Ureido-substituted benzenesulfonamides potently inhibit carbonic anhydrase IX and show antimetastatic activity in a model of breast cancer metastasis

Journal of Medicinal Chemistry

Volumn 54, Issue 6, 2011, Pages 1896-1902

  Pacchiano, Fabio ^a   Carta, Fabrizio ^a   McDonald, Paul C ^b   Lou, Yuanmei ^b   Vullo, Daniela ^a   Scozzafava, Andrea ^a   Dedhar, Shoukat ^b,c   Supuran, Claudiu T ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b BRITISH COLUMBIA CANCER RESEARCH CENTRE   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 [[(3' NITROPHENYL)CARBAMOYL]AMINO]BENZENESULFONAMIDE; 4 [[[(4' ACETYLPHENYL)AMINO]CARBONYL]AMINO]BENZENESULFONAMIDE; BENZENESULFONAMIDE DERIVATIVE; CARBONATE DEHYDRATASE IX; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; DOSE RESPONSE; DRUG METABOLISM; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME INHIBITION; FEMALE; LUNG METASTASIS; MOUSE; NONHUMAN;

ANIMALS; ANTIGENS, NEOPLASM; ANTINEOPLASTIC AGENTS; BENZENE DERIVATIVES; CARBONIC ANHYDRASES; CATALYTIC DOMAIN; FEMALE; HUMANS; ISOENZYMES; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MODELS, MOLECULAR; NEOPLASM METASTASIS; NITROBENZENES; PROTEIN BINDING; STRUCTURE-ACTIVITY RELATIONSHIP; SULFONAMIDES; UREA;

EID: 79952808077     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm101541x     Document Type: Article

References (42)

1. Supuran, C. T. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators Nat. Rev. Drug Discovery 2008, 7, 168-181 (Pubitemid 351194064)
2. özensoy, 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
3. De Simone, G.; Supuran, C. T. Carbonic anhydrase IX: biochemical and crystllographic characterization of a novel antitumor target Biochim. Biophys. Acta 2010, 1804, 404-409
4. Supuran, C. T. Carbonic anhydrase inhibitors Bioorg. Med. Chem. Lett. 2010, 20, 3467-3474
5. 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 extracellular catalytic domain of the tumor-associated human carbonic anhydrase IX Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 16233-16238
6. Avastová, E.; Hulíková, A.; Rafajová, M.; Zat'ovi-ová, M.; Gibadulinová, A.; Casini, A.; Cecchi, A.; Scozzafava, A.; Supuran, C.; Pastorek, J. Hypoxia activates the capacity of tumor-associated carbonic anhydrase IX to acidify extracellular pH FEBS Lett. 2004, 577, 439-445 (Pubitemid 39535327)
7. Dubois, L.; Douma, K.; Supuran, C. T.; Chiu, R. K.; van Zandvoort, M. A. M. J.; Pastoreková, S.; Scozzafava, A.; Wouters, B. G.; Lambin, P. Imaging the hypoxia surrogate marker CA IX requires expression and catalytic activity for binding fluorescent sulfonamide inhibitors Radiother. Oncol. 2007, 83, 367-373 (Pubitemid 46915545)
8. Dubois, L.; Lieuwes, N. G.; Maresca, A.; Thiry, A.; Supuran, C. T.; Scozzafava, A.; Wouters, B. G.; Lambin, P. Imaging of CA IX with fluorescent labelled sulfonamides distinguishes hypoxic and (re)-oxygenated cells in a xenograft tumour model Radiother. Oncol. 2009, 92, 423-428
9. Wouters, B.G.;; Koritzinsky, M. Hypoxia signalling through mTOR and the unfolded protein response in cancer Nat. Rev. Cancer 2008, 8, 851-864
10. Swietach, P.; Wigfield, S.; Cobden, P.; Supuran, C. T.; Harris, A. L.; Vaughan-Jones, R. D. Tumor-associated carbonic anhydrase 9 spatially coordinates intracellular pH in three-dimensional multicellular growth J. Biol. Chem. 2008, 283, 20473-20483
11. 2 diffusion BJU Int. 2008, 101 (Suppl. 4) 22-24
12. Swietach, P.; Hulikova, A.; Vaughan-Jones, R. D.; Harris, A. L. New insights into the physiological role of carbonic anhydrase IX in tumour pH regulation Oncogene 2010, 29, 6509-6521
13. Chiche, J.; Ilc, K.; Laferriare, J.; Trottier, E.; Dayan, F.; Mazure, N. M.; Brahimi-Horn, M. C.; Pouysségur, J. Hypoxia-inducible carbonic anhydrase IX and XII promote tumor cell growth by counteracting acidosis through the regulation of the intracellular pH Cancer Res. 2009, 69, 358-368
14. Ahlskog, J. K. J.; Dumelin, C. E.; Trüssel, S.; Marlind, J.; Neri, D. In vivo targeting of tumor-associated carbonic anhydrases using acetazolamide derivatives Bioorg. Med. Chem. Lett. 2009, 19, 4851-4856
15. Ahlskog, J. K.; Schliemann, C.; Mayrlind, J.; Qureshi, U.; Ammar, A.; Pedleym, R. B.; Neri, D. Human monoclonal antibodies targeting carbonic anhydrase IX for the molecular imaging of hypoxic regions in solid tumours Br. J. Cancer. 2009, 101, 645-657
16. Hilvo, M.; Baranauskiene, L.; Salzano, A. M.; Scaloni, A.; Matulis, D.; Innocenti, A.; Scozzafava, A.; Monti, S. M.; Di Fiore, A.; De Simone, G.; Lindfors, M.; Janis, J.; Valjakka, J.; Pastorekova, S.; Pastorek, J.; Kulomaa, M. S.; Nordlund, H. R.; Supuran, C. T.; Parkkila, S. Biochemical characterization of CA IX: one of the most active carbonic anhydrase isozymes J. Biol. Chem. 2008, 283, 27799-27809
17. Wykoff, C. C.; Beasley, N. J.; 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. J.; Harris, A. L. Hypoxia-inducible expression of tumor-associated carbonic anhydrases Cancer Res. 2000, 60, 7075-7083 (Pubitemid 32059187)
18. Bartosova, M.; Parkkila, S.; Pohlodek, K.; 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, 1-8
19. Pastoreková, S.; Pastorek, J. Cancer-Related Carbonic Anhydrase Isozymes and Their Inhibition. In Carbonic Anhydrase: Its Inhibitors and Activators; Supuran, C. T.; Scozzafava, A.; Conway, J., Eds.; CRC Press: Boca Raton, FL, 2004; pp 255 - 281.
20. Ebbesen, P.; Pettersen, E. O.; Gorr, T. A.; Jobst, G.; Williams, K.; Kienninger, J.; Wenger, R. H.; Pastorekova, S.; Dubois, L.; Lambin, P.; Wouters, B. G.; Supuran, C. T.; Poellinger, L.; Ratcliffe, P.; Kanopka, A.; Görlach, A.; Gasmann, M.; Harris, A. L.; Maxwell, P.; Scozzafava, A. Taking advantage of tumor cell adaptations to hypoxia for developing new tumor markers and treatment strategies J. Enzyme Inhib. Med. Chem. 2009, 24 (S1) 1-39
21. 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
22. Zatovicova, M; Jelenska, L; Hulikova, A; Csaderova, L; Ditte, Z; Ditte, P; Goliasova, T; Pastorek, J; Pastorekova, S. Carbonic anhydrase IX as an Anticancer therapy target: preclinical evaluation of internalizing monoclonal antibody directed to catalytic domain Curr. Pharm. Des. 2010, 16, 3255-3263
23. Pacchiano, F.; Aggarwal, M.; Avvaru, B. S.; Robbins, A. H.; Scozzafava, A.; McKenna, R.; Supuran, C. T. Selective hydrophobic pocket binding observed within the carbonic anhydrase II active site accommodate different 4-substituted-ureido-benzenesulfonamides and correlate to inhibitor potency Chem. Commun. (Cambridge, U. K.) 2010, 46, 8371-8373
24. Roth, J. S.; Degering, E. F. The preparation of sulfanilamide derivatives containing a urea or thiourea grouping J. Am. Chem. Soc. 1945, 67, 126-128
25. Supuran, C. T.; Scozzafava, A.; Jurca, B. C.; Ilies, M. A. Carbonic anhydrase inhibitors. Part 49. Synthesis of substituted ureido- and thioureido derivatives of aromatic/heterocyclic sulfonamides with increased affinities for isozyme I Eur. J. Med. Chem. 1998, 33, 83-93 (Pubitemid 28152310)
26. Scozzafava, A.; Supuran, C. T. Carbonic anhydrase inhibitors. Arylsulfonylureido and arylureido-substituted aromatic and heterocyclic sulfonamides: towards selective inhibitors of carbonic anhydrase isozyme I J. Enzyme Inhib. 1999, 14, 343-363 (Pubitemid 29408271)
27. Alterio, V.; Di Fiore, A.; D'Ambrosio, K.; Supuran, C. T.; De Simone, G. X-Ray Crystallography of CA inhibitors and Its Importance in Drug Design. In Drug Design of Zinc-Enzyme Inhibitors: Functional, Structural, and Disease Applications; Supuran, C. T.; Winum, J. Y., Eds.; Wiley: Hoboken, NJ, 2009; pp 73 - 138.
28. Avvaru, B. S.; Wagner, J. M.; Maresca, A.; Scozzafava, A.; Robbins, A. H.; Supuran, C. T.; McKenna, R. Carbonic anhydrase inhibitors. The X-ray crystal structure of human isoform II in adduct with an adamantyl analogue of acetazolamide resides in a new hydrophobic binding pocket Bioorg. Med. Chem. Lett. 2010, 20, 4376-4381
29. Di Fiore, A.; Monti, S. M.; Innocenti, A.; Winum, J.-Y.; De Simone, G.; Supuran, C. T. Carbonic anhydrase inhibitors. X-ray crystallographic and solution binding studies for the interaction of a boron containing aromatic sulfamide with mammalian isoforms I-XV Bioorg. Med. Chem. Lett. 2010, 20, 3601-3605
30. Wagner, J.; Avvaru, B. S.; Robbins, A. H.; Scozzafava, A.; Supuran, C. T.; McKenna, R. Coumarinyl-substituted sulfonamides strongly inhibit several human carbonic anhydrase isoforms: solution and crystallographic investigations Bioorg. Med. Chem. 2010, 18, 4873-4878
31. 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
32. Chen, C. L.; Chu, J. S.; Su, W. C.; Huang, S. C.; Lee, W. Y. Hypoxia and metabolic phenotypes during breast carcinogenesis: expression of HIF-1alpha, GLUT1, and CAIX Virchows Arch. 2010, 457, 53-61
33. Kristiansen, G.; Rose, M.; Geisler, C.; Fritzsche, F. R.; Gerhardt, J.; Luke, C.; Ladhoff, A. M.; Knuchel, R.; Dietel, M.; Moch, H.; Varga, Z.; Theurillat, J. P.; Gorr, T. A.; Dahl, E. Endogenous myoglobin in human breast cancer is a hallmark of luminal cancer phenotype Br. J. Cancer 2010, 102, 1736-1745
34. 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 (Pubitemid 32786278)
35. Hussain, S. A.; Ganesan, R.; Reynolds, G.; Gross, L.; Stevens, A.; Pastorek, J.; Murray, P. G.; Perunovic, B.; Anwar, M. S.; Billingham, L.; James, N. D.; Spooner, D.; Poole, C. J.; Rea, D. W.; Palmer, D. H. Hypoxia-regulated carbonic anhydrase IX expression is associated with poor survival in patients with invasiv breast cancer Br. J. Cancer 2007, 96, 104-109 (Pubitemid 46094646)
36. Aslakson, C. J.; Miller, F. R. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor Cancer Res. 1992, 52, 1399-1405
37. Heppner, G. H.; Miller, F. R.; Shekhar, P. M. Nontransgenic models of breast cancer Breast Cancer Res. 2000, 2, 331-334 (Pubitemid 32223615)
38. Eckhardt, B. L.; Parker, B. S.; van Laar, R. K.; Restall, C. M.; Natoli, A. L.; Tavaria, M. D.; Stanley, K. L.; Sloan, E. K.; Moseley, J. M.; Anderson, R. L. Genomic analysis of a spontaneous model of breast cancer metastasis to bone reveals a role for the extracellular matrix Mol. Cancer Res. 2005, 3, 1-13 (Pubitemid 40189591)
39. Pulaski, B. A.; Ostrand-Rosenberg, S. Mouse 4T1 breast tumor model Curr. Protoc. Immunol. 2001, 20, 202-212
40. Tao, K.; Fang, M.; Alroy, J.; Sahagian, G. G. Imagable 4T1 model for the study of late stage breast cancer BMC Cancer 2008, 8, 228
41. Lou, Y.; Preobrazhenska, O.; auf dem Keller, U.; Sutcliffe, M.; Barclay, L.; McDonald, P. C.; Roskelley, C.; Overall, C. M.; Dedhar, S. Epithelial-mesenchymal transition (EMT) is not sufficient for spontaneous murine breast cancer metastasis Dev. Dyn. 2008, 237, 2755-2768
42. Ebos, J. M.; Lee, C. R.; Cruz-Munoz, W.; Bjarnason, G. A.; Christensen, J. G.; Kerbel, R. S. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis Cancer Cell 2009, 15, 232-239