Sulfonamides incorporating 1,3,5-triazine moieties selectively and potently inhibit carbonic anhydrase transmembrane isoforms IX, XII and XIV over cytosolic isoforms i and II: Solution and X-ray crystallographic studies

Bioorganic and Medicinal Chemistry

Volumn 19, Issue 10, 2011, Pages 3105-3119

  Carta, Fabrizio ^a   Garaj, Vladimir ^a,b   Maresca, Alfonso ^a   Wagner, Jason ^c   Avvaru, Balendu Sankara ^c   Robbins, Arthur H ^c   Scozzafava, Andrea ^a   McKenna, Robert ^c   Supuran, Claudiu T ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b Physics and Informatics   (Slovakia)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

1,3,5 Triazine; Carbonic anhydrase; Isoform IX, XII; Isoform selective inhibitor; Sulfonamide; X ray crystallography

Indexed keywords

1,3,5 TRIAZINYL BENZENESULFONAMIDE DERIVATIVE; 2 (TERT BUTYLDIMETHYLSILYLOXY)ETHANOL; 2'' [4' CHLORO 6' (4 SULFAMOYLBENZYLAMINO) 1',3',5' TRIAZIN 2' YLAMINO] 3'' (6'',7'' DIHYDROXYPHENYL)PROPANOIC ACID; 2'' [4' CHLORO 6' (4 SULFAMOYLBENZYLAMINO) 1',3',5' TRIAZIN 2' YLAMINO]ACETIC ACID; 2'' [4' CHLORO 6' (4 SULFAMOYLPHENETHYLAMINO) 1',3',5' TRIAZIN 2' YLAMINO] 3'' (6'',7'' DIHYDROXYPHENYL)PROPANOIC ACID; 2'' [4' CHLORO 6' (4 SULFAMOYLPHENETHYLAMINO) 1',3',5' TRIAZIN 2' YLAMINO]ACETIC ACID; 2'' [4' CHLORO 6' (4 SULFAMOYLPHENYLAMINO) 1',3',5' TRIAZIN 2' YLAMINO]PROPANOIC ACID; 2'',2''' [6' (4 SULFAMOYLPHENETHYLAMINO) 1',3',5' TRIAZINE 2',4' DIYL] BIS(AZANEDIYL)BIS(3''HYDROXYPROPANOIC ACID); 2'',2''' [6' (4 SULFAMOYLPHENETHYLAMINO) 1',3',5' TRIAZINE 2',4' DIYL] BIS(AZANEDIYL)DIPROPANOIC ACID; 2'',2''' [6' (4 SULFAMOYLPHENYLAMINO) 1',3',5' TRIAZINE 2',4' DIYL] BIS(AZANEDIYL)DIACETIC ACID; 3'' [4' CHLORO 6' (4 SULFAMOYLBENZYLAMINO) 1',3',5' TRIAZIN 2' YLAMINO]PROPANOIC ACID; 3'' [4' CHLORO 6' (4 SULFAMOYLPHENETHYLAMINO) 1',3',5' TRIAZIN 2' YLAMINO]PROPANOIC ACID; 3'',3''' [6' (4 SULFAMOYLPHENYLAMINO) 1',3',5' TRIAZINE 2',4' DIYL] BIS(AZANEDIYL)DIPROPANOIC ACID; 4 (4',6' DICHLORO 1',3',5' TRIAZIN 2' YLAMINO)BENZENESULFONAMIDE; 4 [(4',6' DICHLORO 1',3',5' TRIAZIN 2' YLAMINO)METHYL]BENZENESULFONAMIDE; 4 [4' [2'' (TERT BUTYLDIMETHYLSILYLOXY)ETHOXY] 6' CHLORO 1',3',5' TRIAZIN 2' YLAMINO]BENZENESULFONAMIDE; 4 [4' CHLORO 6' (2'' HYDROXYETHYLAMINO) 1',3',5' TRIAZIN 2' YLAMINO]BENZENESULFONAMIDE; 4 [4' CHLORO 6' (4'' HYDROXYBUTYLAMINO) 1',3',5' TRIAZIN 2' YLAMINO]BENZENESULFONAMIDE; 4 [6 (4',6' DICHLORO 1',3',5' TRIAZIN 2' YLAMINO)ETHYL]BENZENESULFONAMIDE; ACETAZOLAMIDE; BENZENESULFONAMIDE DERIVATIVE; CARBONATE DEHYDRATASE; DICLOFENAMIDE; DIMETHYL 2'',2''' [6' (4 SULFAMOYLBENZYLAMINO) 1',3',5' TRIAZINE 2',4' DIYL] BIS(AZANEDIYL)DIACETATE; DIMETHYL 2',2''' [6' (4 SULFAMOYLPHENYLAMINO) 1',3',5' TRIAZINE 2',4' DIYL]BIS(AZANEDIYL)DIACETIC ACID; ETHOXZOLAMIDE; METHYL 2 AMINOACETATE HYDROCHLORIDE; METHYL 2'' [4' CHLORO 6' (4 SULFAMOYLBENZYLAMINO) 1',3',5' TRIAZIN 2' YLAMINO]ACETATE; METHYL 2'' [4' CHLORO 6' (4 SULFAMOYLPHENETHYLAMINO) 1',3',5' TRIAZIN 2' YLAMINO]ACETATE; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ANTIBACTERIAL ACTIVITY; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG POTENCY; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME INHIBITION; HYDROGEN BOND; HYDROPHILICITY; NONHUMAN; NUCLEOPHILICITY; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY;

ANTIFUNGAL AGENTS; CARBONIC ANHYDRASE I; CARBONIC ANHYDRASE II; CARBONIC ANHYDRASE INHIBITORS; CRYSTALLOGRAPHY, X-RAY; CYTOSOL; FUNGI; HUMANS; ISOENZYMES; MODELS, MOLECULAR; STRUCTURE-ACTIVITY RELATIONSHIP; SULFONAMIDES; TRIAZINES;

CANDIDA ALBICANS; FILOBASIDIELLA NEOFORMANS; MAMMALIA;

EID: 79956195097     PISSN: 09680896     EISSN: 14643391     Source Type: Journal    
DOI: 10.1016/j.bmc.2011.04.005     Document Type: Article

References (56)

1. V. Garaj, L. Puccetti, G. Fasolis, J.Y. Winum, J.L. Montero, A. Scozzafava, D. Vullo, A. Innocenti, and C.T. Supuran Bioorg. Med. Chem. Lett. 14 2004 5427
2. V. Garaj, L. Puccetti, G. Fasolis, J.Y. Winum, J.L. Montero, A. Scozzafava, D. Vullo, A. Innocenti, and C.T. Supuran Bioorg. Med. Chem. Lett. 15 2005 3102
3. G.F. D'Alelio, and H.J. White J. Org. Chem. 24 1959 643
4. C.T. Supuran Nat. Rev. Drug Disc. 7 2008 168
5. O. Özensoy, G. De Simone, and C.T. Supuran Curr. Med. Chem. 17 2010 1516
6. G. De Simone, and C.T. Supuran Biochim. Biophys. Acta 1804 2010 404
7. C.T. Supuran Bioorg. Med. Chem. Lett. 20 2010 3467
8. V. Alterio, M. Hilvo, A. Di Fiore, C.T. Supuran, P. Pan, S. Parkkila, A. Scaloni, J. Pastorek, S. Pastorekova, C. Pedone, A. Scozzafava, S.M. Monti, and G. De Simone Proc. Natl. Acad. Sci. U.S.A. 106 2009 16233
9. E. Švastová, A. Hulíková, M. Rafajová, M. Zat'ovičová, A. Gibadulinová, A. Casini, A. Cecchi, A. Scozzafava, C. Supuran, and J. Pastorek FEBS Lett. 577 2004 439
10. L. Dubois, K. Douma, C.T. Supuran, R.K. Chiu, M.A.M.J. van Zandvoort, S. Pastoreková, A. Scozzafava, B.G. Wouters, and P. Lambin Radiother. Oncol. 83 2007 367
11. L. Dubois, N.G. Lieuwes, A. Maresca, A. Thiry, C.T. Supuran, A. Scozzafava, B.G. Wouters, and P. Lambin Radiother. Oncol. 92 2009 423
12. P. Swietach, S. Wigfield, P. Cobden, C.T. Supuran, A.L. Harris, and R.D. Vaughan-Jones J. Biol. Chem. 283 2008 20473
13. P. Swietach, S. Wigfield, C.T. Supuran, A.L. Harris, and R.D. Vaughan-Jones BJU Int. 101 2008 22
14. P. Swietach, A. Hulikova, R.D. Vaughan-Jones, and A.L. Harris Oncogene 29 2010 6509
15. J.K.J. Ahlskog, C.E. Dumelin, S. Trüssel, J. Marlind, and D. Neri Bioorg. Med. Chem. Lett. 19 2009 4851
16. F. Pacchiano, F. Carta, P.C. McDonald, Y. Lou, D. Vullo, A. Scozzafava, S. Dedhar, and C.T. Supuran J. Med. Chem. 54 2011 1896
17. M. Hilvo, L. Baranauskiene, A.M. Salzano, A. Scaloni, D. Matulis, A. Innocenti, A. Scozzafava, S.M. Monti, A. Di Fiore, G. De Simone, M. Lindfors, J. Janis, J. Valjakka, S. Pastorekova, J. Pastorek, M.S. Kulomaa, H.R. Nordlund, C.T. Supuran, and S. Parkkila J. Biol. Chem. 283 2008 27799
18. Lou, Y.; McDonald, P. C.; Oloumi, A.; Chia, S. K.; Ostlund, C.; Ahmadi, A.; Kyle, A.; Auf dem Keller, U.; Leung, S.; Huntsman, D. G.; Clarke, B.; Sutherland, B. W.; Waterhouse, D.; Bally, M. B.; Roskelley, C. D.; Overall, C. M.; Minchinton, A.; Pacchiano, F.; Carta, F.; Scozzafava, A.; Touisni, N.; Winum, J. Y.; Supuran, C. T.; Dedhar, S. Cancer Res. 2011, in press (Epub Mar 17, 2011).
19. M. Bartosova, S. Parkkila, K. Pohlodek, T.J. Karttunen, S. Galbavy, V. Mucha, A.L. Harris, J. Pastorek, and S. Pastorekova J. Pathol. 197 2002 1
20. S. Pastoreková, J. Pastorek Cancer-related Carbonic Anhydrase Isozymes and their Inhibition C.T. Supuran, A. Scozzafava, and J. Conway Carbonic Anhydrase: Its Inhibitors and Activators 2004 CRC Press Boca Raton, FL 255 281
21. P. Ebbesen, E.O. Pettersen, T.A. Gorr, G. Jobst, K. Williams, J. Kienninger, R.H. Wenger, S. Pastorekova, L. Dubois, P. Lambin, B.G. Wouters, C.T. Supuran, L. Poellinger, P. Ratcliffe, A. Kanopka, A. Görlach, M. Gasmann, A.L. Harris, P. Maxwell, and A. Scozzafava J. Enzyme Inhib. Med. Chem. 24 2009 1
22. M.S. Kyllönen, S. Parkkila, H. Rajaniemi, A. Waheed, J.H. Grubb, G.N. Shah, and W.S. Sly J. Histochem. Cytochem. 51 2003 1217
23. D.A. Whittington, J.H. Grubb, A. Waheed, G.N. Shah, W.S. Sly, and D.W. Christianson J. Biol. Chem. 279 2004 7223
24. K. D'Ambrosio, R.M. Vitale, J.M. Dogné, B. Masereel, A. Innocenti, A. Scozzafava, G. De Simone, and C.T. Supuran J. Med. Chem. 51 2008 3230
25. C. Temperini, A. Cecchi, N.A. Boyle, A. Scozzafava, J.E. Cabeza, P. Wentworth, G.M. Blackburn, and C.T. Supuran Bioorg. Med. Chem. Lett. 18 2008 999
26. J.R. Casey, P.E. Morgan, D. Vullo, A. Scozzafava, A. Mastrolorenzo, and C.T. Supuran J. Med. Chem. 47 2004 2337
27. M. Feldshtein, S. Elkrinawi, B. Yerushalmi, B. Marcus, D. Vullo, H. Romi, R. Ofir, D. Landau, S. Sivan, C.T. Supuran, and O.S. Birk Am. J. Hum. Genet. 87 2010 713
28. D. Vullo, A. Innocenti, I. Nishimori, J. Pastorek, A. Scozzafava, S. Pastorekova, and C.T. Supuran Bioorg. Med. Chem. Lett. 15 2005 963
29. I. Nishimori, D. Vullo, A. Innocenti, A. Scozzafava, A. Mastrolorenzo, and C.T. Supuran Bioorg. Med. Chem. Lett. 15 2005 3828
30. D. Vullo, J. Voipio, A. Innocenti, C. Rivera, H. Ranki, A. Scozzafava, K. Kaila, and C.T. Supuran Bioorg. Med. Chem. Lett. 15 2005 971
31. R.G. Khalifah J. Biol. Chem. 246 1971 2561
32. R.A. Hall, and F.A. Mühlschlegel Fungal and Nematode Carbonic Anhydrases: Their Inhibition in Drug Design C.T. Supuran, J.Y. Winum, Drug Design of Zinc-Enzyme Inhibitors: Functional, Structural, and Disease Applications 2009 John Wiley & Sons Hoboken 301 322
33. U.M. Ohndorf, C. Schlicker, and C. Steegborn Crystallographic Studies on Carbonic Anhydrases from Fungal Pathogens for Structure-assisted Drug Development C.T. Supuran, J.Y. Winum, Drug Design of Zinc-Enzyme Inhibitors: Functional, Structural, and Disease Applications 2009 John Wiley & Sons Hoboken 323 334
34. P. Burghout, D. Vullo, A. Scozzafava, P.W.M. Hermans, and C.T. Supuran Bioorg. Med. Chem. 19 2011 243
35. C.T. Supuran Curr. Pharm. Des. 16 2010 3233
36. I. Nishimori, T. Minakuchi, A. Maresca, F. Carta, A. Scozzafava, and C.T. Supuran Curr. Pharm. Des. 16 2010 3300
37. J.Y. Winum, S. Kohler, and C.T. Supuran Curr. Pharm. Des. 16 2010 3310
38. V. Alterio, A. Di Fiore, K. D'Ambrosio, C.T. Supuran, G. De Simone C.T. Supuran, and J.Y. Winum X-ray Crystallography of CA Inhibitors and its Importance in Drug Design of Zinc-Enzyme Inhibitors: Functional, Structural, and Disease Applications 2009 Wiley Hoboken 73 138
39. B.S. Avvaru, J.M. Wagner, A. Maresca, A. Scozzafava, A.H. Robbins, C.T. Supuran, and R. McKenna Bioorg. Med. Chem. Lett. 20 2010 4376
40. J.Y. Winum, C. Temperini, K. El Cheikh, A. Innocenti, D. Vullo, S. Ciattini, J.L. Montero, A. Scozzafava, and C.T. Supuran J. Med. Chem. 49 2006 7024
41. J.M. Wagner, B.S. Avvaru, A.H. Robbins, A. Scozzafava, C.T. Supuran, and R. McKenna Bioorg. Med. Chem. 18 2010 4873
42. F. Pacchiano, M. Aggarwal, B.S. Avvaru, A.H. Robbins, A. Scozzafava, R. McKenna, and C.T. Supuran Chem. Commun. (Camb.) 46 2010 8371
43. K. Köhler, A. Hillebrecht, J.S. Wischeler, A. Innocenti, A. Heine, C.T. Supuran, and G. Klebe Angew. Chem., Int. Ed. 46 2007 7697
44. E. Eriksson, T.A. Jones, and A. Liljas Proteins: Struct. Funct., Genet. 4 1988 274
45. C.T. Supuran, and A. Scozzafava J. Enzyme Inhib. 14 1999 343
46. J.D. McKerrow, J.M.A. Al-Rawi, and P. Brooks Synth. Commun. 40 2010 1161
47. P.A. Procopiou, V.J. Barrett, N.J. Bevan, K. Biggadike, P.C. Box, P.R. Butchers, D.M. Coe, R. Conroy, A. Emmons, A.J. Ford, D.S. Holmes, H. Horsley, F. Kerr, A.-M. Li-Kwai-Cheung, B.E. Looker, I.S. Mann, I.M. McLay, V.S. Morrison, P.J. Mutch, C.E. Smith, and P. Tomlin J. Med. Chem. 53 2010 4522
48. C.A. Forsman, G. Behravan, A. Osterman, and B.H. Jonsson Acta Chem. Scand. 42 1988 314
49. R.G. Khalifah, D.J. Strader, S.H. Bryant, and S.M. Gibson Biochemistry 16 1977 2241
50. st Ed., 1982, Wiley, New York.
51. S.Z. Fisher, C.M. Maupin, M. Budayova-Spano, L. Govindasamy, C.K. Tu, M. Agbandje-McKenna, D.N. Silverman, G.A. Voth, and R. McKenna Biochemistry 42 2007 2930 2937
52. Z. Otwinowski, and W. Minor Methods Enzymol. 276 1997 307
53. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, R.W. Grosse-Kunstleve, A.J. McCoy, N.W. Moriarty, R. Oeffner, R.J. Read, D.C. Richardson, J.S. Richardson, T.C. Terwilliger, and P.H. Zwart Acta Crystallogr., Sect. D 66 2010 213
54. A.W. Schuettelkopf, and D.M.F. van Aalten Acta Crystallogr., Sect. D D60 2004 1355
55. P. Emsley, and K. Cowtan Acta Crystallogr., Sect. D 60 2004 2126
56. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton J. Appl. Crystallogr. 26 1993 283