoM-SIA. Perspect. Drug Discovery Des. 1998, 12/13/14, 87-104.
52. Smith, G. M.; Alexander, R. S.; Christianson, D. W.; McKeever, B. M.; Ponticello, G. S. et al. Positions of His-64 and a bound water in human carbonic anhydrase II upon binding three structurally related inhibitors. Protein Sci. 1994, 3, 118-125.
53. Sotriffer, C. A.; Stahl, M.; Klebe, G. The Docking Problem. Handbook of Chemoinfarmatics; Wiley-VCH: Weinheim, 2003; pp 1732-1766.
54. Masereel, B.; Rolin, S.; Abbate, F.; Scozzafava, A.; Supuran, C. T. Carbonic anhydrase inhibitors: anticonvulsant sulfonamides incorporating valproyl and other lipophilic moieties. J. Med. Chem. 2002, 45, 312-320.
55. Casini, A.; Antel, J.; Abbate, F.; Scozzafava, A.; David, S. et al. Carbonic anhydrase inhibitors: SAR and X-ray crystallographic study for the interaction of sugar sulfamates/sulfamides with isozymes I. II and IV. Bioorg. Med. Chem. Lett. 2003, 13, 841-845.
56. Maryanoff, B. E.; Costanzo, M. J.; Nortey, S. O.; Greco, M. N.; Shank, R. P. et al. Structure-activity studies on anticonvulsant sugar sulfamates related to topiramate. Enhanced potency with cyclic sulfate derivatives. J. Med. Chem. 1998, 41. 1315-1343.
57. Recacha, R.; Costanzo, M. J.; Maryanoff, B. E.; Chattopadhyay, D. Crystal structure of human carbonic anhydrase II complexed with an anti- convulsant sugar sulphamate. Biochem. J. 2002. 361, 437-441.
58. Sotriffer, C. A.; Gohlke, H.; Klebe, G. Docking into knowledge-based potential fields: a comparative evaluation of DrugScore. J. Mad. Chem. 2002, 45, 1967-1970.
59. Winum, J. Y.; Vullo, D.; Casini, A.; Montero, J. L.; Scozzafava, A. et al. Carbonic anhydrase inhibitors. Inhibition of cytosolic isozymes I and II and transmembrane, tumor-associated isozyme IX with sulfamates including EMATE also acting as steroid sulfatase inhibitors. J. Med. Chem. 2003, 46, 2197-2204.
60. SYBYL molecular modeling package; version 6.8 ed.; Tripos Inc.: 1699 South Hanley Road, Suite 303, St. Louis, MO 63144.
61. Clark, M.; Cramer, R. D.; van Opdenbosch, N. Validation of the General Purpose Tripos 5.2 Force Field. J. Comput. Chem. 1989, 10, 982-1012.
62. Dewar, M. J. S.; Zoebisch, E. G.; Healy, E. F.; Stewart, J. J. P. AM1 A new general purpose quantum mechanical molecular model. J. Am. Chem. Soc. 1985, 107, 3902-3909.
63. Stewart, J. J. MOPAC: a semiempirical molecular orbital program. J. Comput.-Aided Mol. Des. 1990, 4, 1-105.
64. Bush, B. L.; Nachbar, R. B., Jr. Sample-distance partial least squares: PLS optimized for many variables, with application to CoMFA. J. Comput.-Aided Mol. Des. 1993, 7, 587-619.
65. Goodsell, D. S.; Olson, A. J. Automated docking of substrates to proteins by simulated annealing. Proteins 1990, 8, 195-202.
66. Klebe, G. From structure to recognition principles: mining in crystal data as a prerequisite for drug design. Ernst Schering Res. Found Workshop 2003, 42, 103-126.
67. Weiner, S. J.; Kollman, P. A.; Case, D. A.; Singh, U. C.; Ohio, C. et al. A new force field for molecular mechanical simulation of nucleic acids and proteins. J. Am. Chem. Soc. 1984, 106, 765-784.
68. DeLano, W. L. The PyMOL Molecular Graphics System; DeLano Scientific: San Carlos, CA, 2002. http://www.pymol.org.