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

Volumn 46, Issue 11, 2003, Pages 2197-2204

  Winum, Jean Yves ^a   Vullo, Daniela ^b   Casini, Angela ^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

4 CHLOROPHENYLSULFAMATE; ACETAZOLAMIDE; CARBONATE DEHYDRATASE I; CARBONATE DEHYDRATASE II; CARBONATE DEHYDRATASE INHIBITOR; ENZYME INHIBITOR; ETHOXZOLAMIDE; ISOENZYME; METHAZOLAMIDE; OCTYLSULFAMATE; PHENYLSULFAMATE; PRASTERONE SULFATE; STERYL SULFATASE; STERYL SULFATASE INHIBITOR; SULFAMIC ACID; TOPIRAMATE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CHEMOTHERAPY; CANCER RADIOTHERAPY; CARCINOGENICITY; DRUG DESIGN; DRUG EFFECT; DRUG POTENCY; DRUG SYNTHESIS; GENE OVEREXPRESSION;

ANTIGENS, NEOPLASM; ARYLSULFATASES; CARBONIC ANHYDRASE I; CARBONIC ANHYDRASE II; CARBONIC ANHYDRASES; CYTOSOL; ENZYME INHIBITORS; ESTRONE; HUMANS; MEMBRANE PROTEINS; NEOPLASM PROTEINS; STERYL-SULFATASE; STRUCTURE-ACTIVITY RELATIONSHIP; SULFONIC ACIDS; TUMOR MARKERS, BIOLOGICAL;

EID: 0038587356     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm021124k     Document Type: Article

References (61)

1. Supuran, C. T.; Scozzafava, A. Applications of carbonic anhydrase inhibitors and activators in therapy. Exp. Opin. Ther. Pat. 2002, 12, 217-242.
2. Supuran, C. T.; Scozzafava, A. Carbonic anhydrase inhibitors. Curr. Med. Chem. Immunol., Endoc. Metab. Agents 2001, 1, 61-97.
3. Supuran C. T.; Scozzafava, A. Carbonic anhydrase inhibitors and their therapeutic potential. Exp. Opin. Ther. Pat. 2000,10, 575- 600.
4. Abbate, F.; Supuran, C. T.; Scozzafava, A.; Orioli, P.; Stubbs, M.; Klebe, G. Nonaromatic sulfonamide group as an ideal anchor for potent human carbonic anhvdrase inhibitors: Role of hydrogen-bonding networks in ligand binding and drug design. J. Med. Chem. 2002, 45, 3583-3587.
5. 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.
6. Casini, A.; Antel, J.; Abbate, F.; Davids, S.; Waldeck, H.; Scozzafava, A.; 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.
7. (a) Smith, H. J.; Nicholls, P. J.; Simons, C.; Le Lain, R. Inhibitors of steroidogenesis as agents for the treatment of hormone-dependent cancers. Exp. Opin. Ther. Pat. 2001, 11, 789-824.
8. (b) Ahmed, S.; Owen, C. P.; James, K.; Sampson, L.; Patel, C. K. Review of estrone sulfatase and its inhibitors-an important new target against hormone dependent breast cancer. Curr. Med. Chem. 2002, 9, 263-273.
9. (a) Woo, L. W. L.; Purohit, A.; Malini, B.; Reed, M. J.; Potter, B. V. L. Potent active site-directed inhibition of steroid sulphatase by tricyclic coumarin-based sulphamates. Chem. Biol. 2000, 7, 773-791.
10. (b) Poirier, D.; Ciobanu, L. C.; Maltais, R. Steroid sulfatase inhibitors. Exp. Opin. Ther. Pat. 1999, 9, 1083-1099.
11. (c) Ciobanu, L. C.; Luu-The, V.; Poirier, D. Nonsteroidal compounds designed to mimic potent steroid sulfatase inhibitors. J. Steroid Biochem. Mol. Biol. 2002, 80, 339-353.
12. (d) Malini, B.; Purohit, A.; Ganeshapillai, D.; Woo, L. W.; Potter, B. V.; Reed, M. J. Inhibition of steroid sulphatase activity by tricyclic coumrnarin sulphamates. J. Steroid Biochem. Mol. Biol. 2000, 75, 253-258.
13. Ahmed, S.; James, K.; Owen, C. P. inhibition of estrone sulfatase (ES) by derivatives of 4-[(aminosulfonyl)oxy]benzoic acid. Bioorg. Med. Chem. Lett 2002, 12, 2391-2394.
14. (b) Ahmed, S.; James, K.; Owen, C. P.; Patel, C. K.; Sampson, L. The mechanism of irreversible inhibition of estrone sulfatase (ES) through the consideration of a range of methane- and amino-sulfonate-based compounds. Bioorg. Med. Chem. Lett 2002, 12, 1279-1282.
15. (c) Ahmed, S.; Owen, C. P.; James, K.; Patel, C. K.; Patel, M. Acid dissociation constant, a potential physicochemical factor in the inhibition of the enzyme estrone sulfatase (ES). Bioorg. Med. Chem. Lett. 2001, 11, 899-902.
16. (d) Ahmed, S.; James, K.; Owen, C. P.; Patel, C. K. Design, synthesis and biochemical evaluation of AC ring mimics s novel inhibitors of the enzyme estrone sulfatase. Bioorg. Med. Chem. Lett. 2002, 12, 1343-1346.
17. (e) Ahmed, S.; Owen, C. P.; James, K.; Patel, C. K.; Patel, M. Novel inhibitors of the enzyme estrone sulfatase (ES). Bioorg. Med. Chem. Lett. 2001, 11, 841-844.
18. Golob, T.; Liebl, R.; von Angerer, E. Sulfamoyloxy-substituted 2-phenylindoles: Antiestrogen- based inhibitors of the steroid sulfatase in human breast cancer cells. Bioorg. Med. Chem. 2002, 10, 3941-3953.
19. (a) Nussbaumer, P.; Bilban, M.; Billich, A. 4,4′-Benzophenone-O,O′-disulfamate: a potent inhibitor of steroid sulfatase. Bioorg. Med. Chem. Lett. 2002, 12, 2093-2095.
20. (b) Nussbaumer, P.; Lehr, P.; Billich, A. 2-Substituted 4-(thio)chromenone 6-O-sulfamates: potent inhibitors of human steroid sulfatase. J. Med. Chem. 2002, 45, 4310-4320.
21. Hernandez-Guzman, F. G.; Higashiyama, T.; Osawa, Y.; Ghosh, D. Purification, characterization and crystallization of human placental estrone/dehydroepiandrosterone sulfatase, a membrane-bound enzyme of the endoplasmic reticulum. J. Steroid Biochem. Mol. Biol. 2001, 78, 441-450.
22. Hoffmann, R.; Happle, R. Current understanding of androgenetic alopecia. Part I: ethiopathogenesis. Eur. J. Dermatol. 2000, 10, 319-327.
23. Wolf, O. T.; Kirschbaum, C. Actions of dehydroepiandrosterone and its sulfate in central nervous system: effect on cognition and emotion in animals and humans. Brain Res. Rev. 1999, 30, 264-288.
24. Suitters, A. J.; Shaw, S.; Wales, M. R.; Porter, J. P.; Leonard, J.; Woodger, R.; Brand, H.; Bodmer, M.; Foulkes, R. Immune enhancing effects of dehydroepiandrosterone and dehydroepiandrosterone sulphate and the role of steroid sulfatase. Immunology 1997, 91, 314-321.
25. Chegwidden, W. R.; Spencer, I. M.; Supuran, C. T. The roles of carbonic anhydrase isozymes in cancer. In Gene Families: Studies of DNA, RNA, Enzymes and Proteins; Xue, G., Xue, Y., Xu, Z., Holmes, R., Hammond, G. L., Lim, H. A., Eds.; World Scientific: Singapore, 2001; pp 157-170.
26. Winum, J.-Y.; Toupet, L.; Barragan, V.; Dewynter, G.; Montero, J.-L. N-(tert-Butoxycarbonyl)-N-[4-(dimethylazaniumylidene)- 1,4-dihydropyridin-1-ylsulfonyl]azanide: a new sulfamoylating agent. Structure and reactivity towards amines. Org. Lett. 2002, 3, 2241-2243.
27. Okada, M.; Iwashita, S.; Koizumi, N. Efficient general method for sulfamoylation of a hydroxyl group. Tetrahedron Lett. 2000, 41, 7057-7051.
28. Appel, R.; Berger, G. Hydrazinsulfonsaiire-amide, I. Uber das hydrazodisulfamid. Chem. Ber. 1958, 91, 1339-1341.
29. Hedayatullah, M.; Guy, A. Synthese et reduction d'azidosulfates d'aryle. Tetrahedron Lett. 1975, 29, 2455-2458.
30. Lohaus, G. Preparation and reactions of aryloxysulfonyl isocyantes. Chem. Ber. 1972, 105, 2791-2799.
31. Spillane, W. J.; Hogan, G.; McGrath, P. Aminolysis and hydrolysis of sulfamate esters: substantial N=S bonding in the transition state leading to N=sulfonylamines. J. Phys. Org. Chem. 1995, 8, 610-616.
32. Eberhard, O.; Roman, M. Sulfamic acid esters. German Patent 2,418,217, 1975. [Chem. Abstr. 1976, 84, 16980q].
33. Schwarz, S.; Thieme, I.; Richter, M.; Undeutsch, B.; Henkel, H.; Elger, W. Synthesis of estrogen sulfamates: compounds with a novel endocrinological profile. Steroids 1996, 61, 710-717.
34. Römer, J.; Steinbach, J.; Kasch, H.; Scheller, D. Preparation and Characterization of the sulphamates of estra-3,17β-diols. Rapid conversion of 16α-fluoroestradiol into 16α-fluoroestradiol-3,17β-disulphamates J. Prakt. Chem. 1999, 341, 574-583.
35. Kochetkov, N. K.; Usov, A. I.; Deryabin, V. V. Monosaccharides XXVIII. Synthesis of monosaccharide sulfamates from salts of monosaccharide hydrogen sulfates. J. Gen. Chem. USSR (Engl. Transl.) 1972, 42, 2755-2757.
36. Lo, Y. S.; Nolan, J. C.; Maren, T. H.; Welstead, W. J.; Gripshover, D. F.; Shamblee, D. A. Synthesis and physicochemical properties of sulfamate derivatives as topical antglaucoma agents. J. Med. Chem. 1992, 35, 4790-4794.
37. Lindskog, S.; Behravan, G.; Engstrand, C.; Forsman, C.; Jonsson, B. H.; Liang, Z.; Ren, X.; Xue, Y. Structure- function relations in human carbonic anhydrase II as studied by site-directed mutagenesis. In Carbonic anhydrase - From biochemistry and genetics to physiology and clinical medicine; Botrè, F., Gros, G., Storey, B. T., Eds.; VCH: Weinheim, 1991; pp 1-13.
38. Behravan, G.; Jonsson, B. H.; Lindskog, S. Fine-tuning of the catalytic properties of carbonic anhydrase. Studies of a Thr200- His variant of human isoenzyme II. Eur. J. Biochem. 1990, 190, 351-357.
39. Khalifah, R. G.; Strader, D. J.; Bryant, S. H.; Gibson, S. M. Carbon-13 nuclear magnetic resonance probe of active site ionization of human carbonic anhydrase B. Biochemistry 1977, 16, 2241-2247.
40. Lindskog, S.; Coleman, J. E. The catalytic mechanism of carbonic anhydrase. Proc. Natl. Acad. Sci. U.S.A. 1964, 70, 2505-2508.
41. Steiner, H.; Jonsson, B. H.; Lindskog, S. The catalytic mechanism of carbonic anhydrase. Hydrogen-isotope effects on the kinetic parameters of the human C isoenzyme. Eur. J. Biochem. 1975, 59, 253-259.
42. Pastorek, J.; Pastorekova, S.; Callebaut, I.; Mornon, J. P.; Zelnik, V.; Opavsky, R.; Zatovicova, M.; Liao, S.; Portetelle, D.; Stanbridge, E. J.; Zavada, J.; Bumy, A.; Kettmann, R. Cloning and characterization of MN, a human tumor-associated protein with a domain homologous to carbonic anhydrase and a putative helix-loop-helix DNA binding segment. Oncogene 1994, 9, 2877-2888.
43. Wingo, T.; Tu, C.; Laipis, P. J.; Silverman, D. N. The catalytic properties of human carbonic anhydrase IX. Biochem. Biophys. Res. Commun. 2001, 288, 666-669.
44. Pocker, Y.; Stone, J. T. The catalytic versatility of erythrocyte carbonic anhydrase. III. Kinetic studies of the enzyme-catalyzed hydrolysis ofp-nitrophenyl acetate. Biochemistry 1967, 6, 668-678.
45. Khalifah, R. G. The carbon dioxide hydration activity of carbonic anhydrase. J. Biol. Chem. 1971, 246, 2561-2573.
46. (a) Wykoff, C. C.; Beasley, N.; Watson, P. H.; Turner, K. J.; Pastorek, J.; Sibtain, A.; Wilson, G. D.; Turley, H.; Talks, K. L.; Maxwell, P. H.; Pugh, C. W.; Ratcliffe, P.; Harris, A. L. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res. 2000, 60, 7075-7083.
47. (b) Höckel, M.; Vaupel, P. Tumor hypoxia: definitions and current clinical, biologic and molecular aspects. J. Natl. Cancer Inst. 2001, 93, 266-276.
48. (a) Loncaster, J. A.; Harris, A. L.; Davidson, S. E.; Logue, J. P.; Hunter, R. D.; Wykoff, C. C.;Pastorek, J.; Ratcliffe, P. J.; Stratford, I. J.; West, C. M. Carbonic anhydrase (CA IX) expression, a potential new intrinsic marker of hypoxia: correlations with tumor oxygen measurements and prognosis in locally advanced carcinoma of the cervix. Cancer Res. 2001, 61, 6394-6399.
49. (b) Chia, S. K.; Wykoff, C. C.; Watson, P. H.; Han, C.; Leek, R. D.; Pastorek, J.; Gatter, K. C.; Ratcliffe, P.; Harris, A. L. Prognostic significance of a novel hypoxia-regulated marker, carbonic anhydrase IX, in invasive breast carcinoma. J. Clin. Oncol. 2001, 19, 3660-3668.
50. (a) Wykoff, C. C.; Beasley, N.; Watson, P. H.; Campo, L.; Chia, S. K.; English, R.; Pastorek, J.; Sly, W. S.; Ratcliffe, P. J.; Harris, A. L. Expression of the hypoxia-inducible and tumor-associated carbonic anhydrases in ductal carcinoma in situ of the breast. Am. J. Pathol. 2001, 158, 1011-1019.
51. (b) Beasley, N.; Wykoff, C. C.; Watson, P. H.; Leek, R.; Turley, H.; Gatter, K.; Pastorek, J.; Cox, G. J.; Ratcliffe, P. J.; Harris, A. L. Carbonic anhydrase IX, an endogenous hypoxia marker, expression in head and neck squamous cell carcinoma and its relationship to hypoxia, necrosis, and microvessel density. Cancer Res. 2001, 61, 5262-5267.
52. (a) Koukourakis, M. I.; Giatromanolaki, A.; Sivridis, E.; Simopoulos, K.; Pastorek, J.; Wykoff, C. C.; Gatter, K. C.; Harris, A. L. Hypoxia-regulated carbonic anhydrase-9 (CA9) relates to poor vascularization and resistance of squamous cell head and neck cancer to chemoradiotherapy. Clin Cancer Res. 2001, 7, 3399-3403.
53. (b) Turner, K. J.; Crew, J. P.; Wykoff, C. C.; Watson, P. H.; Poulsom, R.; Pastorek, J.; Ratcliffe, P. J.; Cranston, D.; Harris, A. L. The hypoxia-inducible genes VEGF and CA9 are differentially regulated in superficial vs invasive bladder cancer. Br. J. Cancer 2002, 86, 1276-82.
54. (a) Giatromanolaki, A.; Koukourakis, M. I.; Sivridis, E.; Pastorek, J.; Wykoff, C. C.; Gatter, K. C.; Harris, A. L. Expression of hypoxia-inducible carbonic anhydrase-9 relates to angiogenic pathways and independently to poor outcome in nonsmall cell lung cancer. Cancer Res. 2001, 61, 7992-7998.
55. (b) Bartosova, M.; Parkkila, S.; Pohlodek, T. J.; Karttunen, T. J.; Galbavy, S.; Mucha, V.; Harris, A. L.; Pastorek, J.; Pastorekova, S. Expression of carbonic anhydrase IX in breast is associated with malignant tissues and is related to overexpression of c-erbB2. J Pathol. 2002, 197, 314-321.
56. (a) Parkkila, S.; Rajaniemi, H.; Parkkila, A. K.; Kivela, J.; Waheed, A.; Pastorekova, S.; Pastorek, J.; Sly, W. S. Carbonic anhydrase inhibitor suppresses invasion of renal cancer cells in vitro. Proc. Natl. Acad Sci. U.S.A. 2000, 97, 2220-2224.
57. (b) Xiang, Y.; Ma, B.; Li, T.; Yu, H. M.; Li, X. J. Acetazolamide suppresses tumor metastasis and related protein expression in mice bearing Lewis lung carcinoma. Acta Pharmacol. Sin. 2002, 23, 745-751.
58. (a) Scozzafava, A.; Supuran, C. T. Carbonic anhydrase inhibitors: synthesis of N-morpholylthiocarbonylsulfenylamino aromatic/heterocyclic sulfonamides and their interaction with isozymes I, II and IV. Bioorg. Med. Chem. Lett. 2000, 10, 1117-1120.
59. (b) Supuran, C. T.; Scozzafava, A. Carbonic anhydrase inhibitors: aromatic sulfonamides and disulfonamides act as efficient tumor growth inhibitors. J. Enzyme Inhib. 2000, 15, 597-610.
60. Supuran, C. T.; Scozzafava, A. Carbonic anhydrase inhibitors-Part 94. 1,3,4-Thiadiazole-2- sulfonamide derivatives as anti-tumor agents? Eur. J. Med. Chem. 2000, 35, 867-874.
61. 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.