Characterization of carbonic anhydrase isozyme specific inhibition by sulfamated 2-ethylestra compounds

Letters in Drug Design and Discovery

Volumn 8, Issue 9, 2011, Pages 678-684

  Sippel, Katherine H ^a   Stander, Andre ^b   Tu, Chingkuang ^b   Venkatakrishnan, Balasubramanian ^a   Robbins, Arthur H ^a   Agbandje McKenna, Mavis ^a   Joubert, Fourie ^c   Joubert, Annie M ^b   McKenna, Robert ^a  

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

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF PRETORIA   (South Africa)

Author keywords

2 ethylestra compounds; Anti cancer therapy; Carbonic anhydrase; Isozyme specific; Steroid sulfatase inhibitors; Structure based drug design

Indexed keywords

2 ETHYLESTRADIOL 3 O SULFAMATE; 2 ETHYLESTRADIOL 3,17 O,O BIS SULFAMATE; 2 ETHYLESTRONE 3 O SULFAMATE; CARBONATE DEHYDRATASE II; CARBONATE DEHYDRATASE INHIBITOR; CARBONATE DEHYDRATASE IX; OXYGEN 18; SULFAMATED 2 ETHYLESTRA DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CRYSTAL STRUCTURE; DRUG DESIGN; DRUG STRUCTURE; ENZYME INHIBITION; ENZYME SPECIFICITY; HYDROGEN BOND; PRIORITY JOURNAL;

EID: 80053006853     PISSN: 15701808     EISSN: 1875628X     Source Type: Journal    
DOI: None     Document Type: Article

References (36)

1. Fotsis, T.; Zhang, Y.; Pepper, M. S.; Adlercreutz, H.; Montesano, R.; Nawroth, P. P.; Schweigerer, L. The endogenous oestrogen metabolite 2-methoxyoestradiol inhibits angiogenesis and suppresses tumour growth. Nature 1994, 368(6468), 237-9. (Pubitemid 24108838)
2. Attalla, H.; Makela, T. P.; Adlercreutz, H.; Andersson, L. C. 2-Methoxyestradiol arrests cells in mitosis without depolymerizing tubulin. Biochem Biophys Res Commun 1996, 228(2), 467-73. (Pubitemid 26396096)
3. Nakagawa-Yagi, Y.; Ogane, N.; Inoki, Y.; Kitoh, N. The endogenous estrogen metabolite 2-methoxyestradiol induces apoptotic neuronal cell death in vitro. Life Sci 1996, 58(17), 1461-7. (Pubitemid 26124374)
4. Mukhopadhyay, T.; Roth, J. A. Induction of apoptosis in human lung cancer cells after wild-type p53 activation by methoxyestradiol. Oncogene 1997, 14(3), 379-84. (Pubitemid 27073094)
5. Schumacher, G.; Kataoka, M.; Roth, J. A.; Mukhopadhyay, T. Potent antitumor activity of 2-methoxyestradiol in human pancreatic cancer cell lines. Clin Cancer Res 1999, 5(3), 493-9. (Pubitemid 29131956)
6. D'Amato, R. J.; Lin, C. M.; Flynn, E.; Folkman, J.; Hamel, E. 2-Methoxyestradiol, an endogenous mammalian metabolite, inhibits tubulin polymerization by interacting at the colchicine site. Proc Natl Acad Sci U S A 1994, 91(9), 3964-8. (Pubitemid 24139553)
7. Jordan, M. A.; Wilson, L. Microtubules and actin filaments: dynamic targets for cancer chemotherapy. Curr Opin Cell Biol 1998, 10(1), 123-30. (Pubitemid 28066130)
8. Dahut, W. L.; Lakhani, N. J.; Gulley, J. L.; Arlen, P. M.; Kohn, E. C.; Kotz, H.; McNally, D.; Parr, A.; Nguyen, D.; Yang, S. X.; Steinberg, S. M.; Venitz, J.; Sparreboom, A.; Figg, W. D. Phase I clinical trial of oral 2-methoxyestradiol, an antiangiogenic and apoptotic agent, in patients with solid tumors. Cancer Biol Ther 2006, 5(1), 22-7. (Pubitemid 43234973)
9. Purohit, A.; Hejaz, H. A.; Walden, L.; MacCarthy-Morrogh, L.; Packham, G.; Potter, B. V.; Reed, M. J. The effect of 2-methoxyoestrone-3-O-sulphamate on the growth of breast cancer cells and induced mammary tumours. Int J Cancer 2000, 85(4), 584-9. (Pubitemid 30075140)
10. Purohit, A.; Vernon, K. A.; Hummelinck, A. E.; Woo, L. W.; Hejaz, H. A.; Potter, B. V.; Reed, M. J. The development of A-ring modified analogues of oestrone-3-O-sulphamate as potent steroid sulphatase inhibitors with reduced oestrogenicity. J Steroid Biochem Mol Biol 1998, 64(5-6), 269-75. (Pubitemid 28221630)
11. Verma, R. P. An Approach Towards the Quantitative Structure-Activity Relationships for Sulfamate-Based Estrone Sulfatase Inhibitors. Letters in Drug Design & Discovery 2005, 2(3), 205-218. (Pubitemid 40694849)
12. Bubert, C.; Leese, M. P.; Mahon, M. F.; Ferrandis, E.; Regis-Lydi, S.; Kasprzyk, P. G.; Newman, S. P.; Ho, Y. T.; Purohit, A.; Reed, M. J.; Potter, B. V. 3, 17-disubstituted 2-alkylestra-1, 3, 5 (10)-trien-3-ol derivatives: synthesis, in vitro and in vivo anticancer activity. J Med Chem 2007, 50(18), 4431-43. (Pubitemid 47378840)
13. Leese, M. P.; Hejaz, H. A.; Mahon, M. F.; Newman, S. P.; Purohit, A.; Reed, M. J.; Potter, B. V. A-ring-substituted estrogen-3-O-sulfamates: potent multitargeted anticancer agents. J Med Chem 2005, 48(16), 5243-56. (Pubitemid 41113911)
14. Leese, M. P.; Leblond, B.; Smith, A.; Newman, S. P.; Di Fiore, A.; De Simone, G.; Supuran, C. T.; Purohit, A.; Reed, M. J.; Potter, B. V. 2-substituted estradiol bis-sulfamates, multitargeted antitumor agents: synthesis, in vitro SAR, protein crystallography, and in vivo activity. J Med Chem 2006, 49(26), 7683-96. (Pubitemid 46033660)
15. Elger, W.; Schwarz, S.; Hedden, A.; Reddersen, G.; Schneider, B. Sulfamates of various estrogens are prodrugs with increased systemic and reduced hepatic estrogenicity at oral application. J Steroid Biochem Mol Biol 1995, 55(3-4), 395-403. (Pubitemid 26022205)
16. Abbate, F.; Winum, J. Y.; Potter, B. V.; Casini, A.; Montero, J. L.; Scozzafava, A.; Supuran, C. T. Carbonic anhydrase inhibitors: X-ray crystallographic structure of the adduct of human isozyme II with EMATE, a dual inhibitor of carbonic anhydrases and steroid sulfatase. Bioorg Med Chem Lett 2004, 14(1), 231-4. (Pubitemid 38016213)
17. Krishnamurthy, V. M.; Kaufman, G. K.; Urbach, A. R.; Gitlin, I.; Gudiksen, K. L.; Weibel, D. B.; Whitesides, G. M. Carbonic anhydrase as a model for biophysical and physical-organic studies of proteins and protein-ligand binding. Chem Rev 2008, 108(3), 946-1051. (Pubitemid 351577855)
18. Supuran, C. T.; Briganti, F.; Tilli, S.; Chegwidden, W. R.; Scozzafava, A. Carbonic anhydrase inhibitors: sulfonamides as antitumor agents? Bioorg Med Chem 2001, 9(3), 703-14. (Pubitemid 32208589)
19. Thiry, A.; Dogne, J. M.; Masereel, B.; Supuran, C. T. Targeting tumor-associated carbonic anhydrase IX in cancer therapy. Trends Pharmacol Sci 2006, 27(11), 566-73. (Pubitemid 44574507)
20. 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(15), 1516-26.
21. 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(6), 1322-31.
22. 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(38), 16233-8.
23. Cozier, G. E.; Leese, M. P.; Lloyd, M. D.; Baker, M. D.; Thiyagarajan, N.; Acharya, K. R.; Potter, B. V. Structures of human carbonic anhydrase II/inhibitor complexes reveal a second binding site for steroidal and nonsteroidal inhibitors. Biochemistry 2010, 49(16), 3464-76.
24. Khalifah, R. G., Histidine-200 alters inhibitor binding in human carbonic anhydrase B. A carbon-13 nuclear magnetic resonance identification. Biochemistry 1977, 16(10), 2236-40. (Pubitemid 8120894)
25. Silverman, D. N., Carbonic anhydrase: oxygen-18 exchange catalyzed by an enzyme with rate-contributing proton-transfer steps. Methods Enzymol 1982, 87, 732-52.
26. Segel, I., Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-State Enzyme Systems. Wiley-Interscience: New York, 1975.
27. McPherson, A., Preparation and Analysis of Protein Crystals. John Wiley and Sons: New York, 1982.
28. Otwinowski, Z.; Minor, W., Processing of X-ray Diffraction Data Collected in Oscillation Mode. Yale University: New Haven, CT, USA, 1997; Vol. 276.
29. Fisher, S. Z.; Maupin, C. M.; Budayova-Spano, M.; Govindasamy, L.; Tu, C.; Agbandje-McKenna, M.; Silverman, D. N.; Voth, G. A.; McKenna, R., Atomic crystal and molecular dynamics simulation structures of human carbonic anhydrase II: insights into the proton transfer mechanism. Biochemistry 2007, 46(11), 2930-7. (Pubitemid 46449117)
30. Adams, P. D.; Afonine, P. V.; Bunkoczi, G.; Chen, V. B.; Davis, I. W.; Echols, N.; Headd, J. J.; Hung, L. W.; Kapral, G. J.; Grosse-Kunstleve, R. W.; McCoy, A. J.; Moriarty, N. W.; Oeffner, R.; Read, R. J.; Richardson, D. C.; Richardson, J. S.; Terwilliger, T. C.; Zwart, P. H., PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 2010, 66(Pt 2), 213-21.
31. Schuttelkopf, A. W.; van Aalten, D. M., PRODRG: a tool for highthroughput crystallography of protein-ligand complexes. Acta Crystallogr D Biol Crystallogr 2004, 60(Pt 8), 1355-63. (Pubitemid 41079731)
32. Emsley, P.; Cowtan, K., Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 2004, 60(Pt 12 Pt 1), 2126-32. (Pubitemid 41742764)
33. Wallace, A. C.; Laskowski, R. A.; Thornton, J. M., LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng 1995, 8(2), 127-34.
34. Krissinel, E.; Henrick, K., Inference of macromolecular assemblies from crystalline state. J Mol Biol 2007, 372(3), 774-97. (Pubitemid 47321791)
35. Praaenikar, J.; Afonine, P. V.; Guncar, G.; Adams, P. D.; Turk, D., Averaged kick maps: less noise, more signal... and probably less bias. Acta Crystallogr D Biol Crystallogr 2009, 65(Pt 9), 921-31.
36. DeLano, W. L. The Pymol Molecular Graphics System, Delano Scientific: Palo Alto, CA, USA, 2002.