Steroid sulfatase inhibitors: Promising new tools for breast cancer therapy?

Journal of Steroid Biochemistry and Molecular Biology

Volumn 125, Issue 1-2, 2011, Pages 39-45

  Geisler, Jürgen ^a   Sasano, Hironobu ^b   Chen, Shiuan ^c   Purohit, Atul ^d  

^a UNIVERSITY OF OSLO   (Norway)

^b TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^d HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

Androgens; Aromatase inhibitors; Breast cancer; Estrogens; Irosustat; STX 213; STX 64; STX 681; Sulfatase inhibitors

Indexed keywords

4 [N (4 BROMOBENZYL) N (1,2,4 TRIAZOL 4 YL)AMINO]BENZONITRILE; 6 [2 (ADAMANTYLIDENE) HYDROXYBENZOXAZOLE] SULFAMATE; ANASTROZOLE; ANDROGEN; ANTINEOPLASTIC AGENT; AROMATASE; ESTERASE INHIBITOR; ESTROGEN; ESTRONE 3 SULFAMATE; IROSUSTAT; KW 2581; LETROZOLE; SR 16157; STEROID SULFATASE INHIBITOR; STX 213; STX 681; TESTOSTERONE 17BETA DEHYDROGENASE; UNCLASSIFIED DRUG;

ANDROGEN SYNTHESIS; BREAST CANCER; CANCER DIAGNOSIS; CANCER PATIENT; CANCER RESEARCH; CANCER THERAPY; CANCER TISSUE; DRUG DOSE ESCALATION; DRUG INHIBITION; DRUG STRUCTURE; ESTROGEN SYNTHESIS; GENE EXPRESSION; HUMAN; NONHUMAN; REVIEW;

ANDROGENS; AROMATASE INHIBITORS; BREAST NEOPLASMS; CLINICAL TRIALS AS TOPIC; ENZYME INHIBITORS; ESTROGENS; FEMALE; HUMANS; MOLECULAR STRUCTURE; STERYL-SULFATASE;

EID: 79957779156     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2011.02.002     Document Type: Review

References (55)

1. J. Geisler, and P.E. Lonning Aromatase inhibition: translation into a successful therapeutic approach Clin. Cancer Res. 11 8 2005 2809 2821 (Pubitemid 40525179)
2. J. Geisler, and P.E. Lonning Aromatase inhibitors as adjuvant treatment of breast cancer Crit. Rev. Oncol. Hematol. 57 1 2006 53 61 (Pubitemid 41804080)
3. W.R. Miller, J.M. Bartlett, P. Canney, and M. Verrill Hormonal therapy for postmenopausal breast cancer: the science of sequencing Breast Cancer Res. Treat. 103 2 2007 149 160 (Pubitemid 46789136)
4. S. Chia, W. Gradishar, L. Mauriac, J. Bines, F. Amant, M. Federico, L. Fein, G. Romieu, A. Buzdar, J.F. Robertson, A. Brufsky, K. Possinger, P. Rennie, F. Sapunar, E. Lowe, and M. Piccart Double-blind, randomized placebo controlled trial of fulvestrant compared with exemestane after prior nonsteroidal aromatase inhibitor therapy in postmenopausal women with hormone receptor-positive, advanced breast cancer: results from EFECT J. Clin. Oncol. 26 10 2008 1664 1670
5. D Ghosh Human sulfatases: a structural perspective to catalysis Cell. Mol. Life Sci. 64 15 2007 2013 2022 (Pubitemid 47094434)
6. M.J. Reed, A. Purohit, L.W. Woo, S.P. Newman, and B.V. Potter Steroid sulfatase: molecular biology, regulation, and inhibition Endocr. Rev. 26 2 2005 171 202
7. N Chanplakorn, P. Chanplakorn, T. Suzuki, K. Ono, M.S. Chan, Y. Miki, S. Saji, T. Ueno, M. Toi, and H. Sasano Increased estrogen sulfatase (STS) and 17beta-hydroxysteroid dehydrogenase type 1(17beta-HSD1) following neoadjuvant aromatase inhibitor therapy in breast cancer patients Breast Cancer Res. Treat. 120 3 2010 639 648
8. P.E. Lonning, H. Helle, N.K. Duong, D. Ekse, T. Aas, and J. Geisler Tissue estradiol is selectively elevated in receptor positive breast cancers while tumour estrone is reduced independent of receptor status J. Steroid Biochem. Mol. Biol. 117 1-3 2009 31 41
9. S. Masamura, S.J. Santner, D.F. Heitjan, and R.J. Santen Estrogen deprivation causes estradiol hypersensitivity in human breast cancer cells J. Clin. Endocrinol. Metab. 80 10 1995 2918 2925
10. A. Billich, P. Nussbaumer, and P. Lehr Stimulation of MCF-7 breast cancer cell proliferation by estrone sulfate and dehydroepiandrosterone sulfate: inhibition by novel non-steroidal steroid sulfatase inhibitors J. Steroid Biochem. Mol. Biol. 73 5 2000 225 235
11. J. Geisler Breast cancer tissue estrogens and their manipulation with aromatase inhibitors and inactivators J. Steroid Biochem. Mol. Biol. 86 3-5 2003 245 253 (Pubitemid 37420000)
12. A. Subramanian, M. Salhab, and K. Mokbel Oestrogen producing enzymes and mammary carcinogenesis: a review Breast Cancer Res. Treat. 111 2 2008 191 202
13. J.R. Pasqualini, and G.S. Chetrite Recent insight on the control of enzymes involved in estrogen formation and transformation in human breast cancer J. Steroid Biochem. Mol. Biol. 93 2-5 2005 221 236 (Pubitemid 40602495)
14. L. Tseng, J. Mazella, L.Y. Lee, and M.L. Stone Estrogen sulfatase and estrogen sulfotransferase in human primary mammary carcinoma J. Steroid Biochem. 19 4 1983 1413 1417 (Pubitemid 14248009)
15. J.A. Aka, M. Mazumdar, C.Q. Chen, D. Poirier, and S.X. Lin 17beta-hydroxysteroid dehydrogenase type 1 stimulates breast cancer by dihydrotestosterone inactivation in addition to estradiol production Mol. Endocrinol. 24 4 2010 832 845
16. B.P. Haynes, A.H. Straume, J. Geisler, R. A'Hern, H. Helle, I.E. Smith, P.E. Lonning, and M. Dowsett Intratumoral estrogen disposition in breast cancer Clin. Cancer Res. 16 6 2010 1790 1801
17. S.J. Santner, P.D. Feil, and R.J. Santen In situ estrogen production via the estrone sulfatase pathway in breast tumors: relative importance versus the aromatase pathway J. Clin. Endocrinol. Metab. 59 1 1984 29 33 (Pubitemid 14087520)
18. T.R. Evans, M.G. Rowlands, M. Law, and R.C. Coombes Intratumoral oestrone sulphatase activity as a prognostic marker in human breast carcinoma Br. J. Cancer 69 3 1994 555 561 (Pubitemid 24076479)
19. T. Utsumi, N. Yoshimura, S. Takeuchi, J. Ando, M. Maruta, K. Maeda, and N. Harada Steroid sulfatase expression is an independent predictor of recurrence in human breast cancer Cancer Res. 59 2 1999 377 381 (Pubitemid 29048871)
20. T. Saeki, S. Takashima, H. Sasaki, N. Hanai, and D.S. Salomon Localization of estrone sulfatase in human breast carcinomas Breast Cancer 6 4 1999 331 337
21. T. Suzuki, T. Nakata, Y. Miki, C. Kaneko, T. Moriya, T. Ishida, S. Akinaga, H. Hirakawa, M. Kimura, and H. Sasano Estrogen sulfotransferase and steroid sulfatase in human breast carcinoma Cancer Res. 63 11 2003 2762 2770 (Pubitemid 36667146)
22. S.A. Chen, M.J. Besman, R.S. Sparkes, S. Zollman, I. Klisak, T. Mohandas, P.F. Hall, and J.E. Shively Human aromatase: cDNA cloning, Southern blot analysis, and assignment of the gene to chromosome 15 DNA 7 1 1988 27 38 (Pubitemid 18044631)
23. S.E Bulun, Z. Lin, G. Imir, S. Amin, M. Demura, B. Yilmaz, R. Martin, H. Utsunomiya, S. Thung, B. Gurates, M. Tamura, D. Langoi, and S. Deb Regulation of aromatase expression in estrogen-responsive breast and uterine disease: from bench to treatment Pharmacol. Rev. 57 3 2005 359 383 (Pubitemid 41196955)
24. E.R. Simpson, C. Clyne, G. Rubin, W.C. Boon, K. Robertson, K. Britt, C. Speed, and M. Jones Aromatase - a brief overview Annu. Rev. Physiol. 64 2002 93 127 (Pubitemid 34259227)
25. I.E. Smith, and M. Dowsett Aromatase inhibitors in breast cancer N. Engl. J. Med. 348 24 2003 2431 2442 (Pubitemid 36682823)
26. J. Geisler, H. Helle, D. Ekse, N.K. Duong, D.B. Evans, Y. Nordbo, T. Aas, and P.E. Lonning Letrozole is superior to anastrozole in suppressing breast cancer tissue and plasma estrogen levels Clin. Cancer Res. 14 19 2008 6330 6335
27. J. Geisler, N. King, G. Anker, G. Ornati, E. Di Salle, P.E. Lonning, and M. Dowsett In vivo inhibition of aromatization by exemestane, a novel irreversible aromatase inhibitor, in postmenopausal breast cancer patients Clin. Cancer Res. 4 9 1998 2089 2093 (Pubitemid 28415652)
28. J Geisler, B. Haynes, G. Anker, M. Dowsett, and P.E. Lonning Influence of letrozole and anastrozole on total body aromatization and plasma estrogen levels in postmenopausal breast cancer patients evaluated in a randomized, cross-over study J. Clin. Oncol. 20 3 2002 751 757 (Pubitemid 34111382)
29. V.V. Isomaa, S.A. Ghersevich, O.K. Maentausta, E.H. Peltoketo, M.H. Poutanen, and R.K. Vihko Steroid biosynthetic enzymes: 17 beta-hydroxysteroid dehydrogenase Ann. Med. 25 1 1993 91 97 (Pubitemid 23088768)
30. J.M. Day, P.A. Foster, H.J. Tutill, M.F. Parsons, S.P. Newman, S.K. Chander, G.M. Allan, H.R. Lawrence, N. Vicker, B.V. Potter, M.J. Reed, and A. Purohit 17beta-hydroxysteroid dehydrogenase Type 1, and not Type 12, is a target for endocrine therapy of hormone-dependent breast cancer Int. J. Cancer 122 9 2008 1931 1940 (Pubitemid 351441181)
31. Y Laplante, C. Rancourt, and D. Poirier Relative involvement of three 17beta-hydroxysteroid dehydrogenases (types 1, 7 and 12) in the formation of estradiol in various breast cancer cell lines using selective inhibitors Mol. Cell. Endocrinol. 301 1-2 2009 146 153
32. J.M. Day, H.J. Tutill, A. Purohit, and M.J. Reed Design and validation of specific inhibitors of 17beta-hydroxysteroid dehydrogenases for therapeutic application in breast and prostate cancer, and in endometriosis Endocr. Relat. Cancer 15 3 2008 665 692
33. M.J Reed, A. Singh, M.W. Ghilchik, N.G. Coldham, and A. Purohit Regulation of oestradiol 17 beta hydroxysteroid dehydrogenase in breast tissues: the role of growth factors J. Steroid Biochem. Mol. Biol. 39 5B 1991 791 798
34. A.K. Jansson, C. Gunnarsson, M. Cohen, T. Sivik, and O. Stal 17beta-hydroxysteroid dehydrogenase 14 affects estradiol levels in breast cancer cells and is a prognostic marker in estrogen receptor-positive breast cancer Cancer Res. 66 23 2006 11471 11477 (Pubitemid 46009980)
35. J.A. Aka, M. Mazumdar, and S.X. Lin Reductive 17beta-hydroxysteroid dehydrogenases in the sulfatase pathway: critical in the cell proliferation of breast cancer Mol. Cell. Endocrinol. 301 1-2 2009 183 190
36. M. Frotscher, E. Ziegler, S. Marchais-Oberwinkler, P. Kruchten, A. Neugebauer, L. Fetzer, C. Scherer, U. Muller-Vieira, J. Messinger, H. Thole, and R.W. Hartmann Design, synthesis, and biological evaluation of (hydroxyphenyl)naphthalene and -quinoline derivatives: potent and selective nonsteroidal inhibitors of 17beta-hydroxysteroid dehydrogenase type 1 (17beta-HSD1) for the treatment of estrogen-dependent diseases J. Med. Chem. 51 7 2008 2158 2169 (Pubitemid 351503271)
37. J.M Day, H.J. Tutill, S.P. Newman, A. Purohit, H.R. Lawrence, N. Vicker, B.V. Potter, and M.J. Reed 17Beta-hydroxysteroid dehydrogenase Type 1 and Type 2: association between mRNA expression and activity in cell lines Mol. Cell. Endocrinol. 248 1-2 2006 246 249
38. B. Husen, K. Huhtinen, M. Poutanen, L. Kangas, J. Messinger, and H. Thole Evaluation of inhibitors for 17beta-hydroxysteroid dehydrogenase type 1 in vivo in immunodeficient mice inoculated with MCF-7 cells stably expressing the recombinant human enzyme Mol. Cell. Endocrinol. 248 1-2 2006 109 113
39. A. Purohit, L.W. Woo, B.V. Potter, and M.J. Reed In vivo inhibition of estrone sulfatase activity and growth of nitrosomethylurea-induced mammary tumors by 667 COUMATE Cancer Res. 60 13 2000 3394 3396 (Pubitemid 30482153)
40. P.A. Foster, S.P. Newman, S.K. Chander, C. Stengel, R. Jhalli, L.L. Woo, B.V. Potter, M.J. Reed, and A. Purohit In vivo efficacy of STX213, a second-generation steroid sulfatase inhibitor, for hormone-dependent breast cancer therapy Clin. Cancer Res. 12 18 2006 5543 5549 (Pubitemid 44497272)
41. P.A Foster, S.K. Chander, M.F. Parsons, S.P. Newman, L.W. Woo, B.V. Potter, M.J. Reed, and A. Purohit Efficacy of three potent steroid sulfatase inhibitors: pre-clinical investigations for their use in the treatment of hormone-dependent breast cancer Breast Cancer Res. Treat. 111 1 2008 129 138 (Pubitemid 352009238)
42. A. Billich, J.G. Meingassner, P. Nussbaumer, S. Desrayaud, C. Lam, A. Winiski, and E. Schreiner 6-[2-(Adamantylidene)-hydroxybenzoxazole]-O-sulfamate, a steroid sulfatase inhibitor for the treatment of androgen- and estrogen-dependent diseases J. Steroid Biochem. Mol. Biol. 92 1-2 2004 29 37 (Pubitemid 39486060)
43. H. Ishida, T. Nakata, M. Suzuki, Y. Shiotsu, H. Tanaka, N. Sato, Y. Terasaki, M. Takebayashi, H. Anazawa, C. Murakata, P.K. Li, T. Kuwabara, and S. Akinaga A novel steroidal selective steroid sulfatase inhibitor KW-2581 inhibits sulfated-estrogen dependent growth of breast cancer cells in vitro and in animal models Breast Cancer Res. Treat. 106 2 2007 215 227 (Pubitemid 350045018)
44. L. Sambucetti, C. Green, L. Rausch, W. Chao, S. Le Valley, N. Zaveri, and J. Mirsalis SR 16157 is a potent dual-acting inhibitor of estrogen biosynthesis and estrogen receptor Cancer Res. 69 24 Suppl. 2009 5124 (abstract)
45. S.J. Stanway, A. Purohit, L.W. Woo, S. Sufi, D. Vigushin, R. Ward, R.H. Wilson, F.Z. Stanczyk, N. Dobbs, E. Kulinskaya, M. Elliott, B.V. Potter, M.J. Reed, and R.C. Coombes Phase I study of STX 64 (667 Coumate) in breast cancer patients: the first study of a steroid sulfatase inhibitor Clin. Cancer Res. 12 5 2006 1585 1592
46. R.C. Coombes, P. Schmid, N. Isambert, P. Soulié, F. Cardoso, T. Besse-Hammer, T. Lesimple, D. Slosman, A. Kornowski, V. Fohanno, and P. Fumoleau A Phase I dose escalation study of steroid sulfatase inhibitor BN83495/STX64 in postmenopausal women with ER positive breast cancer Cancer Res. 69 24 Suppl. 2009 4097 abstract
47. L.W. Woo, T. Jackson, A. Putey, G. Cozier, P. Leonard, K.R. Acharya, S.K. Chander, A. Purohit, M.J. Reed, and B.V. Potter Highly potent first examples of dual aromatase-steroid sulfatase inhibitors based on a biphenyl template J. Med. Chem. 53 5 2010 2155 2170
48. M. Numazawa, T. Tominaga, Y. Watari, and Y. Tada Inhibition of estrone sulfatase by aromatase inhibitor-based estrogen 3-sulfamates Steroids 71 5 2006 371 379
49. L.W. Woo, C. Bubert, O.B. Sutcliffe, A. Smith, S.K. Chander, M.F. Mahon, A. Purohit, M.J. Reed, and B.V. Potter Dual aromatase-steroid sulfatase inhibitors J. Med. Chem. 50 15 2007 3540 3560 (Pubitemid 47195462)
50. L.W. Woo, D.S. Fischer, C.M. Sharland, M. Trusselle, P.A. Foster, S.K. Chander, A. Di Fiore, C.T. Supuran, G. De Simone, A. Purohit, M.J. Reed, and B.V. Potter Anticancer steroid sulfatase inhibitors: synthesis of a potent fluorinated second-generation agent, in vitro and in vivo activities, molecular modeling, and protein crystallography Mol. Cancer Ther. 7 8 2008 2435 2444
51. L.W Woo, O.B. Sutcliffe, C. Bubert, A. Grasso, S.K. Chander, A. Purohit, M.J. Reed, and B.V. Potter First dual aromatase-steroid sulfatase inhibitors J. Med. Chem. 46 15 2003 3193 3196 (Pubitemid 36842404)
52. P.M. Wood, L.W. Woo, A. Humphreys, S.K. Chander, A. Purohit, M.J. Reed, and B.V. Potter A letrozole-based dual aromatase-sulphatase inhibitor with in vivo activity J. Steroid Biochem. Mol. Biol. 94 1-3 2005 123 130 (Pubitemid 40614525)
53. T. Jackson, L.W. Woo, M.N. Trusselle, S.K. Chander, A. Purohit, M.J. Reed, and B.V. Potter Dual aromatase-sulfatase inhibitors based on the anastrozole template: synthesis, in vitro SAR, molecular modelling and in vivo activity Org. Biomol. Chem. 5 20 2007 2940 2952
54. L.W Woo, T. Jackson, A. Putey, G. Cozier, P. Leonard, K.R. Acharya, S.K. Chander, A. Purohit, M.J. Reed, and B.V. Potter Highly potent first examples of dual aromatase-steroid sulfatase inhibitors based on a biphenyl template J. Med. Chem. 53 5 2010 2155 2170
55. P.A. Foster, S.K. Chander, S.P. Newman, L.W. Woo, O.B. Sutcliffe, C. Bubert, D. Zhou, S. Chen, B.V. Potter, M.J. Reed, and A. Purohit A new therapeutic strategy against hormone-dependent breast cancer: the preclinical development of a dual aromatase and sulfatase inhibitor Clin. Cancer Res. 14 20 2008 6469 6477