Structures of human carbonic anhydrase II/inhibitor complexes reveal a second binding site for steroidal and nonsteroidal inhibitors

Biochemistry

Volumn 49, Issue 16, 2010, Pages 3464-3476

  Cozier, Gyles E ^a   Leese, Mathew P ^a   Lloyd, Matthew D ^a   Baker, Matthew D ^a,b   Thiyagarajan, Nethaji ^b   Acharya, K Ravi ^b   Potter, Barry V L ^a  

^a University of Bath   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

, INHIBITOR; ACTIVE SITE; ADJACENT SITES; AROMATASE; CANCER DRUG; CARBONIC ANHYDRASES; CYANOBIPHENYLS; DEGREE OF FLEXIBILITY; DRUG DESIGN; DRUG TARGETS; HUMAN CARBONIC ANHYDRASES; HYDROGEN CARBONATES; IN-VIVO; MODE OF BINDING; NONSTEROIDAL LIGANDS; PH BALANCE; RED BLOOD CELL; STEROID SULFATASE; STRUCTURAL BASIS; STRUCTURAL CHANGE; SULFAMATES; SULFATASES;

BINDING ENERGY; BLOOD; CARBON DIOXIDE; COORDINATION REACTIONS; ENZYME INHIBITION; ESTERS; ZINC; ZINC COMPOUNDS;

CARBONIC ANHYDRASE;

2 ETHYLESTRADIOL 3,17 O,O BIS(SULFAMATE); 2 METHOXYESTRADIOL 17 O SULFAMATE; 2 METHOXYESTRADIOL 3 O SULFAMATE; 2 METHOXYESTRADIOL 3,17 O,O BIS(SULFAMATE); 5' [(4H 1,2,4 TRIAZOL 4 YL)METHYL] 3 CHLORO 2' CYANOBIPHENYL 4 YL SULFAMATE; AROMATASE INHIBITOR; CARBONATE DEHYDRATASE II; CARBONATE DEHYDRATASE INHIBITOR; ENZYME INHIBITOR; ESTRONE 3 O SULFAMATE; STERYL SULFATASE; SULFATASE; UNCLASSIFIED DRUG; ZINC ION;

ARTICLE; BETA SHEET; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISSOCIATION CONSTANT; DRUG DESIGN; DRUG STRUCTURE; ENZYME ACTIVE SITE; ENZYME INHIBITION; ERYTHROCYTE; HUMAN; IC 50; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEIN TARGETING;

BICARBONATES; BINDING SITES; CARBON DIOXIDE; CARBONIC ANHYDRASE II; COLORIMETRY; ENZYME INHIBITORS; ESTRONE; HUMANS; KINETICS; MODELS, MOLECULAR; PROTEIN CONFORMATION;

EID: 77951222675     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi902178w     Document Type: Article

References (49)

1. 2 elimination Annu. Rev. Physiol. 50, 695-717
2. Casini, A., Scozzafava, A., Mincione, F., Menabuoni, L., Starnotti, M., and Supuran, C. T. (2003) Carbonic anhydrase inhibitors: Topically acting antiglaucoma sulfonamides incorporating esters and amides of 3- and 4-carboxybenzolamide Bioorg. Med. Chem. Lett. 13, 2867-2873
3. Recacha, R., Costanzo, M. J., Maryanoff, B. E., and Chattopadhyay, D. (2002) Crystal structure of human carbonic anhydrase II complexed with an anti-convulsant sugar sulphamate Biochem. J. 361, 437-441
4. Supuran, C. T. (2003) Carbonic anhydrase inhibitors in the treatment and prophylaxis of obesity Expert Opin. Ther. Pat. 13 1545-1550 (Pubitemid 37369481)
5. Abbate, F., Winum, J.-Y., Potter, B. V. L., Casini, A., Montero, J.-L., Scozzafava, A., and Supuran, C. T. (2004) Carbonic anhydrase inhibitors: X-ray crystallographic structure of the adduct of human isozyme II with EMATE, a dual inhibitor of carbonic anhydrase and steroid sulfatase Bioorg. Med. Chem. Lett. 14, 231-234 (Pubitemid 38016213)
6. Ho, Y. T., Purohit, A., Vicker, N., Newman, S. P., Robinson, J. J., Leese, M. P., Ganeshapillai, D., Woo, L. W. L., Potter, B. V. L., and Reed, M. J. (2003) Inhibition of carbonic anhydrase II by steroidal and non-steroidal sulphamates Biochem. Biophys. Res. Commun. 305, 909-914 (Pubitemid 36597850)
7. Supuran, C. T., Scozzafava, A., and Casini, A. (2003) Carbonic anhydrase inhibitors Med. Res. Rev. 23, 146-189 (Pubitemid 36241096)
8. Hilvo, M., Tolvanen, M., Clark, A., Shen, B., Shah, G. N., Waheed, A., Halmi, P., Hainninen, M., Haimalainen, J. M., Vihinen, M., Sly, W. S., and Parkkila, S. (2005) Characterization of CA XV, a new GPI-anchored form of carbonic anhydrase Biochem. J. 392, 83-92 (Pubitemid 41689404)
9. Türeci, O., Sahin, E., Vollmar, E., Siemer, S., Gottert, E., Seitz, G., Parkkila, A.-K., Shah, G. N., Grubb, J. H., Pfreundschuh, M., and Sly, W. S. (1998) Human carbonic anhydrase XII: cDNA cloning, expression, and chromosomal localization of a carbonic anhydrase gene that is over-expressed in some renal cell cancers Proc. Natl. Acad. Sci. U.S.A. 95, 7608-7613 (Pubitemid 28293300)
10. Loncaster, J. A., Harris, A. L., Davidson, S. E., Logue, J. P., Hunter, R. D., Wycoff, C. C., Pastorek, J., Ratcliffe, P. J., Stratford, I. J., and West, C. M. L. (2001) 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. 61, 6394-6399 (Pubitemid 32783244)
11. Wykoff, C. C., Beasley, N. J. P., 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., and Harris, A. L. (2000) Hypoxia-inducible expression of tumor-associated carbonic anhydrases Cancer Res. 60, 7075-7083 (Pubitemid 32059187)
12. Howarth, N. M., Purohit, A., Reed, M. J., and Potter, B. V. L. (1994) Estrone sulfamates: Potent inhibitors of estrone sulfatase with therapeutic potential J. Med. Chem. 37, 219-221 (Pubitemid 24063038)
13. Purohit, A., Williams, G. J., Roberts, C. J., Potter, B. V. L., and Reed, M. J. (1995) In vivo inhibition of oestrone sulphatase and dehydroepiandrosterone sulphatase by oestrone-3- O -sulphamate Int. J. Cancer 63, 106-111
14. Newman, S. P., Foster, P. A., Ho, Y. T., Day, J. M., Raobaikady, B., Kasprzyk, P. G., Leese, M. P., Potter, B. V. L., Reed, M. J., and Purohit, A. (2007) The therapeutic potential of a series of orally bioavailable anti-angiogenic microtubule disruptors as therapy for hormone-independent prostate and breast cancers Br. J. Cancer 97, 1673-1682
15. MacCarthy-Morrogh, L., Townsend, P. A., Purohit, A., Hejaz, H. A. M., Potter, B. V. L., Reed, M. J., and Packham, G. (2000) Differential effects of estrone and estrone-3- O -sulfamate derivatives on mitotic arrest, apoptosis, and microtubule assembly in human breast cancer cells Cancer Res. 60, 5441-5450
16. Purohit, A., Woo, L. W. L., Barrow, D., Hejaz, H. A. M., Nicholson, R. I., Potter, B. V. L., and Reed, M. J. (2001) Non-steroidal and steroidal sulfamates: New drugs for cancer therapy Mol. Cell. Endocrinol. 171, 129-135
17. Reed, M. J., Purohit, A., Woo, L. W. L., Newman, S. P., and Potter, B. V. L. (2005) Steroid sulfatase: Molecular biology, regulation, and inhibition Endocr. Rev. 26, 171-202
18. Stanway, S. J., Purohit, A., Woo, L. W. L., Sufi, S., Vigushin, D., Ward, R., Wilson, R. H., Stanczyk, F. Z., Dobbs, N., Kulinskaya, E., Elliott, M., Potter, B. V. L., Reed, M. J., and Coombes, R. C. (2006) Phase I study of STX 64 (667 coumate) in breast cancer patients: The first study of a steroid sulfatase inhibitor Clin. Cancer Res. 12, 1585-1592
19. Woo, L. W. L., Howarth, N. M., Purohit, A., Hejaz, H. A. M., Reed, M. J., and Potter, B. V. L. (1998) Steroidal and non-steroidal sulfamates as potent inhibitors of steroid sulfatase J. Med. Chem. 41, 1068-1083
20. Purohit, A., Williams, G. J., Howarth, N. M., Potter, B. V. L., and Reed, M. J. (1995) Inactivation of steroid sulfatase by an active site-directed inhibitor, estrone 3- O -sulfamate Biochemistry 34, 11508-11514
21. Elger, W., Schwarz, S., Hedden, A., Reddersen, G., and Schneider, B. (1995) Sulfamates of various estrogens are prodrugs with increased systemic and reduced hepatic estrogenicity at oral application J. Steroid Biochem. Mol. Biol. 55, 395-403
22. Ireson, C. R., Chander, S. K., Purohit, A., Perera, S., Newman, S. P., Parish, D., Leese, M. P., Smith, A. C., Potter, B. V. L., and Reed, M. J. (2004) Pharmacokinetics and efficacy of 2-methoxyoestradiol and 2-methoxyoestradiol- bis-sulphamate in vivo in rodents Br. J. Cancer 90, 932-937
23. Leese, M. P., Leblond, B., Smith, A., Newman, S. P., DiFiore, A., DeSimone, G., Supuran, C. T., Purohit, A., Reed, M. J., and Potter, B. V. L. (2006) 2-Substituted estradiol bis-sulfamates, multitargeted antitumor agents: Synthesis, in vitro SAR, protein crystallography, and in vivo activity J. Med. Chem. 49, 7683-7696
24. Lloyd, M. D., Pederick, R. L., Natesh, R., Woo, L. W. L., Purohit, A. P., Reed, M. J., Acharya, K. R., and Potter, B. V. L. (2005) Crystal structure of human carbonic anhydrase II at 1.95 ⋯ resolution in complex with 667-coumate, a novel anti-cancer agent Biochem. J. 385, 715-720
25. Lloyd, M. D., Thiyagarajan, N., Ho, Y. T., Woo, L. W. L., Sutcliffe, O. B., Purohit, A., Reed, M. J., Acharya, K. R., and Potter, B. V. L. (2005) First crystal structures of human carbonic anhydrase II in complex with dual aromatase-steroid sulfatase inhibitors Biochemistry 44, 6858-6866
26. Woo, L. W. L., Jackson, T., Putey, A., Cozier, G., Leonard, P., Acharya, K. R., Chander, S. K., Purohit, A., Reed, M. J., and Potter, B. V. L. (2010) Highly potent first examples of dual aromatase-steroid sulfatase inhibitors based on a biphenyl template J. Med. Chem. 53, 2155-2170
27. Leese, M. P., Hejaz, H. A. M., Mahon, M. F., Newman, S. P., Purohit, A., Reed, M. J., and Potter, B. V. L. (2005) A-ring-substituted estrogen-3- O -sulfamates: Potent multitargeted anticancer agents J. Med. Chem. 48, 5243-5256
28. Armstrong, J. M., Myers, D. V., Verpoorte, J. A., and Edsall, J. T. (1966) Purification and properties of human carbonic anhydrases J. Biol. Chem. 241, 5137-5149
29. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode, in Methods in Enzymology (Carter, C. W. J. and Sweet, R. M., Eds.) pp 307 - 326, Academic Press, New York.
30. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674
31. Eriksson, A. E., Jones, T. A., and Liljas, A. (1988) Refined structure of human carbonic anhydrase II at 2.0 ⋯ resolution Proteins 4, 274-282
32. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J.-S., Kuszewski, J., Nilges, N., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography and NMR system (CNS): A new software system for macromolecular structure determination Acta Crystallogr. D54, 905-921
33. Brunger, A. T. (2007) Version 1.2 of the crystallography and NMR system Nat. Protocols 2, 2728-2733
34. Korostelev, A., Bertram, R., and Chapman, M. S. (2002) Simulated-annealing real-space refinement as a tool in model building Acta Crystallogr., Sect. D 58, 761-767
35. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
36. Kleywegt, G. (2007) Crystallographic refinement of ligand complexes Acta Crystallogr., Sect. D 63, 94-100
37. Abbate, F., Casini, A., Owa, T., Scozzafava, A., and Supuran, C. T. (2004) Carbonic anhydrase inhibitors: E7070, a sulfonamide anticancer agent, potently inhibits cytosolic isozymes I and II, and transmembrane, tumour-associated isozyme IX Bioorg. Med. Chem. Lett. 14, 217-223
38. Ippolito, J. A., Nair, S. K., Alexander, R. S., Kiefer, L. L., Fierke, C. A., and Christianson, D. W. (1995) Structure of His94'Asp carbonic anhydrase II in a new crystalline form reveals a partially occupied zinc binding site Protein Eng. 8, 975-980
39. Alexander, R. S., Kiefer, L. L., Fierke, C. A., and Christianson, D. W. (1993) Engineering the zinc binding site of human carbonic anhydrase II: Structure of the His-94'Cys apoenzyme in a new crystalline form Biochemistry 32, 1510-1518
40. Thea, S., Cevasco, G., Guanti, G., and Williams, A. (1986) The anionic sulphonylamine mechanism in the hydrolysis of aryl sulphamates J. Chem. Soc., Chem. Commun., 1582-1583
41. Nussbaumer, P., Winiski, A. P., and Billich, A. (2003) Estrogenic potential of 2-alkyl-4-(thio)chromenone 6- O -sulfamates: Potent inhibitors of human steroid sulfatase J. Med. Chem. 46, 5091-5094
42. Sahm, U. G., Williams, G. J., Purohit, A., Hidalgo Aragones, M. I., Parish, D., Reed, M. J., Potter, B. V. L., and Pouton, C. W. (1996) Development of an oral formulation for oestrone 3- O -sulphamate, a potent sulphatase inhibitor Pharm. Sci. 2, 17-20
43. Nair, S. K., Ludwig, P. A., and Christianson, D. W. (1994) Two-site binding of phenol in the active site of human carbonic anhydrase II: Structural implications for substrate association J. Am. Chem. Soc. 116, 3659-3660
44. Kim, C.-Y., Chandra, P. P., Jain, A., and Christianson, D. W. (2001) Fluoroaromatic-fluoroaromatic interactions between inhibitors bound in the crystal lattice of human carbonic anhydrase II J. Am. Chem. Soc. 123, 9620-9627
45. Jude, K. M., Banerjee, A. L., Haldar, M. K., Manokaran, S., Roy, B., Mallik, S., Srivastava, D. K., and Christianson, D. W. (2006) Ultrahigh resolution crystal structures of human carbonic anhydrases I and II complexed with two-prong inhibitors reveal the molecular basis of high affinity J. Am. Chem. Soc. 128, 3011-3018
46. Cappalonga Bunn, A. M., Alexander, R. S., and Christianson, D. W. (1994) Mapping protein-peptide affinity: Binding of peptidylsulfonamide inhibitors to human carbonic anhydrase II J. Am. Chem. Soc. 116, 5063-5068
47. Ramstrom, O. and Lehn, J.-M. (2002) Drug discovery by dynamic combinatorial libraries Nat. Rev. Drug Discov. 1, 26-36
48. Huc, I. and Lehn, J.-M. (1997) Virtual combinatorial libraries: Dynamic generation of molecular and supramolecular diversity by self-assembly Proc. Natl. Acad. Sci. U.S.A. 94, 2106-2110
49. Poulsen, S.-A. and Bornaghi, L. F. (2006) Fragment-based drug discovery of carbonic anhydrase II inhibitors by dynamic combinatorial chemistry utilizing alkene cross metathesis Bioorg. Med. Chem. 14, 3275-3284