Estrone-3-Sulphate, a Potential Novel Ligand for Targeting Breast Cancers

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Banerjee, Nilasha ^a   Fonge, Humphrey ^a   Mikhail, Andrew ^a   Reilly, Raymond M ^a   Bendayan, Reina ^a   Allen, Christine ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRONE SULFATE; ORGANIC ANION TRANSPORTER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD ANALYSIS; BREAST CANCER; CANCER DIAGNOSIS; CELL STRAIN MCF 7; CONTROLLED STUDY; DRUG CLEARANCE; DRUG DISTRIBUTION; DRUG UPTAKE; EX VIVO STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; MICROVASCULARIZATION; MOUSE; MUSCLE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TARGETING; TUMOR VOLUME; TUMOR XENOGRAFT;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; ESTRADIOL; ESTRONE; FEMALE; HUMANS; LIGANDS; MCF-7 CELLS; MICE; MICE, NUDE; ORGANIC CATION TRANSPORT PROTEINS;

EID: 84878091737     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064069     Document Type: Article

References (46)

1. Subramanian A, Salhab M, Mokbel K, (2008) Oestrogen producing enzymes and mammary carcinogenesis: a review. Breast Cancer Res Treat 111: 191-202.
2. Pasqualini JR, (2004) The selective estrogen enzyme modulators in breast cancer: a review. Biochim Biophys Acta 1654: 123-143.
3. Chetrite GS, Cortes-Prieto J, Philippe JC, Wright F, Pasqualini JR (2000) Comparison of estrogen concentrations, estrone sulfatase and aromatase activities in normal, and in cancerous, human breast tissues. J Steroid Biochem Mol Biol 72: 23-27. S0960076000000406 [pii].
4. Chetrite GS, Cortes-Prieto JC, Philippe JC, Pasqualini JR, (2007) Estradiol inhibits the estrone sulfatase activity in normal and cancerous human breast tissues. J Steroid Biochem Mol Biol 104: 289-292 S0960-0760(07)00082-9 [pii];10.1016/j.jsbmb.2007.03.030 [doi].
5. Pasqualini JR, Chetrite G, Blacker C, Feinstein MC, Delalonde L, et al. (1996) 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 81: 1460-1464.
6. Pasqualini JR, Chetrite G, Nguyen BL, Maloche C, Delalonde L, et al. (1995) Estrone sulfate-sulfatase and 17 beta-hydroxysteroid dehydrogenase activities: a hypothesis for their role in the evolution of human breast cancer from hormone-dependence to hormone-independence. J Steroid Biochem Mol Biol 53: 407-412. 0960-0760(95)00116-H [pii].
7. Santner SJ, Leszczynski D, Wright C, Manni A, Feil PD, et al. (1986) Estrone sulfate: a potential source of estradiol in human breast cancer tissues. Breast Cancer Res Treat 7: 35-44.
8. Purohit A, Woo LW, Potter BV, (2011) Steroid sulfatase: a pivotal player in estrogen synthesis and metabolism. Mol Cell Endocrinol 340: 154-160 S0303-7207(11)00320-0 [pii];10.1016/j.mce.2011.06.012 [doi].
9. Utsumi T, Yoshimura N, Takeuchi S, Maruta M, Maeda K, et al. (2000) Elevated steroid sulfatase expression in breast cancers. J Steroid Biochem Mol Biol 73: 141-145.
10. Geisler J (2003) Breast cancer tissue estrogens and their manipulation with aromatase inhibitors and inactivators. J Steroid Biochem Mol Biol 86: 245-253. S0960076003003649 [pii].
11. Van Landeghem AA, Poortman J, Nabuurs M, Thijssen JH, (1985) Endogenous concentration and subcellular distribution of estrogens in normal and malignant human breast tissue. Cancer Res 45: 2900-2906.
12. Tan E, Tirona RG, Pang KS, (1999) Lack of zonal uptake of estrone sulfate in enriched periportal and perivenous isolated rat hepatocytes. Drug Metab Dispos 27: 336-341.
13. Verheugen C, Pardridge WM, Judd HL, Chaudhuri G, (1984) Differential permeability of uterine and liver vascular beds to estrogens and estrogen conjugates. J Clin Endocrinol Metab 59: 1128-1132.
14. Kis O, Zastre JA, Ramaswamy M, Bendayan R, (2010) pH dependence of organic anion-transporting polypeptide 2B1 in Caco-2 cells: potential role in antiretroviral drug oral bioavailability and drug-drug interactions. J Pharmacol Exp Ther 334: 1009-1022.
15. Konig J (2011) Uptake transporters of the human OATP family: molecular characteristics, substrates, their role in drug-drug interactions, and functional consequences of polymorphisms. Handb Exp Pharmacol 1-28. 10.1007/978-3-642-14541-4_1 [doi].
16. Banerjee N, Allen C, Bendayan R, (2012) Differential role of organic anion-transporting polypeptides in estrone-3-sulphate uptake by breast epithelial cells and breast cancer cells. J Pharmacol Exp Ther 342: 510-519 jpet.112.192344 [pii];10.1124/jpet.112.192344 [doi].
17. Meyer zu Schwabedissen HE, Tirona RG, Yip CS, Ho RH, Kim RB, (2008) Interplay between the nuclear receptor pregnane X receptor and the uptake transporter organic anion transporter polypeptide 1A2 selectively enhances estrogen effects in breast cancer. Cancer Res 68: 9338-9347.
18. Miki Y, Suzuki T, Kitada K, Yabuki N, Shibuya R, et al. (2006) Expression of the steroid and xenobiotic receptor and its possible target gene, organic anion transporting polypeptide-A, in human breast carcinoma. Cancer Res 66: 535-542.
19. Kindla J, Rau TT, Jung R, Fasching PA, Strick R, et al. (2011) Expression and localization of the uptake transporters OATP2B1, OATP3A1 and OATP5A1 in non-malignant and malignant breast tissue. Cancer Biol Ther 11: 584-591. 14533 [pii].
20. Zahedi P, De SR, Piquette-Miller M, Allen C, (2011) Docetaxel distribution following intraperitoneal administration in mice. J Pharm Pharm Sci 14: 90-99.
21. Kirpotin DB, Drummond DC, Shao Y, Shalaby MR, Hong K, et al. (2006) Antibody targeting of long-circulating lipidic nanoparticles does not increase tumor localization but does increase internalization in animal models. Cancer Res 66: 6732-6740 66/13/6732 [pii];10.1158/0008-5472.CAN-05-4199 [doi].
22. Scherr FF, Sarmah AK, (2011) Simultaneous analysis of free and sulfo-conjugated steroid estrogens in artificial urine solution and agricultural soils by high-performance liquid chromatography. J Environ Sci Health B 46: 763-772 10.1080/03601234.2012.597702 [doi].
23. Blom MJ, Wassink MG, Kloosterboer HJ, Ederveen AG, Lambert JG, et al. (2001) Metabolism of estradiol, ethynylestradiol, and moxestrol in rat uterus, vagina, and aorta: influence of sex steroid treatment. Drug Metab Dispos 29: 76-81.
24. Fung AS, Jonkman J, Tannock IF, (2012) Quantitative immunohistochemistry for evaluating the distribution of Ki67 and other biomarkers in tumor sections and use of the method to study repopulation in xenografts after treatment with paclitaxel. Neoplasia 14: 324-334.
25. Obaidat A, Roth M, Hagenbuch B, (2012) The expression and function of organic anion transporting polypeptides in normal tissues and in cancer. Annu Rev Pharmacol Toxicol 52: 135-151 10.1146/annurev-pharmtox-010510-100556 [doi].
26. Pizzagalli F, Varga Z, Huber RD, Folkers G, Meier PJ, et al. (2003) Identification of steroid sulfate transport processes in the human mammary gland. J Clin Endocrinol Metab 88: 3902-3912.
27. Wlcek K, Svoboda M, Thalhammer T, Sellner F, Krupitza G, et al. (2008) Altered expression of organic anion transporter polypeptide (OATP) genes in human breast carcinoma. Cancer Biol Ther 7: 1450-1455. 6282 [pii].
28. Lonning PE, Haynes BP, Straume AH, Dunbier A, Helle H, et al. (2011) Recent data on intratumor estrogens in breast cancer. Steroids 76: 786-791 S0039-128X(11)00080-8 [pii];10.1016/j.steroids.2011.02.040 [doi].
29. Sacco SM, Power KA, Chen J, Ward WE, Thompson LU (2007) Interaction of sesame seed and tamoxifen on tumor growth and bone health in athymic mice. Exp Biol Med (Maywood) 232: 754-761. 232/6/754 [pii].
30. Tan E, Lu T, Pang KS, (2001) Futile cycling of estrone sulfate and estrone in the recirculating perfused rat liver preparation. J Pharmacol Exp Ther 297: 423-436.
31. Tan E, Pang KS, (2001) Sulfation is rate limiting in the futile cycling between estrone and estrone sulfate in enriched periportal and perivenous rat hepatocytes. Drug Metab Dispos 29: 335-346.
32. Back DJ, Breckenridge AM, Crawford FE, Giles M, Orme ML, et al. (1981) The pharmacokinetics of oestrone sulphate in the rat. J Steroid Biochem 14: 1045-1047.
33. Nozawa T, Suzuki M, Yabuuchi H, Irokawa M, Tsuji A, et al. (2005) Suppression of cell proliferation by inhibition of estrone-3-sulfate transporter in estrogen-dependent breast cancer cells. Pharm Res 22: 1634-1641.
34. Pasqualini JR, Chetrite G, Nestour EL, (1996) Control and expression of oestrone sulphatase activities in human breast cancer. J Endocrinol 150Suppl: S99-105.
35. Hagenbuch B, (2010) Drug uptake systems in liver and kidney: a historic perspective. Clin Pharmacol Ther 87: 39-47.
36. Ismair MG, Stieger B, Cattori V, Hagenbuch B, Fried M, et al. (2001) Hepatic uptake of cholecystokinin octapeptide by organic anion-transporting polypeptides OATP4 and OATP8 of rat and human liver. Gastroenterology 121: 1185-1190.
37. Kullak-Ublick GA, Ismair MG, Stieger B, Landmann L, Huber R, et al. (2001) Organic anion-transporting polypeptide B (OATP-B) and its functional comparison with three other OATPs of human liver. Gastroenterology 120: 525-533.
38. Meier PJ, Eckhardt U, Schroeder A, Hagenbuch B, Stieger B, (1997) Substrate specificity of sinusoidal bile acid and organic anion uptake systems in rat and human liver. Hepatology 26: 1667-1677.
39. Ahmed N, Garcia G, Ali H, van Lier JE, (2009) (18)F-labelling of A-ring substituted 16alpha-fluoro-estradiols as potential radiopharmaceuticals for PET imaging. Steroids 74: 42-50.
40. Benard F, Ahmed N, Beauregard JM, Rousseau J, Aliaga A, et al. (2008) [18F]Fluorinated estradiol derivatives for oestrogen receptor imaging: impact of substituents, formulation and specific activity on the biodistribution in breast tumour-bearing mice. Eur J Nucl Med Mol Imaging 35: 1473-1479.
41. Osborne JR, Port E, Gonen M, Doane A, Yeung H, et al. (2010) 18F-FDG PET of locally invasive breast cancer and association of estrogen receptor status with standardized uptake value: microarray and immunohistochemical analysis. J Nucl Med 51: 543-550.
42. Scharl A, Kullander S, Beckmann MW, Spicer JA, Baranczuk RJ, et al. (1991) Prolonged clearance of intraperitoneal 16 alpha-[125I]iodo-17 beta-estradiol in presence of ascites. Am J Obstet Gynecol 165: 1847-1853.
43. Howell A, Bundred NJ, Cuzick J, Allred DC, Clarke R, (2008) Response and resistance to the endocrine prevention of breast cancer. Adv Exp Med Biol 617: 201-211 10.1007/978-0-387-69080-3_19 [doi].
44. Nicholson RI, Johnston SR, (2005) Endocrine therapy-current benefits and limitations. Breast Cancer Res Treat 93Suppl 1: S3-10 10.1007/s10549-005-9036-4 [doi].
45. Hayes E, Nicholson RI, Hiscox S (2011) Acquired endocrine resistance in breast cancer: implications for tumour metastasis. Front Biosci 16: 838-848. 3723 [pii].
46. Roop RP, Ma CX, (2012) Endocrine resistance in breast cancer: molecular pathways and rational development of targeted therapies. Future Oncol 8: 273-292 10.2217/fon.12.8 [doi].