Exploring breast cancer estrogen disposition: The basis for endocrine manipulation

Clinical Cancer Research

Volumn 17, Issue 15, 2011, Pages 4948-4958

  Lønning, Per E ^a,b   Haynes, Ben P ^c   Straume, Anne H ^a,b   Dunbier, Anita ^c   Helle, Hildegunn ^a,b   Knappskog, Stian ^a,b   Dowsett, Mitch ^c  

^a UNIVERSITY OF BERGEN   (Norway)

^b HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^c ROYAL MARSDEN HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANASTROZOLE; CYTOCHROME P450; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; ESTRONE; LETROZOLE;

AROMATIZATION; BREAST CANCER; DISEASE ACTIVITY; DRUG EFFICACY; ENZYME ACTIVITY; ESTROGEN ACTIVITY; ESTROGEN BLOOD LEVEL; ESTROGEN METABOLISM; ESTROGEN SYNTHESIS; GENE EXPRESSION REGULATION; HUMAN; NONHUMAN; PHYSICAL CHEMISTRY; POSTMENOPAUSE; PREMENOPAUSE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RECEPTOR BINDING; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; TISSUE LEVEL; TREATMENT RESPONSE;

BREAST; BREAST NEOPLASMS; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MODELS, BIOLOGICAL; NEOPLASMS, HORMONE-DEPENDENT; SIGNAL TRANSDUCTION;

EID: 79960992886     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-11-0043     Document Type: Review

References (88)

1. Trichopoulos D, MacMahon B, Cole P. Menopause and breast cancer risk. J Natl Cancer Inst 1972;48:605-13.
2. Feinleib M. Breast cancer and artificial menopause: a cohort study. J Natl Cancer Inst 1968;41:315-29.
3. Key T, Appleby P, Barnes I, Reeves G Endogenous Hormones and Breast Cancer Collaborative Group. Endogenous sex hormones and breast cancer in postmenopausal women: reanalysis of nine prospective studies. J Natl Cancer Inst 2002;94:606-16. (Pubitemid 34498648)
4. Russo J, Russo IH. Genotoxicity of steroidal estrogens. Trends Endocrinol Metab 2004;15:211-4. (Pubitemid 38833991)
5. Clemons M, Goss P. Estrogen and the risk of breast cancer. N Engl J Med 2001;344:276-85. (Pubitemid 32108534)
6. Rebbeck TR, Kauff ND, Domchek SM. Meta-analysis of risk reduction estimates associated with risk-reducing salpingo-oophorectomy in BRCA1 or BRCA2 mutation carriers. J Natl Cancer Inst 2009;101:80-7.
7. Carey LA. Targeted chemotherapy? Platinum in BRCA1-dysfunctional breast cancer. J Clin Oncol 2010;28:361-3.
8. Sørlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A 2001;98:10869-74. (Pubitemid 32878711)
9. Abe O, Abe R, Enomoto K, et al. Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet 2005;365:1687-717.
10. Lønning PE. Aromatase inhibitors in breast cancer. Endocr Relat Cancer 2004;11:179-89. (Pubitemid 38832825)
11. Ruder HJ, Loriaux L, Lipsett MB. Estrone sulfate: production rate and metabolism in man. J Clin Invest 1972;51:1020-33.
12. Longcope C. The metabolism of estrone sulfate in normal males. J Clin Endocrinol Metab 1972;34:113-22.
13. Edwards DP, McGuire WL. 17 alpha-Estradiol is a biologically active estrogen in human breast cancer cells in tissue culture. Endocrinology 1980;107:884-91. (Pubitemid 10019072)
14. Suzuki M, Ishida H, Shiotsu Y, Nakata T, Akinaga S, Takashima S, et al. 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.
15. Santner SJ, Feil PD, Santen RJ. 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. (Pubitemid 14087520)
16. Price T, Aitken J, Head J, Mahendroo M, Means G, Simpson E. Determination of aromatase cytochrome P450 messenger ribonucleic acid in human breast tissue by competitive polymerase chain reaction amplification. J Clin Endocrinol Metab 1992;74:1247-52.
17. Esteban JM, Warsi Z, Haniu M, Hall P, Shively JE, Chen S. Detection of intratumoral aromatase in breast carcinomas. An immunohistochemicalstudy with clinicopathologic correlation. Am J Pathol 1992;140: 337-43.
18. Miller WR. Aromatase activity in breast tissue. J Steroid Biochem Mol Biol 1991;39[5B]:783-90.
19. Miller WR, Anderson TJ, Jack WJL. Relationship between tumour aromatase activity, tumour characteristics and response to therapy. J Steroid Biochem Mol Biol 1990;37:1055-9.
20. Bulun SE, Sebastian S, Takayama K, Suzuki T, Sasano H, Shozu M. The human CYP19 (aromatase P450) gene: update on physiologic roles and genomic organization of promoters. J Steroid Biochem Mol Biol 2003;86:219-24. (Pubitemid 37412560)
21. Lønning PE, Dowsett M, Powles TJ. Postmenopausal estrogen synthesis and metabolism: alterations caused by aromatase inhibitors used for the treatment of breast cancer. J Steroid Biochem 1990;35: 355-66. (Pubitemid 20120427)
22. Dowsett M, Cantwell B, Lal A, Jeffcoate SL, Harris AL. Suppression of postmenopausal ovarian steroidogenesis with the luteinizing hormone- releasing hormone agonist goserelin. J Clin Endocrinol Metab 1988;66:672-7.
23. Couzinet B, Meduri G, Lecce MG, Young J, Brailly S, Loosfelt H, et al. The postmenopausal ovary is not a major androgen-producing gland. J Clin Endocrinol Metab 2001;86:5060-6. (Pubitemid 33020564)
24. Sluijmer AV, Heineman MJ, De Jong FH, Evers JL. Endocrine activity of the postmenopausal ovary: the effects of pituitary down-regulation and oophorectomy. J Clin Endocrinol Metab 1995;80:2163-7.
25. Lønning PE, Helle SI, Johannessen DC, Adlercreutz H, Lien EA, Tally M, et al. Relations between sex hormones, sex hormone binding globulin, insulin-like growth factor-I and insulin-like growth factor binding protein-1 in post-menopausal breast cancer patients. Clin Endocrinol (Oxf) 1995;42:23-30.
26. Geisler J, Lønning PE. Aromatase inhibition: translation into a successful therapeutic approach. Clin Cancer Res 2005;11:2809-21. (Pubitemid 40525179)
27. Lønning PE, Geisler J, Johannessen DC, Ekse D. Plasma estrogen suppression with aromatase inhibitors evaluated by a novel, sensitive assay for estrone sulphate. J Steroid Biochem Mol Biol 1997;61:255-60. (Pubitemid 27455686)
28. Dowsett M, Goss PE, Powles TJ, Hutchinson G, Brodie AM, Jeffcoate SL, et al. Use of the aromatase inhibitor 4-hydroxyandrostenedione in postmenopausal breast cancer: optimization of therapeutic dose and route. Cancer Res 1987;47:1957-61. (Pubitemid 17056706)
29. Hankinson SE, Manson JE, Spiegelman D, Willett WC, Longcope C, Speizer FE. Reproducibility of plasma hormone levels in postmenopausal women over a 2-3-year period. Cancer Epidemiol Biomarkers Prev 1995;4:649-54.
30. Lønning PE, Helle H, Duong NK, 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.
31. Lønning PE, Kvinnsland S, Thorsen T, Ueland PM. Alterations in the metabolism of oestrogens during treatment with aminoglutethimide in breast cancer patients. Preliminary findings. Clin Pharmacokinet 1987;13:393-406. (Pubitemid 18018787)
32. Lee AJ, Cai MXX, Thomas PE, Conney AH, Zhu BT. Characterization of the oxidative metabolites of 17beta-estradiol and estrone formed by 15 selectively expressed human cytochrome p450 isoforms. Endocrinology 2003;144:3382-98. (Pubitemid 36904414)
33. Zhou SF, Liu JP, Chowbay B. Polymorphism of human cytochrome P450 enzymes and its clinical impact. Drug Metab Rev 2009;41:89-295.
34. Bolt HM. Metabolism of estrogens-natural and synthetic. Pharmacol Ther 1979;4:155-81.
35. Martucci CP, Fishman J. P450 enzymes of estrogen metabolism. Pharmacol Ther 1993;57:237-57. (Pubitemid 23175382)
36. Lee AJ, Conney AH, Zhu BT. Human cytochrome P450 3A7 has a distinct high catalytic activity for the 16alpha-hydroxylation of estrone but not 17beta-estradiol. Cancer Res 2003;63:6532-6. (Pubitemid 37255207)
37. Hershcopf RJ, Bradlow HL, Fishman J. Differential hydroxylations of estrone and estradiol in man. J Clin Endocrinol Metab 1986;62:170-3. (Pubitemid 16186861)
38. Huang ZQ, Fasco MJ, Figge HL, Keyomarsi K, Kaminsky LS. Expression of cytochromes P450 in human breast tissue and tumors. Drug Metab Dispos 1996;24:899-905. (Pubitemid 26274749)
39. Cribb AE, Knight MJ, Dryer D, Guernsey J, Hender K, Tesch M, et al. Role of polymorphic human cytochrome P450 enzymes in estrone oxidation. Cancer Epidemiol Biomarkers Prev 2006;15:551-8.
40. Adlercreutz H, Höckerstedt K, Bannwart C, Bloigu S, Hämäläinen E, Fotsis T, et al. Effect of dietary components, including lignans and phytoestrogens, on enterohepatic circulation and liver metabolism of estrogens and on sex hormone binding globulin (SHBG). J Steroid Biochem 1987;27:1135-44. (Pubitemid 18020183)
41. Gurpide E. Metabolic influences on the action of estrogens: therapeutic implications. Pediatrics 1978;62:1114-20. (Pubitemid 9091360)
42. Bulun SE, Simpson ER. Regulation of aromatase expression in human tissues. Breast Cancer Res Treat 1994;30:19-29. (Pubitemid 24250756)
43. Jacobs S, MacNeill F, Lønning P, Dowsett M, Jones A, Powles T. Aromatase activity, serum oestradiol and their correlation with demographic indices. J Steroid Biochem Mol Biol 1992;41:769-71.
44. Shozu M, Sebastian S, Takayama K, Hsu WT, Schultz RA, Neely K, et al. Estrogen excess associated with novel gain-of-function mutations affecting the aromatase gene. N Engl J Med 2003;348:1855-65. (Pubitemid 36532311)
45. Smith EP, Boyd J, Frank GR, Takahashi H, Cohen RM, Specker B, et al. Estrogen resistance caused by a mutation in the estrogenreceptor gene in a man. N Engl J Med 1994;331:1056-61. (Pubitemid 24317698)
46. Ma CX, Adjei AA, Salavaggione OE, Coronel J, Pelleymounter L, Wang L, et al. Human aromatase: gene resequencing and functional genomics. Cancer Res 2005;65:11071-82. (Pubitemid 41713378)
47. Colomer R, Monzo M, Tusquets I, Rifa J, Baena JM, Barnadas A, et al. A single-nucleotide polymorphism in the aromatase gene is associated with the efficacy of the aromatase inhibitor letrozole in advanced breast carcinoma. Clin Cancer Res 2008;14:811-6. (Pubitemid 351231164)
48. Wang LW, Ellsworth KA, Moon I, Pelleymounter LL, Eckloff BW, Martin YN, et al. Functional genetic polymorphisms in the aromatase gene CYP19 vary the response of breast cancer patients to neoadjuvant therapy with aromatase inhibitors. Cancer Res 2010;70:319-28.
49. Lønning PE, Johannessen DC, Thorsen T. Alterations in the production rate and the metabolism of oestrone and oestrone sulphate in breast cancer patients treated with aminoglutethimide. Br J Cancer 1989;60:107-11. (Pubitemid 19187757)
50. Lønning PE, Ekse D. A sensitive assay for measurement of plasma estrone sulphate in patients on treatment with aromatase inhibitors. J Steroid Biochem Mol Biol 1995;55:409-12. (Pubitemid 26017225)
51. Geisler J, Berntsen H, Lønning PE. A novel HPLC-RIA method for the simultaneous detection of estrone, estradiol and estrone sulphate levels in breast cancer tissue. J Steroid Biochem Mol Biol 2000;72:259-64. (Pubitemid 30261530)
52. Geisler J, Ekse D, Helle H, Duong NK, Lønning PE. An optimised, highly sensitive radioimmunoassay for the simultaneous measurement of estrone, estradiol and estrone sulfate in the ultra-low range in human plasma samples. J Steroid Biochem Mol Biol 2008;109:90-5.
53. Geisler J, Helle H, Ekse D, Duong NK, Evans DB, Nordbø Y, et al. Letrozole is superior to anastrozole in suppressing breast cancer tissue and plasma estrogen levels. Clin Cancer Res 2008;14:6330-5.
54. Xu X, Roman JM, Issaq HJ, Keefer LK, Veenstra TD, Ziegler RG. Quantitative measurement of endogenous estrogens and estrogen metabolites in human serum by liquid chromatography-tandem mass spectrometry. Anal Chem 2007;79:7813-21. (Pubitemid 47622412)
55. Santen RJ, Demers L, Ohorodnik S, Settlage J, Langecker P, Blanchett D, et al. Superiority of gas chromatography/tandem mass spectrometry assay (GC/MS/MS) for estradiol for monitoring of aromatase inhibitor therapy. Steroids 2007;72:666-71. (Pubitemid 46977432)
56. Lee JS, Ettinger B, Stanczyk FZ, Vittinghoff E, Hanes V, Cauley JA, et al. Comparison of methods to measure low serum estradiol levels in postmenopausal women. J Clin Endocrinol Metab 2006;91:3791-7. (Pubitemid 44536845)
57. Corona G, Elia C, Casetta B, Da Ponte A, Del Pup L, Ottavian E, et al. Liquid chromatography tandem mass spectrometry assay for fast and sensitive quantification of estrone-sulfate. Clin Chim Acta 2010;411:574-80.
58. Blonder J, Johann DJ, Veenstra TD, Xiao Z, Emmert-Buck MR, Ziegler RG, et al. Quantitation of steroid hormones in thin fresh frozen tissue sections. Anal Chem 2008;80:8845-52.
59. Arai S, Miyashiro Y, Shibata Y, Kashiwagi B, Tomaru Y, Kobayashi M, et al. New quantification method for estradiol in the prostatic tissues of benign prostatic hyperplasia using liquid chromatography-tandem mass spectrometry. Steroids 2010;75:13-9.
60. Longcope C, Femino A, Flood C, Williams KIH. Metabolic clearance rate and conversion ratios of [3H]2-hydroxyestrone in normal men. J Clin Endocrinol Metab 1982;54:374-80. (Pubitemid 12006613)
61. Lønning PE, Skulstad P. Alterations in the urine excretion of estrogen metabolites in breast cancer women treated with aminoglutethimide. J Steroid Biochem 1989;33[4A]:565-71. (Pubitemid 19255729)
62. Vermeulen A, Deslypere JP, Paridaens R, Leclercq G, Roy F, Heuson JC. Aromatase, 17 b-hydroxysteroid dehydrogenase and intratissular sex hormone concentrations in cancerous and normal glandular breast tissue in postmenopausal women. Eur J Cancer Clin Oncol 1986;22:515-25. (Pubitemid 16113813)
63. Chetrite GS, Cortes-Prieto J, Philippe JC, Wright F, Pasqualini JR. Comparison of estrogen concentrations, estrone sulfatase and aromatase activities in normal, and in cancerous, human breast tissues. J Steroid Biochem Mol Biol 2000;72:23-7. (Pubitemid 30145713)
64. van Landeghem AA, Poortman J, Nabuurs M, Thijssen JHH. Endogenous concentration and subcellular distribution of estrogens in normal and malignant human breast tissue. Cancer Res 1985; 45:2900-6. (Pubitemid 15232767)
65. Larionov AA, Berstein LM, Miller WR. Local uptake and synthesis of oestrone in normal and malignant postmenopausal breast tissues. J Steroid Biochem Mol Biol 2002;81:57-64. (Pubitemid 34790230)
66. Gurpide E, MacDonald PC, Wiele RLV, Lieberman S. Measurement of the rates of secretion and of peripheral metabolism of two interconvertible compounds: dehydroisoandrosterone-dehydroisoandrosterone sulfate. J Clin Endocrinol Metab 1963;23:346-54.
67. Rowland M, Tozer TN. Clinical pharmacokinetics and pharmacodynamics. 4th ed. Baltimore: Lippincott Williams & Wilkins; 2011.
68. Santner SJ, Leszczynski D, Wright C, Manni A, Feil PD, Santen RJ. Estrone sulfate: a potential source of estradiol in human breast cancer tissues. Breast Cancer Res Treat 1986;7:35-44. (Pubitemid 16120130)
69. Geisler J, King N, Dowsett M, Ottestad L, Lundgren S, Walton P, et al. Influence of anastrozole (Arimidex), a selective, non-steroidal aromatase inhibitor, on in vivo aromatisation and plasma oestrogen levels in postmenopausal women with breast cancer. Br J Cancer 1996; 74:1286-91. (Pubitemid 26360121)
70. Geisler J, Haynes B, Anker G, Dowsett M, Lønning PE. Influence of letrozole (Femara) and anastrozole on total body aromatization and plasma estrogen levels in postmenopausal breast cancer patients evaluated in a randomized, cross-over-designed study. J Clin Oncol 2002;20:751-7. (Pubitemid 34111382)
71. Reed MJ, Owen AM, Lai LC, Coldham NG, Ghilchik MW, Shaikh NA, et al. In situ oestrone synthesis in normal breast and breast tumour tissues: effect of treatment with 4-hydroxyandrostenedione. Int J Cancer 1989;44:233-7. (Pubitemid 19217207)
72. Sasano H, Harada N. Intratumoral aromatase in human breast, endometrial, and ovarian malignancies. Endocr Rev 1998;19:593-607. (Pubitemid 28467713)
73. Sasano H, Anderson TJ, Silverberg SG, Santen RJ, Conway M, Edwards DP, et al. The validation of new aromatase monoclonal antibodies for immunohistochemistry-a correlation with biochemical activities in 46 cases of breast cancer. J Steroid Biochem Mol Biol 2005;95:35-9. (Pubitemid 41137291)
74. Geisler J, Suzuki T, Helle H, Miki Y, Nagasaki S, Duong NK, et al. Breast cancer aromatase expression evaluated by the novel antibody 677: correlations to intra-tumor estrogen levels and hormone receptor status. J Steroid Biochem Mol Biol 2010;118:237-41.
75. Haynes BP, Straume AH, Geisler J, A'Hern R, Helle H, Smith IE, et al. Intratumoral estrogen disposition in breast cancer. Clin Cancer Res 2010;16:1790-801.
76. Poutanen M, Miettinen M, Vihko R. Differential estrogen substrate specificities for transiently expressed human placental 17 beta-hydroxysteroid dehydrogenase and an endogenous enzyme expressed in cultured COS-m6 cells. Endocrinology 1993;133:2639-44. (Pubitemid 24000714)
77. Penning TM, Burczynski ME, Jez JM, Hung CF, Lin HK, Ma H, et al. Human 3alpha-hydroxysteroid dehydrogenase isoforms (AKR1C1-AKR1C4) of the aldo-keto reductase superfamily: functional plasticity and tissue distribution reveals roles in the inactivation and formation of male and female sex hormones. Biochem J 2000;351:67-77.
78. Krazeisen A, Breitling R, Imai K, Fritz S, Möller G, Adamski J. Determination of cDNA, gene structure and chromosomal localization of the novel human 17beta-hydroxysteroid dehydrogenase type 7(1). FEBS Lett 1999;460:373-9. (Pubitemid 29495972)
79. Luu-The V, Tremblay P, Labrie F. Characterization of type 12 17beta-hydroxysteroid dehydrogenase, an isoform of type 3 17beta-hydroxysteroid dehydrogenase responsible for estradiol formation in women. Mol Endocrinol 2006;20:437-43. (Pubitemid 43152516)
80. Wu L, Einstein M, Geissler WM, Chan HK, Elliston KO, Andersson S. Expression cloning and characterization of human 17 beta-hydroxysteroid dehydrogenase type 2, a microsomal enzyme possessing 20 alpha-hydroxysteroid dehydrogenase activity. J Biol Chem 1993;268:12964-9. (Pubitemid 23182471)
81. He XY, Wegiel J, Yang YZ, Pullarkat R, Schulz H, Yang SY. Type 10 17beta-hydroxysteroid dehydrogenase catalyzing the oxidation of steroid modulators of gamma-aminobutyric acid type A receptors. Mol Cell Endocrinol 2005;229:111-7. (Pubitemid 40018089)
82. Lukacik P, Keller B, Bunkoczi G, Kavanagh KL, Lee WH, Adamski J, et al. Structural and biochemical characterization of human orphan DHRS10 reveals a novel cytosolic enzyme with steroid dehydrogenase activity. Biochem J 2007;402:419-27. Erratum in Biochem J 2007;403:615.
83. Everson RB, Lippman ME, Thompson EB, McGuire WL, Wittliff JL, De Sombre ER, et al. Clinical correlations of steroid receptors and male breast cancer. Cancer Res 1980;40:991-7. (Pubitemid 10135797)
84. Perou CM, Sørlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, et al. Molecular portraits of human breast tumours. Nature 2000;406:747-52.
85. Miller WR, Larionov A, Renshaw L, Anderson TJ, Walker JR, Krause A, et al. Gene expression profiles differentiating between breast cancers clinically responsive or resistant to letrozole. J Clin Oncol 2009; 27:1382-7.
86. Dunning AM, Dowsett M, Healey CS, Tee L, Luben RN, Folkerd E, et al. Polymorphisms associated with circulating sex hormone levels in postmenopausal women. J Natl Cancer Inst 2004;96:936-45. (Pubitemid 38868140)
87. Dunbier AK, Anderson H, Ghazoui Z, Folkerd EJ, A'hern R, Crowder RJ, et al. Relationship between plasma estradiol levels and estrogen- responsive gene expression in estrogen receptor-positive breast cancer in postmenopausal women. J Clin Oncol 2010;28: 1161-7.
88. Frasor J, Stossi F, Danes JM, Komm B, Lyttle CR, Katzenellenbogen BS. Selective estrogen receptor modulators: discrimination of agonistic versus antagonistic activities by gene expression profiling in breast cancer cells. Cancer Res 2004;64:1522-33. (Pubitemid 38235626)