Synthesis, structure-activity relationship studies, and X-ray crystallographic analysis of arylsulfonamides as potent carbonic anhydrase inhibitors

Journal of Medicinal Chemistry

Volumn 55, Issue 8, 2012, Pages 3891-3899

  Gitto, Rosaria ^a   Damiano, Francesca M ^a   Mader, Pavel ^b   De Luca, Laura ^a   Ferro, Stefania ^a   Supuran, Claudiu T ^c   Vullo, Daniela ^c   Brynda, Jiří ^b,d   Řezáčová, Pavlína ^b,d   Chimirri, Alba ^a  

^a UNIVERSITY OF MESSINA   (Italy)

^b INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

^c UNIVERSITY OF FLORENCE   (Italy)

^d INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

1 [4 (AMINOSULFONYL)PHENYL] 6 ALKOXY 1,2,3,4 TETRATETRAHYDROISOQUINOLINE 2 SULFONAMIDE; 1 [4 (AMINOSULFONYL)PHENYL] 6 ETHOXY 1,2,3,4 TETRATETRAHYDROISOQUINOLINE 2 SULFONAMIDE; 1 [4 (AMINOSULFONYL)PHENYL] 6 HYDROXY 1,2,3,4 TETRATETRAHYDROISOQUINOLINE 2 SULFONAMIDE; 1 [4 (AMINOSULFONYL)PHENYL] 6 METHOXY 1,2,3,4 TETRATETRAHYDROISOQUINOLINE 2 SULFONAMIDE; 1 [4 (AMINOSULFONYL)PHENYL] 6 PROPOXY 1,2,3,4 TETRATETRAHYDROISOQUINOLINE 2 SULFONAMIDE; 4 (6 ALKOXY 1,2,3,4 TETRAHYDROISOQUINOLIN 1 YL)BENZENESULFONAMIDE; 4 (6 ALKOXY 3,4 DIHYDROISOQUINOLIN 1 YL)BENZENESULFONAMIDE; 4 (6 ETHOXY 1,2,3,4 TETRAHYDROISOQUINOLIN 1 YL)BENZENESULFONAMIDE; 4 (6 ETHOXY 3,4 DIHYDROISOQUINOLIN 1 YL)BENZENESULFONAMIDE; 4 (6 HYDROXY 1,2,3,4 TETRAHYDROISOQUINOLIN 1 YL)BENZENESULFONAMIDE; 4 (6 HYDROXY 3,4 DIHYDROISOQUINOLIN 1 YL)BENZENESULFONAMIDE; 4 (6 METHOXY 1,2,3,4 TETRAHYDROISOQUINOLIN 1 YL)BENZENESULFONAMIDE; 4 (6 METHOXY 3,4 DIHYDROISOQUINOLIN 1 YL)BENZENESULFONAMIDE; 4 (6 PROPOXY 1,2,3,4 TETRAHYDROISOQUINOLIN 1 YL)BENZENESULFONAMIDE; 4 (6 PROPOXY 3,4 DIHYDROISOQUINOLIN 1 YL)BENZENESULFONAMIDE; 4 [AMINOSULFONYL N 2 (3' ALKOXY) PHENETHYL] BENZAMIDE; 4 [AMINOSULFONYL N 2 (3' HYDROXY)PHENYL)ETHYL]BENZAMIDE; 4 [AMINOSULFONYL N 2 (3' METHOXY)PHENYL)ETHYL]BENZAMIDE; 4 [AMINOSULFONYL N 2 (3' PROPOXY)PHENYL)ETHYL]BENZAMIDE; 4 [AMINOSULFONYL N 2 (3'-ETHOXY)PHENYL)ETHYL]BENZAMIDE; ACETAZOLAMIDE; AMINO ACID; CARBONATE DEHYDRATASE; CARBONATE DEHYDRATASE INHIBITOR; SULFONAMIDE; TOPIRAMATE; UNCLASSIFIED DRUG; ZONISAMIDE;

ARTICLE; DRUG SYNTHESIS; ENZYME ACTIVE SITE; ENZYME INHIBITION; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY;

CARBONIC ANHYDRASE INHIBITORS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DRUG DESIGN; HUMANS; ISOENZYMES; MODELS, MOLECULAR; STRUCTURE-ACTIVITY RELATIONSHIP; SULFONAMIDES;

EID: 84860283065     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm300112w     Document Type: Article

References (49)

1. Supuran, C. T.; Scozzafava, A. Carbonic anhydrases as targets for medicinal chemistry Bioorg. Med. Chem. 2007, 15, 4336-4350 (Pubitemid 46777288)
2. Supuran, C. T. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators Nat. Rev. Drug Discovery 2008, 7, 168-181 (Pubitemid 351194064)
3. Supuran, C. T. Carbonic anhydrase inhibition/activation: trip of a scientist around the world in the search of novel chemotypes and drug targets Curr. Pharm. Des. 2010, 16, 3233-3245
4. Supuran, C. T. Carbonic anhydrase inhibitors Bioorg. Med. Chem. Lett. 2010, 20, 3467-3474
5. Supuran, C. T.; Scozzafava, A.; Casini, A. Carbonic anhydrase inhibitors Med. Res. Rev. 2003, 23, 146-189 (Pubitemid 36241096)
6. Supuran, C. T.; Di Fiore, A.; De Simone, G. Carbonic anhydrase inhibitors as emerging drugs for the treatment of obesity Expert Opin. Emerging Drugs 2008, 13, 383-392 (Pubitemid 351957352)
7. Supuran, C. T. Diuretics: from classical carbonic anhydrase inhibitors to novel applications of the sulfonamides Curr. Pharm. Des. 2008, 14, 641-648 (Pubitemid 351736443)
8. De Simone, G.; Supuran, C. T. Antiobesity carbonic anhydrase inhibitors Curr. Top. Med. Chem. 2007, 7, 879-884 (Pubitemid 46830332)
9. Thiry, A.; Dogne, J. M.; Supuran, C. T.; Masereel, B. Carbonic anhydrase inhibitors as anticonvulsant agents Curr. Top. Med. Chem. 2007, 7, 855-864 (Pubitemid 46825082)
10. Thiry, A.; Masereel, B.; Dogne, J. M.; Supuran, C. T.; Wouters, J.; Michaux, C. Exploration of the binding mode of indanesulfonamides as selective inhibitors of human carbonic anhydrase type VII by targeting Lys 91 ChemMedChem 2007, 2, 1273-1280
11. Asiedu, M.; Ossipov, M. H.; Kaila, K.; Price, T. J. Acetazolamide and midazolam act synergistically to inhibit neuropathic pain Pain 2010, 148, 302-308
12. Neri, D.; Supuran, C. T. Interfering with pH regulation in tumours as a therapeutic strategy Nat. Rev. Drug Discovery 2011, 10, 767-777
13. Said, H. M.; Supuran, C. T.; Hageman, C.; Staab, A.; Polat, B.; Katzer, A.; Scozzafava, A.; Anacker, J.; Flentje, M.; Vordermark, D. Modulation of carbonic anhydrase 9 (CA9) in human brain cancer Curr. Pharm. Des. 2010, 16, 3288-3299
14. Guler, O. O.; De Simone, G.; Supuran, C. T. Drug design studies of the novel antitumor targets carbonic anhydrase IX and XII Curr. Med. Chem. 2010, 17, 1516-1526
15. Akurathi, V.; Dubois, L.; Lieuwes, N. G.; Chitneni, S. K.; Cleynhens, B. J.; Vullo, D.; Supuran, C. T.; Verbruggen, A. M.; Lambin, P.; Bormans, G. M. Synthesis and biological evaluation of a 99mTc-labelled sulfonamide conjugate for in vivo visualization of carbonic anhydrase IX expression in tumor hypoxia Nucl. Med. Biol. 2010, 37, 557-564
16. Genis, C.; Sippel, K. H.; Case, N.; Cao, W.; Avvaru, B. S.; Tartaglia, L. J.; Govindasamy, L.; Tu, C.; Agbandje-McKenna, M.; Silverman, D. N.; Rosser, C. J.; McKenna, R. Design of a carbonic anhydrase IX active-site mimic to screen inhibitors for possible anticancer properties Biochemistry 2009, 48, 1322-1331
17. Thiry, A.; Supuran, C. T.; Masereel, B.; Dogne, J. M. Recent developments of carbonic anhydrase inhibitors as potential anticancer drugs J. Med. Chem. 2008, 51, 3051-3056 (Pubitemid 351821862)
18. Pastorekova, S.; Kopacek, J.; Pastorek, J. Carbonic anhydrase inhibitors and the management of cancer Curr. Top. Med. Chem. 2007, 7, 865-878 (Pubitemid 46830331)
19. De Simone, G.; Vitale, R. M.; Di Fiore, A.; Pedone, C.; Scozzafava, A.; Montero, J. L.; Winum, J. Y.; Supuran, C. T. Carbonic anhydrase inhibitors: Hypoxia-activatable sulfonamides incorporating disulfide bonds that target the tumor-associated isoform IX J. Med. Chem. 2006, 49, 5544-5551 (Pubitemid 44373185)
20. Parkkila, S.; Parkkila, A. K.; Rajaniemi, H.; Shah, G. N.; Grubb, J. H.; Waheed, A.; Sly, W. S. Expression of membrane-associated carbonic anhydrase XIV on neurons and axons in mouse and human brain Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 1918-1923 (Pubitemid 32165598)
21. Winum, J. Y.; Scozzafava, A.; Montero, J. L.; Supuran, C. T. Design of zinc binding functions for carbonic anhydrase inhibitors Curr. Pharm. Des. 2008, 14, 615-621 (Pubitemid 351736440)
22. 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 (Pubitemid 44735553)
23. Gitto, R.; Ferro, S.; Agnello, S.; De Luca, L.; De Sarro, G.; Russo, E.; Vullo, D.; Supuran, C. T.; Chimirri, A. Synthesis and evaluation of pharmacological profile of 1-aryl-6,7-dimethoxy-3,4-dihydroisoquinoline-2(1H)- sulfonamides Bioorg. Med. Chem. 2009, 17, 3659-3664
24. Gitto, R.; Agnello, S.; Ferro, S.; Vullo, D.; Supuran, C. T.; Chimirri, A. Identification of potent and selective human carbonic anhydrase VII (hCA VII) inhibitors ChemMedChem 2010, 5, 823-826
25. Gitto, R.; Agnello, S.; Ferro, S.; De Luca, L.; Vullo, D.; Brynda, J.; Mader, P.; Supuran, C. T.; Chimirri, A. Identification of 3,4- Dihydroisoquinoline-2(1 H)-sulfonamides as potent carbonic anhydrase inhibitors: synthesis, biological evaluation, and enzyme-ligand X-ray studies J. Med. Chem. 2010, 53, 2401-2408
26. Gitto, R.; Damiano, F. M.; De Luca, L.; Ferro, S.; Vullo, D.; Supuran, C. T.; Chimirri, A. Synthesis and biological profile of new 1,2,3,4- tetrahydroisoquinolines as selective carbonic anhydrase inhibitors Bioorg. Med. Chem. 2011, 19, 7003-7007
27. Mader, P.; Brynda, J.; Gitto, R.; Agnello, S.; Pachl, P.; Supuran, C. T.; Chimirri, A.; Rezacova, P. Structural basis for the interaction between carbonic anhydrase and 1,2,3,4-tetrahydroisoquinolin-2-ylsulfonamides J. Med. Chem. 2011, 54, 2522-2526
28. 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
29. Eriksson, A. E.; Jones, T. A.; Liljas, A. Refined structure of human carbonic anhydrase II at 2.0 A resolution Proteins 1988, 4, 274-282 (Pubitemid 19094186)
30. Winum, J. Y.; Scozzafava, A.; Montero, J. L.; Supuran, C. T. Sulfamates and their therapeutic potential Med. Res. Rev. 2005, 25, 186-228 (Pubitemid 40299846)
31. Srivastava, D. K.; Jude, K. M.; Banerjee, A. L.; Haldar, M.; Manokaran, S.; Kooren, J.; Mallik, S.; Christianson, D. W. Structural analysis of charge discrimination in the binding of inhibitors to human carbonic anhydrases I and II J..Am. Chem. Soc. 2007, 129, 5528-5537 (Pubitemid 46697640)
32. Alterio, V.; Monti, S. M.; Truppo, E.; Pedone, C.; Supuran, C. T.; De Simone, G. The first example of a significant active site conformational rearrangement in a carbonic anhydrase-inhibitor adduct: the carbonic anhydrase I-topiramate complex Org. Biomol. Chem. 2010, 8, 3528-3533
33. Alterio, V.; Hilvo, M.; Di Fiore, A.; Supuran, C. T.; Pan, P.; Parkkila, S.; Scaloni, A.; Pastorek, J.; Pastorekova, S.; Pedone, C.; Scozzafava, A.; Monti, S. M.; De Simone, G. Crystal structure of the catalytic domain of the tumor-associated human carbonic anhydrase IX Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 16233-16238
34. Whittington, D. A.; Grubb, J. H.; Waheed, A.; Shah, G. N.; Sly, W. S.; Christianson, D. W. Expression, assay, and structure of the extracellular domain of murine carbonic anhydrase XIV: implications for selective inhibition of membrane-associated isozymes J. Biol. Chem. 2004, 279, 7223-7228 (Pubitemid 38248870)
35. Nishimori, I.; Vullo, D.; Innocenti, A.; Scozzafava, A.; Mastrolorenzo, A.; Supuran, C. T. Carbonic anhydrase inhibitors: inhibition of the transmembrane isozyme XIV with sulfonamides Bioorg. Med. Chem. Lett. 2005, 15, 3828-3833 (Pubitemid 41095477)
36. 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 (Pubitemid 41698823)
37. Innocenti, A.; Vullo, D.; Pastorek, J.; Scozzafava, A.; Pastorekova, S.; Nishimori, I.; Supuran, C. T. Carbonic anhydrase inhibitors. Inhibition of transmembrane isozymes XII (cancer-associated) and XIV with anions Bioorg. Med. Chem. Lett. 2007, 17, 1532-1537 (Pubitemid 46290636)
38. Nishimori, I.; Minakuchi, T.; Morimoto, K.; Sano, S.; Onishi, S.; Takeuchi, H.; Vullo, D.; Scozzafava, A.; Supuran, C. T. Carbonic anhydrase inhibitors: DNA cloning and inhibition studies of the alpha-carbonic anhydrase from Helicobacter pylori, a new target for developing sulfonamide and sulfamate gastric drugs J. Med. Chem. 2006, 49, 2117-2126
39. Behnke, C. A.; Le Trong, I.; Godden, J. W.; Merritt, E. A.; Teller, D. C.; Bajorath, J.; Stenkamp, R. E. Atomic resolution studies of carbonic anhydrase II Acta Crystallogr. Biol. Crystallogr. 2010, 66, 616-627
40. Minor, W.; Cymborowski, M.; Otwinowski, Z.; Chruszcz, M. HKL-3000: the integration of data reduction and structure solution - from diffraction images to an initial model in minutes Acta Crystallogr. Biol. Crystallogr. 2006, 62, 859-866 (Pubitemid 44125661)
41. Leslie, A. G. Integration of macromolecular diffraction data Acta Crystallogr. Biol. Crystallogr. 1999, 55, 1696-1702 (Pubitemid 29504424)
42. Evans, P. R. Proceedings of the CCP4 Study Weekend. Data Collection and Processing, Daresbury Laboratory, Warrington, 1993.
43. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. Biol. Crystallogr. 1994, 50, 760-763.
44. Schuttelkopf, A. W.; van Aalten, D. M. PRODRG: a tool for high-throughput crystallography of protein-ligand complexes Acta Crystallogr. Biol. Crystallogr. 2004, 60, 1355-1363 (Pubitemid 41079731)
45. Emsley, P.; Cowtan, K. Coot: model-building tools for molecular graphics Acta Crystallogr. Biol. Crystallogr. 2004, 60, 2126-2132 (Pubitemid 41742764)
46. Sheldrick, G. M. A short history of SHELX Acta Crystallogr., Sect. A: Found. Crystallogr. 2008, 64, 112-122
47. Lovell, S. C.; Davis, I. W.; Arendall, W. B., III; de Bakker, P. I.; Word, J. M.; Prisant, M. G.; Richardson, J. S.; Richardson, D. C. Structure validation by Calpha geometry: phi,psi and Cbeta deviation Proteins 2003, 50, 437-450 (Pubitemid 36158457)
48. DeLano, W. L. The PyMOL Molecular Graphics System; DeLano Scientific: Palo Alto, CA, 2002.
49. Brunger, A. T. Free R value: a novel statistical quantity for assessing the accuracy of crystal structures Nature 1992, 355, 472-475