Steroid sulfatase and estrogen sulfotransferase in human carcinomas

Molecular and Cellular Endocrinology

Volumn 340, Issue 2, 2011, Pages 148-153

  Suzuki, Takashi ^a   Miki, Yasuhiro ^a   Nakamura, Yasuhiro ^a   Ito, Kiyoshi ^a   Sasano, Hironobu ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Carcinoma; Estrogen; Estrogen sulfotransferase; Steroid sulfatase

Indexed keywords

ANDROGEN; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; ESTROGEN SULFOTRANSFERASE; ESTRONE SULFATE; STERYL SULFATASE;

BREAST CARCINOMA; CANCER RECURRENCE; CANCER RISK; CANCER SURVIVAL; COLON CARCINOMA; DISEASE ASSOCIATION; ENDOMETRIUM CARCINOMA; ENZYME ACTIVATION; ENZYME ACTIVITY; ESTROGEN SYNTHESIS; HUMAN; NONHUMAN; OVARY CARCINOMA; PRIORITY JOURNAL; PROGNOSIS; PROSTATE CARCINOMA; PROTEIN EXPRESSION; REVIEW; RISK FACTOR; TUMOR GROWTH;

CARCINOMA; HUMANS; MODELS, BIOLOGICAL; STERYL-SULFATASE; SULFOTRANSFERASES;

EID: 79960251341     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2010.11.001     Document Type: Review

References (73)

1. Abulafia O., Lee Y.C., Wagreich A., Economos K., Serur E., Nacharaju V.L. Sulfatase activity in normal and neoplastic endometrium. Gynecol. Obstet. Invest. 2009, 67:57-60.
2. Adjei A.A., Thomae B.A., Prondzinski J.L., Eckloff B.W., Wieben E.D., Weinshilboum R.M. Human estrogen sulfotransferase (SULT1E1) pharmacogenomics: gene resequencing and functional genomics. Br. J. Pharmacol. 2003, 139:1373-1382.
3. Anderson G.L., Limacher M., Assaf A.R., Bassford T., Beresford S.A., Black H., Bonds D., Brunner R., Brzyski R., Caan B., Chlebowski R., Curb D., Gass M., Hays J., Heiss G., Hendrix S., Howard B.V., Hsia J., Hubbell A., Jackson R., Johnson K.C., Judd H., Kotchen J.M., Kuller L., LaCroix A.Z., Lane D., Langer R.D., Lasser N., Lewis C.E., Manson J., Margolis K., Ockene J., O'Sullivan M.J., Phillips L., Prentice R.L., Ritenbaugh C., Robbins J., Rossouw J.E., Sarto G., Stefanick M.L., Van Horn L., Wactawski-Wende J., Wallace R., Wassertheil-Smoller S. Women's Health Initiative Steering Committee. Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled trial. JAMA 2004, 291:1701-1712.
4. Berstein L.M., Tchernobrovkina A.E., Gamajunova V.B., Kovalevskij A.J., Vasilyev D.A., Chepik O.F., Turkevitch E.A., Tsyrlina E.V., Maximov S.J., Ashrafian L.A., Thijssen J.H. Tumor estrogen content and clinico-morphological and endocrine features of endometrial cancer. J. Cancer Res. Clin. Oncol. 2003, 129:245-249.
5. Chetrite G.S., Cortes-Prieto J., Philippe J.C., Wright F., Pasqualini J.R. Comparison of estrogen concentrations, estrone sulfatase and aromatase activities in normal, and in cancerous, human breast tissues. J. Steroid Biochem. Mol. Biol. 2000, 72:23-27.
6. Choi J.Y., Lee K.M., Park S.K., Noh D.Y., Ahn S.H., Chung H.W., Han W., Kim J.S., Shin S.G., Jang I.J., Yoo K.Y., Hirvonen A., Kang D. Genetic polymorphisms of SULT1A1 and SULT1E1 and the risk and survival of breast cancer. Cancer Epidemiol. Biomarkers Prev. 2005, 14:1090-1095.
7. Chura J.C., Blomquist C.H., Ryu H.S., Argenta P.A. Estrone sulfatase activity in patients with advanced ovarian cancer. Gynecol. Oncol. 2009, 112:205-209.
8. Dassen H., Punyadeera C., Kamps R., Delvoux B., Van Langendonckt A., Donnez J., Husen B., Thole H., Dunselman G., Groothuis P. Estrogen metabolizing enzymes in endometrium and endometriosis. Hum. Reprod. 2007, 22:3148-3158.
9. Day J.M., Purohit A., Tutill H.J., Foster P.A., Woo L.W., Potter B.V., Reed M.J. The development of steroid sulfatase inhibitors for hormone-dependent cancer therapy. Ann. N. Y. Acad. Sci. 2009, 1155:80-87.
10. Evans T.R., Rowlands M.G., Law M., Coombes R.C. Intratumoral oestrone sulphatase activity as a prognostic marker in human breast carcinoma. Br. J. Cancer 1994, 69:555-561.
11. Falany J.L., Macrina N., Falany C.N. Regulation of MCF-7 breast cancer cell growth by beta-estradiol sulfation. Breast Cancer Res. Treat. 2002, 74:167-176.
12. Foster P.A., Reed M.J., Purohit A. Recent developments of steroid sulfatase inhibitors as anti-cancer agents. Anticancer Agents Med. Chem. 2008, 8:732-738.
13. Fu J., Weise A.M., Falany J.L., Falany C.N., Thibodeau B.J., Miller F.R., Kocarek T.A., Runge-Morris M. Expression of estrogenicity genes in a lineage cell culture model of human breast cancer progression. Breast Cancer Res. Treat. 2009, (Epub ahead of print).
14. Ghosh D. Mutations in X-linked ichthyosis disrupt the active site structure of estrone/DHEA sulfatase. Biochim. Biophys. Acta 2004, 1739:1-4.
15. Ghosh D. Human sulfatases: a structural perspective to catalysis. Cell. Mol. Life Sci. 2007, 64:2013-2022.
16. Giton F., de la Taille A., Allory Y., Galons H., Vacherot F., Soyeux P., Abbou C.C., Loric S., Cussenot O., Raynaud J.P., Fiet J. Estrone sulfate (E1S), a prognosis marker for tumor aggressiveness in prostate cancer (PCa). J. Steroid Biochem. Mol. Biol. 2008, 109:158-167.
17. Goodarzi M.O., Antoine H.J., Azziz R. Genes for enzymes regulating dehydroepiandrosterone sulfonation are associated with levels of dehydroepiandrosterone sulfate in polycystic ovary syndrome. J. Clin. Endocrinol. Metab. 2007, 92:2659-2664.
18. Grodstein F., Newcomb P.A., Stampfer M.J. Postmenopausal hormone therapy and the risk of colorectal cancer: a review and meta-analysis. Am. J. Med. 1999, 106:574-582.
19. Hagenbuch B., Meier P.J. The superfamily of organic anion transporting polypeptides. Biochim. Biophys. Acta 2003, 1609:1-18.
20. Härkönen P.L., Mäkelä S.I. Role of estrogens in development of prostate cancer. J. Steroid Biochem. Mol. Biol. 2004, 92:297-305.
21. Hirata H., Hinoda Y., Okayama N., Suehiro Y., Kawamoto K., Kikuno N., Rabban J.T., Chen L.M., Dahiya R. CYP1A1, SULT1A1, and SULT1E1 polymorphisms are risk factors for endometrial cancer susceptibility. Cancer 2008, 112:1964-1973.
22. Hudelist G., Wülfing P., Kersting C., Burger H., Mattsson B., Czerwenka K., Kubista E., Gschwantler-Kaulich D., Fink-Retter A., Singer C.F. Expression of aromatase and estrogen sulfotransferase in preinvasive and invasive breast cancer. J. Cancer Res. Clin. Oncol. 2008, 134:67-73.
23. Hui Y., Yasuda S., Liu M.Y., Wu Y.Y., Liu M.C. On the sulfation and methylation of catecholestrogens in human mammary epithelial cells and breast cancer cells. Biol. Pharm. Bull. 2008, 31:769-773.
24. Iida A., Sekine A., Saito S., Kitamura Y., Kitamoto T., Osawa S., Mishima C., Nakamura Y. Catalog of 320 single nucleotide polymorphisms (SNPs) in 20 quinone oxidoreductase and sulfotransferase genes. J. Hum. Genet. 2001, 46:225-240.
25. Irahara N., Miyoshi Y., Taguchi T., Tamaki Y., Noguchi S. Quantitative analysis of aromatase, sulfatase and 17beta-HSD(1) mRNA expression in soft tissue metastases of breast cancer. Cancer Lett. 2006, 243:23-31.
26. Kapoor R., Sheng J.J. Transfection of human prostate cancer CA-HPV-10 cells with cytosolic sulfotransferase SULT1E1 affects estrogen signaling and gene transcription. Drug Metab. Dispos. 2008, 36:316-321.
27. Kirilovas D., Schedvins K., Naessén T., Von Schoultz B., Carlström K. Conversion of circulating estrone sulfate to 17beta-estradiol by ovarian tumor tissue: a possible mechanism behind elevated circulating concentrations of 17beta-estradiol in postmenopausal women with ovarian tumors. Gynecol. Endocrinol. 2007, 23:25-28.
28. Labrie F., Luu-The V., Labrie C., Belanger A., Simard J., Lin S.X., Pelletier G. Endocrine and intracrine sources of androgens in women: inhibition of breast cancer and other roles of androgens and their precursor dehydroepiandrosterone. Endocr. Rev. 2003, 24:152-182.
29. Lønning P.E., Helle H., Duong N.K., Ekse D., Aas T., Geisler J. Tissue estradiol is selectively elevated in receptor positive breast cancers while tumour estrone is reduced independent of receptor status. J. Steroid Biochem. Mol. Biol. 2009, 117:31-41.
30. Mandelson M.T., Miglioretti D., Newcomb P.A., Harrison R., Potter J.D. Hormone replacement therapy in relation to survival in women diagnosed with colon cancer. Cancer Causes Control 2003, 14:979-984.
31. Matsumoto J., Ariyoshi N., Ishii I., Kitada M. Six novel single nucleotide polymorphisms of the steroid sulfatase gene in a Japanese population. Drug Metab. Pharmacokinet. 2010, 25:403-407.
32. Miki Y., Nakata T., Suzuki T., Darnel A.D., Moriya T., Kaneko C., Hidaka K., Shiotsu Y., Kusaka H., Sasano H. Systemic distribution of steroid sulfatase and estrogen sulfotransferase in human adult and fetal tissues. J. Clin. Endocrinol. Metab. 2002, 87:5760-5768.
33. Miki Y., Suzuki T., Kitada K., Yabuki N., Shibuya R., Moriya T., Ishida T., Ohuchi N., Blumberg B., Sasano H. Expression of the steroid and xenobiotic receptor and its possible target gene, organic anion transporting polypeptide-A, in human breast carcinoma. Cancer Res. 2006, 66:535-542.
34. Milewich L., Porter J.C. In situ steroid sulfatase activity in human epithelial carcinoma cells of vaginal, ovarian, and endometrial origin. J. Clin. Endocrinol. Metab. 1987, 65:164-169.
35. Miyoshi Y., Ando A., Hasegawa S., Ishitobi M., Taguchi T., Tamaki Y., Noguchi S. High expression of steroid sulfatase mRNA predicts poor prognosis in patients with estrogen receptor-positive breast cancer. Clin. Cancer Res. 2003, 9:2288-2293.
36. Muto M., Onogawa T., Suzuki T., Ishida T., Rikiyama T., Katayose Y., Ohuchi N., Sasano H., Abe T., Unno M. Human liver-specific organic anion transporter-2 is a potent prognostic factor for human breast carcinoma. Cancer Sci. 2007, 98:1570-1576.
37. Nagasaki S., Miki Y., Akahira J., Suzuki T., Sasano H. 17beta-hydroxysteroid dehydrogenases in human breast cancer. Ann. N. Y. Acad. Sci. 2009, 1155:25-32.
38. Nakamura Y., Suzuki T., Fukuda T., Ito A., Endo M., Moriya T., Arai Y., Sasano H. Steroid sulfatase and estrogen sulfotransferase in human prostate cancer. Prostate 2006, 66:1005-1012.
39. Nardi A., Pomari E., Zambon D., Belvedere P., Colombo L., Dalla Valle L. Transcriptional control of human steroid sulfatase. J. Steroid Biochem. Mol. Biol. 2009, 115:68-74.
40. Newcomb P.A., Zheng Y., Chia V.M., Morimoto L.M., Doria-Rose V.P., Templeton A., Thibodeau S.N., Potter J.D. Estrogen plus progestin use, microsatellite instability, and the risk of colorectal cancer in women. Cancer Res. 2007, 67:7534-7539.
41. Newman S.P., Purohit A., Ghilchik M.W., Potter B.V., Reed M.J. Regulation of steroid sulphatase expression and activity in breast cancer. J. Steroid Biochem. Mol. Biol. 2000, 75:259-264.
42. O'Connor M.I. Osteoarthritis of the hip and knee: sex and gender differences. Orthop. Clin. North Am. 2006, 37:559-568.
43. Okuda T., Saito H., Sekizawa A., Shimizu Y., Akamatsu T., Kushima M., Yanaihara T., Okai T., Farina A. Steroid sulfatase expression in ovarian clear cell adenocarcinoma: immunohistochemical study. Gynecol. Oncol. 2001, 82:427-434.
44. Pasqualini J.R. The selective estrogen enzyme modulators in breast cancer: a review. Biochim. Biophys. Acta 2004, 1654:123-143.
45. Pasqualini J.R. Estrogen sulfotransferases in breast and endometrial cancers. Ann. N. Y. Acad. Sci. 2009, 1155:88-98.
46. Pasqualini J.R., Chetrite G., Blacker C., Feinstein M.C., Delalonde L., Talbi M., Maloche C. Concentrations of estrone, estradiol, and estrone sulfate and evaluation of sulfatase and aromatase activities in pre- and postmenopausal breast cancer patients. J. Clin. Endocrinol. Metab. 1996, 81:1460-1464.
47. Qian Y., Deng C., Song W.C. Expression of estrogen sulfotransferase in MCF-7 cells by cDNA transfection suppresses the estrogen response: potential role of the enzyme in regulating estrogen-dependent growth of breast epithelial cells. J. Pharmacol. Exp. Ther. 1998, 286:555-560.
48. Ragonese P., D'Amelio M., Savettieri G. Implications for estrogens in Parkinson's disease: an epidemiological approach. Ann. N. Y. Acad. Sci. 2006, 1089:373-382.
49. Rebbeck T.R., Troxel A.B., Wang Y., Walker A.H., Panossian S., Gallagher S., Shatalova E.G., Blanchard R., Bunin G., DeMichele A., Rubin S.C., Baumgarten M., Berlin M., Schinnar R., Berlin J.A., Strom B.L. Estrogen sulfation genes, hormone replacement therapy, and endometrial cancer risk. J. Natl. Cancer Inst. 2006, 98:1311-1320.
50. Reed M.J., Purohit A., Woo L.W., Newman S.P., Potter B.V. Steroid sulfatase: molecular biology, regulation, and inhibition. Endocr. Rev. 2005, 26:171-202.
51. Saeki T., Takashima S., Sasaki H., Hanai N., Salomon D.S. Localization of estrone sulfatase in human breast carcinomas. Breast Cancer 1999, 6:331-337.
52. Santner S.J., Feil P.D., Santen R.J. In situ estrogen production via the estrone sulfatase pathway in breast tumors: relative importance versus the aromatase pathway. J. Clin. Endocrinol. Metab. 1984, 59:29-33.
53. Sato R., Suzuki T., Katayose Y., Miura K., Shiiba K., Tateno H., Miki Y., Akahira J., Kamogawa Y., Nagasaki S., Yamamoto K., Ii T., Egawa S., Evans D.B., Unno M., Sasano H. Steroid sulfatase and estrogen sulfotransferase in colon carcinoma: regulators of intratumoral estrogen concentrations and potent prognostic factors. Cancer Res. 2009, 69:914-922.
54. Selcer K.W., Difrancesca H.M., Chandra A.B., Li P.K. Immunohistochemical analysis of steroid sulfatase in human tissues. J. Steroid Biochem. Mol. Biol. 2007, 105:115-123.
55. Shibuya R., Suzuki T., Miki Y., Yoshida K., Moriya T., Ono K., Akahira J., Ishida T., Hirakawa H., Evans D.B., Sasano H. Intratumoral concentration of sex steroids and expression of sex steroid-producing enzymes in ductal carcinoma in situ of human breast. Endocr. Relat. Cancer 2008, 15:113-124.
56. Smuc T., Rizner T.L. Aberrant pre-receptor regulation of estrogen and progesterone action in endometrial cancer. Mol. Cell. Endocrinol. 2009, 301:74-82.
57. Stanway S.J., Purohit A., Woo L.W., Sufi S., Vigushin D., Ward R., Wilson R.H., Stanczyk F.Z., Dobbs N., Kulinskaya E., Elliott M., Potter B.V., Reed M.J., Coombes R.C. Phase I study of STX 64 (667 Coumate) in breast cancer patients: the first study of a steroid sulfatase inhibitor. Clin. Cancer Res. 2006, 12:1585-1589.
58. Suzuki T., Nakata T., Miki Y., Kaneko C., Moriya T., Ishida T., Akinaga S., Hirakawa H., Kimura M., Sasano H. Estrogen sulfotransferase and steroid sulfatase in human breast carcinoma. Cancer Res. 2003, 63:2762-2770.
59. Suzuki T., Miki Y., Nakamura Y., Moriya T., Ito K., Ohuchi N., Sasano H. Sex steroid-producing enzymes in human breast cancer. Endocr. Relat. Cancer 2005, 12:701-720.
60. Suzuki M., Ishida H., Shiotsu Y., Nakata T., Akinaga S., Takashima S., Utsumi T., Saeki T., Harada N. Expression level of enzymes related to in situ estrogen synthesis and clinicopathological parameters in breast cancer patients. J. Steroid Biochem. Mol. Biol. 2009, 113:195-201.
61. Takase Y., Luu-The V., Poisson-Paré D., Labrie F., Pelletier G. Expression of sulfotransferase 1E1 in human prostate as studied by in situ hybridization and immunocytochemistry. Prostate 2007, 67:405-409.
62. Tseng L., Mazella J., Lee L.Y., Stone M.L. Estrogen sulfatase and estrogen sulfotransferase in human primary mammary carcinoma. J. Steroid Biochem. 1983, 4:1413-1417.
63. Tsunoda Y., Shimizu Y., Tsunoda A., Takimoto M., Sakamoto M.A., Kusano M. Steroid sulfatase in breast carcinoma and change of serum estrogens levels after operation. Acta Oncol. 2006, 45:584-589.
64. Udler M.S., Azzato E.M., Healey C.S., Ahmed S., Pooley K.A., Greenberg D., Shah M., Teschendorff A.E., Caldas C., Dunning A.M., Ostrander E.A., Caporaso N.E., Easton D., Pharoah P.D. Common germline polymorphisms in COMT, CYP19A1, ESR1, PGR, SULT1E1 and STS and survival after a diagnosis of breast cancer. Int. J. Cancer 2009, 125:2687-2696.
65. Utsumi T., Yoshimura N., Takeuchi S., Ando J., Maruta M., Maeda K., Harada N. Steroid sulfatase expression is an independent predictor of recurrence in human breast cancer. Cancer Res. 1999, 59:377-381.
66. Utsunomiya H., Ito K., Suzuki T., Kitamura T., Kaneko C., Nakata T., Niikura H., Okamura K., Yaegashi N., Sasano H. Steroid sulfatase and estrogen sulfotransferase in human endometrial carcinoma. Clin. Cancer Res. 2004, 10:5850-5856.
67. Valle L.D., Toffolo V., Nardi A., Fiore C., Bernante P., Di Liddo R., Parnigotto P.P., Colombo L. Tissue-specific transcriptional initiation and activity of steroid sulfatase complementing dehydroepiandrosterone sulfate uptake and intracrine steroid activations in human adipose tissue. J. Endocrinol. 2006, 190:129-139.
68. Valle L.D., Toffolo V., Nardi A., Fiore C., Armanini D., Belvedere P., Colombo L. The expression of the human steroid sulfatase-encoding gene is driven by alternative first exons. J. Steroid Biochem. Mol. Biol. 2007, 107:22-29.
69. Wong N.A., Malcomson R.D., Jodrell D.I., Groome N.P., Harrison D.J., Saunders P.T. ERbeta isoform expression in colorectal carcinoma: an in vivo and in vitro study of clinicopathological and molecular correlates. J. Pathol. 2005, 207:53-60.
70. Yamamoto Y., Yamashita J., Toi M., Muta M., Nagai S., Hanai N., Furuya A., Osawa Y., Saji S., Ogawa M. Immunohistochemical analysis of estrone sulfatase and aromatase in human breast cancer tissues. Oncol. Rep. 2003, 10:791-796.
71. Yoshimura N., Harada N., Bukholm I., Karesen R., Borresen-Dale A.L., Kristensen V.N. Intratumoural mRNA expression of genes from the oestradiol metabolic pathway and clinical and histopathological parameters of breast cancer. Breast Cancer Res. 2004, 6:R46-55.
72. Zaichuk T., Ivancic D., Scholtens D., Schiller C., Khan S.A. Tissue-specific transcripts of human steroid sulfatase are under control of estrogen signaling pathways in breast carcinoma. J. Steroid Biochem. Mol. Biol. 2007, 105:76-84.
73. Zhang H., Varlamova O., Vargas F.M., Falany C.N., Leyh T.S. Sulfuryl transfer: the catalytic mechanism of human estrogen sulfotransferase. J. Biol. Chem. 1998, 273:10888-10892.