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BioMed Research International
Volume 2014 (2014), Article ID 523210, 11 pages
http://dx.doi.org/10.1155/2014/523210
Research Article

Hydrophobic Substituents of the Phenylmethylsulfamide Moiety Can Be Used for the Development of New Selective Carbonic Anhydrase Inhibitors

1Istituto di Biostrutture e Bioimmagini, CNR, Via Mezzocannone 16, 80134 Naples, Italy
2Latvian Institute of Organic Synthesis, Aizkraukles 21, Riga LV-1006, Latvia
3Laboratorio di Chimica Bioinorganica, Università degli Studi di Firenze, Room 188, Via della Lastruccia 3, 50019 Sesto Fiorentino, Florence, Italy
4Dipartimento di Scienze Farmaceutiche, Università degli Studi di Firenze, Polo Scientifico, Via Ugo Schiff 6, 50019 Sesto Fiorentino, Florence, Italy

Received 28 February 2014; Accepted 13 April 2014; Published 2 September 2014

Academic Editor: Mariya Al-Rashida

Copyright © 2014 Giuseppina De Simone et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. V. Alterio, A. di Fiore, K. D'Ambrosio, C. T. Supuran, and G. de Simone, “Multiple binding modes of inhibitors to carbonic anhydrases: how to design specific drugs targeting 15 different isoforms?” Chemical Reviews, vol. 112, no. 8, pp. 4421–4468, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. C. T. Supuran, “Carbonic anhydrases: novel therapeutic applications for inhibitors and activators,” Nature Reviews Drug Discovery, vol. 7, no. 2, pp. 168–181, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. C. T. Supuran and A. Scozzafava, “Carbonic anhydrases as targets for medicinal chemistry,” Bioorganic and Medicinal Chemistry, vol. 15, no. 13, pp. 4336–4350, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. C. T. Supuran, “Carbonic anhydrases as drug targets—general presentation,” in Drug Design of Zinc-Enzyme Inhibitors: Functional, Structural, and Disease Applications, J.-Y. Winum, Ed., pp. 15–38, John Wiley & Sons, Hoboken, NJ, USA, 2009. View at Google Scholar
  5. J.-Y. Winum, M. Rami, A. Scozzafava, J.-L. Montero, and C. T. Supuran, “Carbonic anhydrase IX: a new druggable target for the design of antitumor agents,” Medicinal Research Reviews, vol. 28, no. 3, pp. 445–463, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. C. T. Supuran, A. Scozzafava, and A. Casini, “Carbonic anhydrase inhibitors,” Medicinal Research Reviews, vol. 23, no. 2, pp. 146–189, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Winum, D. Vullo, A. Casini, J. Montero, A. Scozzafava, and C. T. Supuran, “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,” Journal of Medicinal Chemistry, vol. 46, no. 11, pp. 2197–2204, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Winum, D. Vullo, A. Casini, J. Montero, A. Scozzafava, and C. T. Supuran, “Carbonic anhydrase inhibitors: inhibition of transmembrane, tumor-associated isozyme IX, and cytosolic isozymes I and II with aliphatic sulfamates,” Journal of Medicinal Chemistry, vol. 46, no. 25, pp. 5471–5477, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. J.-Y. Winum, A. Scozzafava, J.-L. Montero, and C. T. Supuran, “Therapeutic potential of sulfamides as enzymes inhibitors,” Medicinal Research Reviews, vol. 26, no. 6, pp. 767–792, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. J.-Y. Winum, A. Scozzafava, J.-L. Montero, and C. T. Supuran, “The sulfamide motif in the design of enzyme inhibitors,” Expert Opinion on Therapeutic Patents, vol. 16, no. 1, pp. 27–47, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Scozzafava, M. D. Banciu, A. Popescu, and C. T. Supuran, “Carbonic anhydrase inhibitors: inhibition of isozymes I, II and IV by sulfamide and sulfamic acid derivatives,” Journal of Enzyme Inhibition and Medicinal Chemistry, vol. 15, no. 5, pp. 443–453, 2000. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Casini, J. Winum, J. Montero, A. Scozzafava, and C. T. Supuran, “Carbonic anhydrase inhibitors: inhibition of cytosolic isozymes I and II with sulfamide derivatives,” Bioorganic and Medicinal Chemistry Letters, vol. 13, no. 5, pp. 837–840, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Casini, J. Antel, F. Abbate et al., “Carbonic anhydrase inhibitors: SAR and X-ray crystallographic study for the interaction of sugar sulfamates/sulfamides with isozymes I, II and IV,” Bioorganic and Medicinal Chemistry Letters, vol. 13, no. 5, pp. 841–845, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. J. Winum, A. Innocenti, J. Nasr et al., “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,” Bioorganic and Medicinal Chemistry Letters, vol. 15, no. 9, pp. 2353–2358, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. J.-Y. Winum, A. Cecchi, J.-L. Montero, A. Innocenti, A. Scozzafava, and C. T. Supuran, “Carbonic anhydrase inhibitors. Synthesis and inhibition of cytosolic/tumor-associated carbonic anhydrase isozymes I, II, and IX with boron-containing sulfonamides, sulfamides, and sulfamates: toward agents for boron neutron capture therapy of hypoxic tumors,” Bioorganic and Medicinal Chemistry Letters, vol. 15, no. 13, pp. 3302–3306, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. F. Abbate, C. T. Supuran, A. Scozzafava, P. Orioli, M. T. Stubbs, and G. Klebe, “Nonaromatic sulfonamide group as an ideal anchor for potent human carbonic anhydrase inhibitors: role of hydrogen-bonding networks in ligand binding and drug design,” Journal of Medicinal Chemistry, vol. 45, no. 17, pp. 3583–3587, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Winum, C. Temperini, K. El Cheikh et al., “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, vol. 49, no. 24, pp. 7024–7031, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. C. Temperini, J. Winum, J. Montero, A. Scozzafava, and C. T. Supuran, “Carbonic anhydrase inhibitors: The X-ray crystal structure of the adduct of N-hydroxysulfamide with isozyme II explains why this new zinc binding function is effective in the design of potent inhibitors,” Bioorganic and Medicinal Chemistry Letters, vol. 17, no. 10, pp. 2795–2801, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. R. E. Marquis and J. T. Whitson, “Management of glaucoma: Focus on pharmacological therapy,” Drugs and Aging, vol. 22, no. 1, pp. 1–21, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. D. Vullo, A. Innocenti, I. Nishimori et al., “Carbonic anhydrase inhibitors. Inhibition of the transmembrane isozyme XII with sulfonamides—a new target for the design of antitumor and antiglaucoma drugs?” Bioorganic and Medicinal Chemistry Letters, vol. 15, no. 4, pp. 963–969, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. C. T. Supuran, A. Casini, and A. Scozzafava, “Development of sulfonamide carbonic anhydrase inhibitors (CAIs),” in Carbonic Anhydrase—Its Inhibitors and Activators, C. T. Supuran, A. Scozzafava, and J. Conway, Eds., pp. 67–148, CRC Press, Boca Raton, Fla, USA, 2004. View at Google Scholar
  22. F. Fabrizi, F. Mincione, T. Somma et al., “A new approach to antiglaucoma drugs: carbonic anhydrase inhibitors with or without NO donating moieties. Mechanism of action and preliminary pharmacology,” Journal of Enzyme Inhibition and Medicinal Chemistry, vol. 27, no. 1, pp. 138–147, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. F. B. Loiselle, P. E. Morgan, B. V. Alvarez, and J. R. Casey, “Regulation of the human NBC3 Na+/HCO3- cotransporter by carbonic anhydrase II and PKA,” The American Journal of Physiology—Cell Physiology, vol. 286, no. 6, pp. C1423–C1433, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Rivera, J. Voipio, and K. Kaila, “Two developmental switches in GABAergic signalling: the K+-Cl- cotransporter KCC2 and carbonic anhydrase CAVII,” Journal of Physiology, vol. 562, no. 1, pp. 27–36, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. D. Vullo, J. Voipio, A. Innocenti et al., “Carbonic anhydrase inhibitors. Inhibition of the human cytosolic isozyme VII with aromatic and heterocyclic sulfonamides,” Bioorganic and Medicinal Chemistry Letters, vol. 15, no. 4, pp. 971–976, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. K. E. Lyons, R. Pahwa, C. L. Comella et al., “Benefits and risks of pharmacological treatments for essential tremor,” Drug Safety, vol. 26, no. 7, pp. 461–481, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Hori, S. Ishida, M. Inoue et al., “Treatment of cystoid macular edema with oral acetazolamide in a patient with best vitelliform macular dystrophy,” Retina, vol. 24, no. 3, pp. 481–482, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. C. T. Supuran, “Carbonic anhydrase inhibitors in the treatment and prophylaxis of obesity,” Expert Opinion on Therapeutic Patents, vol. 13, no. 10, pp. 1545–1550, 2003. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Y. Winum, A. Scozzafava, J. L. Montero, and C. T. Supuran, “Sulfamates and their therapeutic potential,” Medicinal Research Reviews, vol. 25, no. 2, pp. 186–228, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. E. Švastová, A. Hulíková, M. Rafajová et al., “Hypoxia activates the capacity of tumor-associated carbonic anhydrase IX to acidify extracellular pH,” FEBS Letters, vol. 577, no. 3, pp. 439–445, 2004. View at Google Scholar
  31. G. Splendiani and S. Condò, “Diuretic therapy in heart failure,” Giornale Italiano di Nefrologia, vol. 23, pp. S74–S76, 2006. View at Google Scholar · View at Scopus
  32. K. M. Gadde, D. B. Allison, D. H. Ryan et al., “Effects of low-dose, controlled-release, phentermine plus topiramate combination on weight and associated comorbidities in overweight and obese adults (CONQUER): a randomised, placebo-controlled, phase 3 trial,” The Lancet, vol. 377, no. 9774, pp. 1341–1352, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. W. F. Brechue and T. H. Maren, “A comparison between the effect of topical and systemic carbonic anhydrase inhibitors on aqueous humor secretion,” Experimental Eye Research, vol. 57, no. 1, pp. 67–78, 1993. View at Publisher · View at Google Scholar · View at Scopus
  34. V. Alterio, A. di Fiore, K. D’Ambrosio, C. T. Supuran, and G. de Simone, “X-ray crystallography of CA inhibitors and its importance in drug design,” in Drug Design of Zinc-Enzyme Inhibitors: Functional, Structural, and Disease Applications, C. T. Supuran and J. Y. Winum, Eds., pp. 73–138, John Wiley & Sons, Hoboken, NJ, USA, 2009. View at Google Scholar
  35. B. E. Maryanoff, D. F. McComsey, M. J. Costanzo, C. Hochman, V. Smith-Swintosky, and R. P. Shank, “Comparison of sulfamate and sulfamide groups for the inhibition of carbonic anhydrase-II by using topiramate as a structural platform,” Journal of Medicinal Chemistry, vol. 48, no. 6, pp. 1941–1947, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. A. L. Klinger, D. F. McComsey, V. Smith-Swintosky, R. P. Shank, and B. E. Maryanoff, “Inhibition of carbonic anhydrase-II by sulfamate and sulfamide groups: An investigation involving direct thermodynamic binding measurements,” Journal of Medicinal Chemistry, vol. 49, no. 12, pp. 3496–3500, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Di Fiore, S. M. Monti, A. Innocenti, J. Winum, G. de Simone, and C. T. Supuran, “Carbonic anhydrase inhibitors: crystallographic and solution binding studies for the interaction of a boron-containing aromatic sulfamide with mammalian isoforms I-XV,” Bioorganic and Medicinal Chemistry Letters, vol. 20, no. 12, pp. 3601–3605, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Rami, L. Dubois, N.-K. Parvathaneni et al., “Hypoxia-targeting carbonic anhydrase IX inhibitors by a new series of nitroimidazole-sulfonamides/sulfamides/sulfamates,” Journal of Medicinal Chemistry, vol. 56, no. 21, pp. 8512–8520, 2013. View at Google Scholar
  39. A. F. Abdel-Magid and S. J. Mehrman, “Process for preparation of sulfamide derivatives,” Patent Cooperation Treaty International Application WO 2006/127184 A1, 2006. View at Google Scholar
  40. O. Mitsunobu, “The use of diethyl azodicarboxylate and triphenylphosphine in synthesis and transformation of natural products,” Synthesis, vol. 1, no. 1, pp. 1–28, 1981. View at Publisher · View at Google Scholar
  41. R. G. Khalifah, “The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C.,” The Journal of Biological Chemistry, vol. 246, no. 8, pp. 2561–2573, 1971. View at Google Scholar · View at Scopus
  42. A. E. Eriksson, T. A. Jones, and A. Liljas, “Refined structure of human carbonic anhydrase II at 2.0 Å resolution,” Proteins: Structure, Function and Genetics, vol. 4, no. 4, pp. 274–282, 1988. View at Publisher · View at Google Scholar · View at Scopus
  43. F. Pacchiano, M. Aggarwal, B. S. Avvaru et al., “Selective hydrophobic pocket binding observed within the carbonic anhydrase II active site accommodate different 4-substituted-ureido-benzenesulfonamides and correlate to inhibitor potency,” Chemical Communications, vol. 46, no. 44, pp. 8371–8373, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. V. Alterio, M. Hilvo, A. Di Fiore et al., “Crystal structure of the catalytic domain of the tumor-associated human carbonic anhydrase IX,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 38, pp. 16233–16238, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. D. A. Whittington, A. Waheed, B. Ulmasov et al., “Crystal structure of the dimeric extracellular domain of human carbonic anhydrase XII, a bitopic membrane protein overexpressed in certain cancer tumor cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 17, pp. 9545–9550, 2001. View at Publisher · View at Google Scholar · View at Scopus
  46. K. K. Kannan, M. Ramanadham, and T. A. Jones, “Structure, refinement, and function of carbonic anhydrase isozymes: Refinement of human carbonic anhydrase I,” Annals of the New York Academy of Sciences, vol. 429, pp. 49–60, 1984. View at Publisher · View at Google Scholar · View at Scopus
  47. V. Alterio, S. M. Monti, E. Truppo, C. Pedone, C. T. Supuran, and G. de Simone, “The first example of a significant active site conformational rearrangement in a carbonic anhydrase-inhibitor adduct: the carbonic anhydrase I-topiramate complex,” Organic and Biomolecular Chemistry, vol. 8, no. 15, pp. 3528–3533, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. Y. Wang, M. Papamichelakis, W. Chew et al., “Development of a suitable process for the preparation of a TNF-α converting enzyme inhibitor, WAY-281418,” Organic Process Research and Development, vol. 12, no. 6, pp. 1253–1260, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. P. Joseph, F. Turtaut, S. Ouahrani-Bettache et al., “Cloning, characterization, and inhibition studies of a β-carbonic anhydrase from brucella suis,” Journal of Medicinal Chemistry, vol. 53, no. 5, pp. 2277–2285, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. P. Pan, G. C. Rodrigues, A. Scozzafava et al., “Cloning, characterization, and sulfonamide and thiol inhibition studies of an α-carbonic anhydrase from Trypanosoma cruzi, the causative agent of Chagas disease,” Journal of Medicinal Chemistry, vol. 56, no. 4, pp. 1761–1771, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Minakuchi, I. Nishimori, D. Vullo, A. Scozzafava, and C. T. Supuran, “Molecular cloning, characterization, and inhibition studies of the Rv1284 beta-carbonic anhydrase from Mycobacterium tuberculosis with sulfonamides and a sulfamate,” Journal of Medicinal Chemistry, vol. 52, no. 8, pp. 2226–2232, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. Z. Otwinowski and W. Minor, “Processing of X-ray diffraction data collected in oscillation mode,” Methods in Enzymology, vol. 276, pp. 307–326, 1997. View at Publisher · View at Google Scholar · View at Scopus
  53. A. T. Brünger, P. D. Adams, G. M. Clore et al., “Crystallography & NMR system: a new software suite for macromolecular structure determination,” Acta Crystallographica Section D, vol. 54, no. 5, pp. 905–921, 1998. View at Publisher · View at Google Scholar · View at Scopus
  54. T. A. Jones, J. Y. Zou, and S. W. Cowan, “Improved methods for building protein models in electron density maps and the location of errors in these models,” Acta Crystallographica A: Foundations of Crystallography, vol. 47, no. 2, pp. 110–119, 1991. View at Publisher · View at Google Scholar · View at Scopus
  55. F. H. Allen, “The Cambridge Structural Database: a quarter of a million crystal structures and rising,” Acta Crystallographica Section B: Structural Science, vol. 58, no. 3, pp. 380–388, 2002. View at Publisher · View at Google Scholar · View at Scopus
  56. R. A. Laskowski, M. W. MacArthur, D. S. Moss, and J. M. Thornton, “PROCHECK: a program to check the stereochemical quality of protein structures,” Journal of Applied Crystallography, vol. 26, no. 2, pp. 283–291, 1993. View at Google Scholar