Carbonic anhydrase inhibitors: Clash with Ala65 as a means for designing inhibitors with low affinity for the ubiquitous isozyme II, exemplified by the crystal structure of the topiramate sulfamide analogue

Journal of Medicinal Chemistry

Volumn 49, Issue 24, 2006, Pages 7024-7031

  Winum, Jean Yves ^a   Temperini, Claudia ^b   El Cheikh, Khaled ^a   Innocenti, Alessio ^b   Vullo, Daniela ^b   Ciattini, Samuele ^b   Montero, Jean Louis ^a   Scozzafava, Andrea ^b   Supuran, Claudiu T ^b  

^a UNIV MONTPELLIER   (France)

^b UNIVERSITY OF FLORENCE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ANTICONVULSIVE AGENT; ASPARAGINE; CARBONATE DEHYDRATASE II; CARBONATE DEHYDRATASE INHIBITOR; GLUTAMINE; HISTIDINE; RWJ 37947; THREONINE; TOPIRAMATE; ZINC;

ARTICLE; BINDING AFFINITY; DRUG DESIGN; DRUG PROTEIN BINDING; DRUG STRUCTURE; ENZYME INHIBITION; HYDROGEN BOND; X RAY CRYSTALLOGRAPHY;

ALANINE; ANTICONVULSANTS; CARBONIC ANHYDRASE II; CARBONIC ANHYDRASE INHIBITORS; CRYSTALLOGRAPHY, X-RAY; DRUG DESIGN; FRUCTOSE; HYDROGEN BONDING; ISOENZYMES; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PROTEIN BINDING; STRUCTURE-ACTIVITY RELATIONSHIP; SULFONAMIDES;

EID: 33845353402     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm060807n     Document Type: Article

References (59)

1. Supuran, C. T.; Scozzafava, A.; Conway, J. Carbonic Anhydrase. Its Inhibitors and Activators; CRC Press: Boca Raton, FL,, 2004; pp 1-363.
2. (a) Pastorekova, S.; Parkkila, S.; Pastorek, J.; Supuran, C. T. Carbonic anhydrases: current state of the art, therapeutic applications and future prospects. J. Enzyme Inhib. Med. Chem. 2004, 19, 199-229.
3. (b) Supuran, C. T.; Scozzafava, A.; Casini, A. Development of Sulfonamide Carbonic Anhydrase Inhibitors. In Carbonic Anhydrase. Its Inhibitors and Activators; Supuran, C. T., Scozzafava, A., Conway, J., Eds.; CRC Press: Boca Raton, FL, 2004; pp 67-147.
4. (a) Supuran, C. T.; Scozzafava, A.; Casini, A. Carbonic anhydrase inhibitors. Med. Res. Rev. 2003, 23, 146-189.
5. (b) Scozzafava, A.; Mastrolorenzo, A.; Supuran, C. T. Modulation of carbonic anhydrase activity and its applications in therapy. Expert Opin. Ther. Pat. 2004, 14, 667-702.
6. (c) Winum, J. Y.; Montero, J. L.; Scozzafava, A.; Supuran, C. T. New zinc binding motifs in the design of selective carbonic anhydrase inhibitors. Mini-Rev. Med. Chem. 2006, 6, 921-936.
7. Winum, J. Y.; Scozzafava, A.; Montero, J. L.; Supuran, C. T. Sulfamates and their therapeutic potential. Med. Res. Rev. 2005, 25, 186-228.
8. Winum, J.-Y.; Scozzafava, A.; Montero, J.-L.; Supuran, C. T. The sulfamide motif in the design of enzyme inhibitors. Expert Opin. Ther. Pat. 2006, 16, 27-47.
9. Winum, J.-Y.; Scozzafava, A.; Montero, J.-L.; Supuran, C. T. Therapeutic potential of sulfamides as enzyme inhibitors. Med. Res. Rev. 2006, 26, 767-792.
10. Alterio, V.; Vitale, R. M.; Monti, S. M.; Pedone, C.; Scozzafava, A.; Cecchi, A.; De Simone, G.; Supuran, C. T. Carbonic anhydrase inhibitors: X-ray and molecular modeling study for the interaction of a fluorescent antitumor sulfonamide with isozyme II and IX. J. Am. Chem. Soc. 2006, 128, 8329-8335.
11. (a) Weber, A.; Casini, A.; Heine, A.; Kuhn, D.; Supuran, C. T.; Scozzafava, A.; Klebe, G. Unexpected nanomolar inhibition of carbonic anhydrase by COX-2 selective celecoxib: New pharmacological opportunities due to related binding site recognition. J. Med. Chem. 2004, 47, 550-557.
12. (b) Menchise, V.; De Simone, G.; Alterio, V.; Di Fiore, A.; Pedone, C.; Scozzafava, A.; Supuran, C. T. Carbonic anhydrase inhibitors: Stacking with Phe131 determines active site binding region of inhibitors as exemplified by the X-ray crystal structure of a membrane-impermeant antitumor sulfonamide complexed with isozyme II. J. Med. Chem. 2005, 48, 5721-5727.
13. (a) De Simone, G.; Di Fiore, A.; Menchise, V.; Pedone, C.; Antel, J.; Casini, A.; Scozzafava, A.; Wurl, M.; Supuran, C. T. Carbonic anhydrase inhibitors. Zonisamide is an effective inhibitor of the cytosolic isozyme II and mitochondrial isozyme V: solution and X-ray crystallographic studies. Bioorg. Med. Chem. Lett. 2005, 15, 2315-2320.
14. (b) Casini, A.; Antel, J.; Abbate, F.; Scozzafava, A.; David, S.; Waldeck, H.; Schafer, S.; Supuran, C. T. 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.
15. (c) 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.
16. Abbate, F.; Supuran, C. T.; Scozzafava, A.; Orioli, P.; Stubbs, M.; Klebe, G. 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.
17. (a) Boriack, P. A.; Christianson, D. W.; Kingery-Wood, J.; Whitesides, G. M. Secondary interactions significantly removed from the sulfonamide binding pocket of carbonic anhydrase II influence inhibitor binding constants. J. Med. Chem. 1995, 38, 2286-2291.
18. (b) Stams, T.; Chen, Y.; Boriack-Sjodin, P. A.; Hurt, J. D.; Liao, J.; May, J. A.; Dean, T.; Laipis, P.; Silverman, D. N.; Christianson, D. W. Structures of murine carbonic anhydrase IV and human carbonic anhydrase II complexed with brinzolamide: molecular basis of isozyme-drug discrimination. Protein Sci. 1998, 7, 556-563.
19. (c) Kim, C. Y.; Chang, J. S.; Doyon, J. B.; Baird, T. T.; Fierke, C. A.; Jain, A.; Christianson, D. W. Contributions of fluorine to protein-ligand affinity in the binding of fluoroaromatic inhibitors to carbonic anhydrase II. J. Am. Chem. Soc. 2000, 122, 12125-12134.
20. (d) Whittington, D. A.; Waheed, A.; Ulmasov, B.; Shah, G. N.; Grubb, J. H.; Sly, W. S.; Christianson, D. W. Crystal structure of the dimeric extracellular domain of human carbonic anhydrase XII, a bitopic membrane protein overexpressed in certain cancer tumor cells. Proc. Natl. Acd. Sci. U.S.A. 2001, 98, 9545-9550.
21. (e) Jude, K. M.; Banerjee, A. L.; Haldar, M. K.; Manokaran, S.; Roy, B.; Mallik, S.; Srivastava, D. K.; Christianson, D. W. Ultrahigh resolution crystal structures of human carbonic anhydrases I and II complexed with "two-prong" inhibitors reveal the molecular basis of high affinity. J. Am. Chem. Soc. 2006, 128, 3011-3018.
22. Vidgren, J.; Svensson, A.; Liljas, A. Refined structure of the aminobenzolamide complex of human carbonic anhydrase II at 1.9 Å and sulphonamide modelling of bovine carbonic anhydrase III. Int. J. Biol. Macromol. 1993, 15, 97-100.
23. (a) Abbate, F.; Winum, J. Y.; Potter, B. V.; Casini, A.; Montero, J. L.; Scozzafava, A.; Supuran, C. T. Carbonic anhydrase inhibitors: X-ray crystallographic structure of the adduct of human isozyme II with EMATE, a dual inhibitor of carbonic anhydrases and steroid sulfatase. Bioorg. Med. Chem. Lett. 2004, 14, 231-234.
24. (b) Lloyd, M. D.; Pederick, R. L.; Natesh, R.; Woo, L. W.; Purohit, A.; Reed, M. J.; Acharya, K. R.; Potter, B. V. Crystal structure of human carbonic anhydrase II at 1.95 Å resolution in complex with 667-coumate, a novel anti-cancer agent. Biochem. J. 2005, 385, 715-720.
25. (c) Lloyd, M. D.; Thiyagarajan, N.; Ho, Y. T.; Woo, L. W.; Sutcliffe, O. B.; Purohit, A.; Reed, M. J.; Acharya, K. R.; Potter B. V. First crystal structures of human carbonic anhydrase II in complex with dual aromatase-steroid sulfatase inhibitors. Biochemistry 2005, 44, 6858-6866.
26. Recacha, R.; Costanzo, M. J.; Maryanoff, B. E.; Chattopadhyay, D. Crystal structure of human carbonic anhydrase II complexed with an anticonvulsant sugar sulphamate. Biochem. J. 2002, 361, 437-441.
27. Gruneberg, S.; Stubbs, M. T.; Klebe, G. Successful virtual screening for novel inhibitors of human carbonic anhydrase: Strategy and experimental confirmation. J. Med. Chem. 2002, 45, 3588-3602.
28. Maryanoff, B. E.; McComsey, D. F.; Costanzo, M. J.; Hochman, C.; Smith-Swintovsky, V.; Shank, R. P. Comparison of sulfamate and sulfamide groups for the inhibition of carbonic anhydrase-II by using topiramate as a structural platform. J. Med. Chem. 2005, 48, 1941-1947.
29. Klinger, A. L.; McComsey, D. F.; Smith-Swintovsky, V.; Shank, R. P.; Maryanoff, B. E. Inhibition of carbonic anhydrase-II by sulfamate and sulfamide groups: An investigation involving direct thermodynamic binding measurements. J. Med. Chem. 2006, 49, 3496-3500.
30. (a) Casini, A.; Winum, J. Y.; Montero, J. L.; Scozzafava, A.; Supuran, C. T. Carbonic anhydrase inhibitors: inhibition of cytosolic isozymes I and II with sulfamide derivatives. Bioorg. Med. Chem. Lett. 2003, 13, 837-840.
31. (b) Winum, J. Y.; Innocenti, A.; Nasr, J.; Montero, J. L.; Scozzafava, A.; Vullo, D.; Supuran, C. T. Carbonic anhydrase inhibitors: synthesis and inhibition of cytosolic/tumor-associated carbonic anhydrase isozymes I, II, IX and XII with N-hydroxysulfamides, a new zinc binding function in the design of inhibitors. Bioorg. Med. Chem. Lett. 2005, 15, 2353-2358.
32. Winum, J. Y.; Cecchi, A.; Montero, J. L.; Innocenti, A.; Scozzafava, A.; Supuran, C. T. Carbonic anhydrase inhibitors. Synthesis and inhibition of cytosolic/tumor-associated carbonic anhydrase isozymes I, II, and IX with boron-containing sulfonamides, sulfamides and sulfamates: towards agents for boron neutron capture therapy of hypoxic tumors. Bioorg. Med. Chem. Lett. 2005, 15, 3302-3306.
33. Maryanoff, B. E.; Nortey, S. O.; Gardocki, J. F.; Shank, R. P.; Dodgson, S. P. Anticonvulsant O-alkyl sulfamates. 2,3:4,5-Bis-O-(1-methylethylidene)- β-D-fructopyranose sulfamate and relate compounds. J. Med. Chem. 1987, 30, 880-887.
34. (a) Svastova, E.; Hulikova, A.; Rafajova, M.; Zat'ovicova, M.; Gibadulinova, A.; Casini, A.; Cecchi, A.; Scozzafava, A.; Supuran, C. T.; Pastorek, J.; Pastorekova, S. Hypoxia activates the capacity of tumor-associated carbonic anhydrase IX to acidify extracellular pH. FEBS Lett. 2004, 577, 439-445.
35. (b) Supuran, C. T. Indisulam, an anticancer sulfonamide in clinical development. Expert Opin. Invest. Drugs 2003, 12, 283-287.
36. Vullo, D.; Innocenti, A.; Nishimori, I.; Pastorek, J.; Scozzafava, A.; Pastorekova, S.; Supuran, C. T. Carbonic anhydrase inhibitors. Inhibition of the transmembrane isozyme XII with sulfonamides, a new target for the design of antitumor and antiglaucoma drugs? Bioorg. Med. Chem. Lett. 2005, 15, 963-969.
37. Cecchi, A.; Hulikova, A.; Pastorek, J.; Pastorekova, S.; Scozzafava, A.; Winum, J.-Y.; Montero, J.-L.; Supuran, C. T. Carbonic anhydrase inhibitors. Sulfonamides inhibit isozyme IX mediated acidification of hypoxic tumors. Fluorescent sulfonamides design as probes of membrane-bound carbonic anhydrase isozymes involvement in tumorigenesis. J. Med. Chem. 2005, 48, 4834-4841.
38. (e) Thiry, A.; Dogné, J. M.; Masereel, B.; Supuran, C. T. Targeting tumor-associated carbonic anhydrase IX in cancer therapy. Trends Pharmacol. Sci. 2006, 27, 566-573.
39. (a) Supuran, C. T. Carbonic anhydrase inhibitors in the treatment and prophylaxis of obesity. Expert Opin. Ther. Pat. 2003, 13, 1545-1550.
40. (b) Vullo, D.; Franchi, M.; Gallori, E.; Antel, J.; Scozzafava, A.; Supuran, C. T. Carbonic anhydrase inhibitors. Inhibition of mitochondrial isozyme V with aromatic and heterocyclic sulfonamides. J. Med. Chem. 2004, 47, 1272-1279.
41. (c) Nishimori, I.; Vullo, D.; Innocenti, A.; Scozzafava, A.; Mastrolorenzo, A.; Supuran, C. T. Carbonic anhydrase inhibitors. The mitochondrial isozyme VB as a new target for sulfonamide and sulfamate inhibitors. J. Med. Chem. 2005, 48, 7860-7866.
42. Khalifah, R. G. The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C. J. Biol. Chem. 1971, 246, 2561-2573.
43. Briganti, F.; Pierattelli, R.; Scozzafava, A.; Supuran, C. T. Carbonic anhydrase inhibitors. Part 37. Novel classes of carbonic anhydrase inhibitors and their interaction with the native and cobalt-substituted enzyme: kinetic and spectroscopic investigations. Eur. J. Med. Chem. 1996, 31, 1001-1010.
44. (a) Asensio-Sanchez, V. M.; Torreblanca-Aguera, B.; Martinez-Calvo, S.; Calvo, M. J.; Rodriguez, R. Severe ocular side effects with Topamax. Arch. Soc. Esp. Oftalmol. 2006, 81, 345-348.
45. (b) Sacre, A.; Jouret, F.; Manicourt, D.; Devuyst, O. Topiramate induces type 3 renal tubular acidosis by inhibiting renal carbonic anhydrase. Nephrol. Dial., Transplant. 2006, 21, 2995-2996.
46. (c) Alore, P. L.; Jay, W. M.; Macken, M. P. Topiramate, pseudotumor cerebri, weight-loss and glaucoma: an ophthalmologic perspective. Semin. Ophthalmol. 2006, 21, 15-17.
47. (d) Alarcon-Martinez, H.; Casas-Fernandez, C.; Escudero-Rodriguez, N.; Cao-Avellaneda, E.; Domingo-Jimenez, R.; Puche-Mira, A.; Rodriguez-Costa, T. Nephrolithiasis and topiramate. Rev. Neurol. 2006, 42, 91-94.
48. (e) Burmeister, J. E.; Pereira, R. R.; Hartke, E. M.; Kreuz, M. Topiramate and severe metabolic acidosis: case report. Arq. Neuropsiquiatr. 2005, 63, 532-534.
49. Lehtonen, J.; Shen, B.; Vihinen, M.; Casini, A.; Scozzafava, A.; Supuran, C. T.; Parkkila, A. K.; Saarnio, J.; Kivela, A. J.; Waheed, A.; Sly, W. S.; Parkkila, S. Characterization of CA XIII, a novel member of the carbonic anhydrase isozyme family. J. Biol. Chem. 2004, 279, 2719-2727.
50. Eriksson, A. E.; Jones, T. A.; Liljas, A. Refined structure of human carbonic anhydrase II at 2.0 Å resolution. Proteins: Struct. Funct. 1988, 4, 274-282.
51. 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: Consequences for structure-based drug design. In Carbonic Anhydrase. Its Inhibitors and Activators; Supuran, C. T., Scozzafava, A., Conway, J., Eds.; CRC Press: Boca Raton, FL, 2004; pp 45-65.
52. Vullo, D.; Voipio, J.; Innocenti, A.; Rivera, C.; Ranki, H.; Scozzafava, A.; Kaila, K.; Supuran, C. T. Carbonic anhydrase inhibitors. Inhibition of the human cytosolic isozyme VII with aromatic and heterocyclic sulfonamides. Bioorg. Med. Chem. Lett. 2005, 15, 971-976.
53. (a) Nishimori, I.; Vullo, D.; Innocenti, A.; Scozzafava, A.; Matrolorenzo, A.; Supuran, C. T. Carbonic anhydrase inhibitors: Inhibition of the transmembrane isozyme XIV with sulfonamides. Bioorg. Med. Chem. Lett. 2005, 15, 3828-3833.
54. (b) Ozensoy, O.; Nishimori, I.; Vullo, D.; Puccetti, L.; Scozzafava, A.; Supuran, C. T. Carbonic anhydrase inhibitors. Inhibition of the human transmembrane isozyme XIV with a library of aromatic/heterocyclic sulfonamides. Bioorg. Med. Chem. 2005, 13, 6089-6093.
55. Leslie, A. G. W. MOSFLM User's Guide; MRC-LMB: Cambridge, U.K., 1994.
56. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr., Sect. D. 1994, 50, 760-763.
57. Brunger, A. T.; Adams, P. D.; Clore, G. M.; Delano, W. L.; Gros, P.; Grosse-Kunsteleve, R. W.; Fiang, J.; Kuszewsky, J.; Niles, M.; Pannu, N. S.; Read, R. J.; Rice, L. M.; Simmonson, T.; Warren, G. L. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr., Sect. D. 1998, 54, 905-921.
58. Jones, T. A.; Zhou, J. Y.; Cowan, S. W.; Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr., Sect. A 1991, 47, 110-119.
59. Weber, A.; Bohm, M.; Supuran, C. T.; Scozzafava, A.; Sotriffer, C. A.; Klebe, G. 3D QSAR selectivity analyses of carbonic anhydrase inhibitors: Insights for the design of isozyme selective inhibitors. J. Chem. Inf. Model., in press.