Androgens and Breast Cancer in Men and Women

Endocrinology and Metabolism Clinics of North America

Volumn 40, Issue 3, 2011, Pages 533-547

  Dimitrakakis, Constantine ^a,b  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

Author keywords

Androgens; Breast cancer; Hormone therapy; Male breast cancer; Menopause; Testosterone

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; BOLDENONE; BRCA1 PROTEIN; ESTROGEN; ESTROGEN RECEPTOR; FLUTAMIDE; GESTAGEN; ORAL CONTRACEPTIVE AGENT; PLACEBO; TESTOSTERONE;

BODY MASS; BREAST; BREAST ATROPHY; BREAST CANCER; BREAST EPITHELIUM; CANCER HORMONE THERAPY; CANCER INCIDENCE; CANCER RECURRENCE; CANCER RISK; CANCER SURVIVAL; CELL PROLIFERATION; DRUG SAFETY; FEMALE SEXUAL DYSFUNCTION; GYNECOMASTIA; HUMAN; HYPOGONADISM; NONHUMAN; POSTMENOPAUSE; PREMENOPAUSE; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN BINDING; PROTEIN EXPRESSION; REVIEW; STEROID METABOLISM; TUMOR GROWTH; TUMOR VOLUME;

ANDROGENS; ANIMALS; BREAST; BREAST NEOPLASMS; BREAST NEOPLASMS, MALE; CARCINOMA; FEMALE; HUMANS; MALE; PRIMATES; RECEPTORS, ANDROGEN;

PRIMATES;

EID: 80052205280     PISSN: 08898529     EISSN: 15584410     Source Type: Journal    
DOI: 10.1016/j.ecl.2011.05.007     Document Type: Review

References (72)

1. Davis S.R., Moreau M., Kroll R., et al. Testosterone for low libido in postmenopausal women not taking estrogen. N Engl J Med 2008, 359(19):2005-2017.
2. The role of testosterone therapy in postmenopausal women: position statement of The North American Menopause Society. Menopause 2005, 12(5):496-511. North American Menopause Society, [quiz: 649].
3. Schover L.R. Androgen therapy for loss of desire in women: is the benefit worth the breast cancer risk?. Fertil Steril 2008, 90(1):129-140.
4. Dimitrakakis C., Zhou J., Wang J., et al. A physiologic role for testosterone in limiting estrogenic stimulation of the breast. Menopause 2003, 10(4):292-298.
5. Binder G., Iliev D.I., Dufke A., et al. Dominant transmission of prepubertal gynecomastia due to serum estrone excess: hormonal, biochemical, and genetic analysis in a large kindred. J Clin Endocrinol Metab 2005, 90(1):484-492.
6. Kadlubar F., Berkowitz G., Delongchamp R., et al. The CYP3A4*1B variant is related to the onset of puberty, a known risk factor for the development of breast cancer. Cancer Epidemiol Biomarkers Prev 2003, 12(4):327-331.
7. Forsbach G., Guitron-Cantu A., Vazquez-Lara J., et al. Virilizing adrenal adenoma and primary amenorrhea in a girl with adrenal hyperplasia. Arch Gynecol Obstet 2000, 263(3):134-136.
8. Karamanakos P., Mitsiades C.S., Lembessis P., et al. Male breast adenocarcinoma in a prostate cancer patient following prolonged anti-androgen monotherapy. Anticancer Res 2004, 24(2C):1077-1081.
9. Braunstein G.D. Clinical practice. Gynecomastia. N Engl J Med 2007, 357(12):1229-1237.
10. Labrie F. Dehydroepiandrosterone, androgens and the mammary gland. Gynecol Endocrinol 2006, 22(3):118-130.
11. Lobo R.A. Androgens in postmenopausal women: production, possible role, and replacement options. Obstet Gynecol Surv 2001, 56(6):361-376.
12. Labrie F., Belanger A., Simard J., et al. DHEA and peripheral androgen and estrogen formation: intracrinology. Ann N Y Acad Sci 1995, 774:16-28.
13. Labrie F., Luu-The V., Lin S.X., et al. Intracrinology: role of the family of 17 beta-hydroxysteroid dehydrogenases in human physiology and disease. J Mol Endocrinol 2000, 25(1):1-16.
14. Sasano H., Suzuki T., Nakata T., et al. New development in intracrinology of breast carcinoma. Breast Cancer 2006, 13(2):129-136.
15. Birrell S.N., Bentel J.M., Hickey T.E., et al. Androgens induce divergent proliferative responses in human breast cancer cell lines. J Steroid Biochem Mol Biol 1995, 52(5):459-467.
16. Suzuki M., Ishida H., Shiotsu Y., 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(3-5):195-201.
17. Federman D.D. The biology of human sex differences. N Engl J Med 2006, 354(14):1507-1514.
18. Zhou J., Anderson K., Bievre M., et al. Primate mammary gland insulin-like growth factor system: cellular localization and regulation by sex steroids. J Investig Med 2001, 49(1):47-55.
19. Park J.J., Irvine R.A., Buchanan G., et al. Breast cancer susceptibility gene 1 (BRCAI) is a coactivator of the androgen receptor. Cancer Res 2000, 60(21):5946-5949.
20. Spurdle A.B., Antoniou A.C., Duffy D.L., et al. The androgen receptor CAG repeat polymorphism and modification of breast cancer risk in BRCA1 and BRCA2 mutation carriers. Breast Cancer Res 2005, 7(2):R176-R183.
21. Avila D.M., Zoppi S., McPhaul M.J. The androgen receptor (AR) in syndromes of androgen insensitivity and in prostate cancer. J Steroid Biochem Mol Biol 2001, 76(1-5):135-142.
22. Polymorphisms in genes of the steroid receptor superfamily modify postmenopausal breast cancer risk associated with menopausal hormone therapy. Int J Cancer 2010, 126(12):2935-2946. MARIE-GENICA Consortium on Genetic Susceptibility for Menopausal Hormone Therapy Related Breast Cancer Risk.
23. Weiss J.R., Moysich K.B., Swede H. Epidemiology of male breast cancer. Cancer Epidemiol Biomarkers Prev 2005, 14(1):20-26.
24. Cox D.G., Blanche H., Pearce C.L., et al. A comprehensive analysis of the androgen receptor gene and risk of breast cancer: results from the National Cancer Institute Breast and Prostate Cancer Cohort Consortium (BPC3). Breast Cancer Res 2006, 8(5):R54.
25. Haiman C.A., Brown M., Hankinson S.E., et al. The androgen receptor CAG repeat polymorphism and risk of breast cancer in the Nurses' Health Study. Cancer Res 2002, 62(4):1045-1049.
26. Giguere Y., Dewailly E., Brisson J., et al. Short polyglutamine tracts in the androgen receptor are protective against breast cancer in the general population. Cancer Res 2001, 61(15):5869-5874.
27. Westberg L., Baghaei F., Rosmond R., et al. Polymorphisms of the androgen receptor gene and the estrogen receptor beta gene are associated with androgen levels in women. J Clin Endocrinol Metab 2001, 86(6):2562-2568.
28. MacLean H.E., Brown R.W., Beilin J., et al. Increased frequency of long androgen receptor CAG repeats in male breast cancers. Breast Cancer Res Treat 2004, 88(3):239-246.
29. Lillie E.O., Bernstein L., Ingles S.A., et al. Polymorphism in the androgen receptor and mammographic density in women taking and not taking estrogen and progestin therapy. Cancer Res 2004, 64(4):1237-1241.
30. Peters A.A., Buchanan G., Ricciardelli C., et al. Androgen receptor inhibits estrogen receptor-alpha activity and is prognostic in breast cancer. Cancer Res 2009, 69(15):6131-6140.
31. Lanzino M., De Amicis F., McPhaul M.J., et al. Endogenous coactivator ARA70 interacts with estrogen receptor alpha (ERalpha) and modulates the functional ERalpha/androgen receptor interplay in MCF-7 cells. J Biol Chem 2005, 280(21):20421-20430.
32. Kandouz M., Lombet A., Perrot J.Y., et al. Proapoptotic effects of antiestrogens, progestins and androgen in breast cancer cells. J Steroid Biochem Mol Biol 1999, 69(1-6):463-471.
33. Nicolas Diaz-Chico B., German Rodriguez F., Gonzalez A., et al. Androgens and androgen receptors in breast cancer. J Steroid Biochem Mol Biol 2007, 105(1-5):1-15.
34. Niemeier L.A., Dabbs D.J., Beriwal S., et al. Androgen receptor in breast cancer: expression in estrogen receptor-positive tumors and in estrogen receptor-negative tumors with apocrine differentiation. Mod Pathol 2010, 23(2):205-212.
35. Ogawa Y., Hai E., Matsumoto K., et al. Androgen receptor expression in breast cancer: relationship with clinicopathological factors and biomarkers. Int J Clin Oncol 2008, 13(5):431-435.
36. Yager J.D., Davidson N.E. Estrogen carcinogenesis in breast cancer. N Engl J Med 2006, 354(3):270-282.
37. Bulbrook R.D., Thomas B.S., Utsunomiya J., et al. The urinary excretion of 11-deoxy-17-oxosteroids and 17-hydroxycorticosteroids by normal Japanese and British women. J Endocrinol 1967, 38(4):401-406.
38. Page J.H., Colditz G.A., Rifai N., et al. Plasma adrenal androgens and risk of breast cancer in premenopausal women. Cancer Epidemiol Biomarkers Prev 2004, 13(6):1032-1036.
39. Eliassen A.H., Missmer S.A., Tworoger S.S., et al. Endogenous steroid hormone concentrations and risk of breast cancer among premenopausal women. J Natl Cancer Inst 2006, 98(19):1406-1415.
40. Dimitrakakis C., Zava D., Marinopoulos S., et al. Low salivary testosterone levels in patients with breast cancer. BMC Cancer 2010, 10:57.
41. Tworoger S.S., Missmer S.A., Eliassen A.H., et al. The association of plasma DHEA and DHEA sulfate with breast cancer risk in predominantly premenopausal women. Cancer Epidemiol Biomarkers Prev 2006, 15(5):967-971.
42. Olson J.E., Ingle J.N., Ma C.X., et al. A comprehensive examination of CYP19 variation and risk of breast cancer using two haplotype-tagging approaches. Breast Cancer Res Treat 2007, 102(2):237-247.
43. Key T., Appleby P., Barnes I., et al. Endogenous sex hormones and breast cancer in postmenopausal women: reanalysis of nine prospective studies. J Natl Cancer Inst 2002, 94(8):606-616.
44. Rosner W., Auchus R.J., Azziz R., et al. Position statement: utility, limitations, and pitfalls in measuring testosterone: an Endocrine Society position statement. J Clin Endocrinol Metab 2007, 92(2):405-413.
45. Schairer C., Hill D., Sturgeon S.R., et al. Serum concentrations of estrogens, sex hormone binding globulin, and androgens and risk of breast hyperplasia in postmenopausal women. Cancer Epidemiol Biomarkers Prev 2005, 14(7):1660-1665.
46. Key T.J., Appleby P.N., Reeves G.K., et al. Body mass index, serum sex hormones, and breast cancer risk in postmenopausal women. J Natl Cancer Inst 2003, 95(16):1218-1226.
47. Schmitt M., Klinga K., Schnarr B., et al. Dehydroepiandrosterone stimulates proliferation and gene expression in MCF-7 cells after conversion to estradiol. Mol Cell Endocrinol 2001, 173(1-2):1-13.
48. Adly L., Hill D., Sherman M.E., et al. Serum concentrations of estrogens, sex hormone-binding globulin, and androgens and risk of breast cancer in postmenopausal women. Int J Cancer 2006, 119(10):2402-2407.
49. Beattie M.S., Costantino J.P., Cummings S.R., et al. Endogenous sex hormones, breast cancer risk, and tamoxifen response: an ancillary study in the NSABP Breast Cancer Prevention Trial (P-1). J Natl Cancer Inst 2006, 98(2):110-115.
50. Gadducci A., Gargini A., Palla E., et al. Polycystic ovary syndrome and gynecological cancers: is there a link?. Gynecol Endocrinol 2005, 20(4):200-208.
51. Swerdlow A.J., Schoemaker M.J., Higgins C.D., et al. Cancer incidence and mortality in men with Klinefelter syndrome: a cohort study. J Natl Cancer Inst 2005, 97(16):1204-1210.
52. Hultborn R., Hanson C., Kopf I., et al. Prevalence of Klinefelter's syndrome in male breast cancer patients. Anticancer Res 1997, 17(6D):4293-4297.
53. Giordano S.H., Buzdar A.U., Hortobagyi G.N. Breast cancer in men. Ann Intern Med 2002, 137(8):678-687.
54. Brinton L.A., Richesson D.A., Gierach G.L., et al. Prospective evaluation of risk factors for male breast cancer. J Natl Cancer Inst 2008, 100(20):1477-1481.
55. Johnson K.C., Pan S., Mao Y. Risk factors for male breast cancer in Canada, 1994-1998. Eur J Cancer Prev 2002, 11(3):253-263.
56. Bulbrook R.D., Thomas B.S. Hormones are ambiguous risk factors for breast cancer. Acta Oncol 1989, 28(6):841-847.
57. Breast cancer and hormonal contraceptives: collaborative reanalysis of individual data on 53 297 women with breast cancer and 100 239 women without breast cancer from 54 epidemiological studies. Collaborative Group on Hormonal Factors in Breast Cancer. Lancet 1996, 347(9017):1713-1727.
58. Marchbanks P.A., McDonald J.A., Wilson H.G., et al. Oral contraceptives and the risk of breast cancer. N Engl J Med 2002, 346(26):2025-2032.
59. Kahlenborn C., Modugno F., Potter D.M., et al. Oral contraceptive use as a risk factor for premenopausal breast cancer: a meta-analysis. Mayo Clin Proc 2006, 81(10):1290-1302.
60. Rossouw J.E., Anderson G.L., Prentice R.L., et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. JAMA 2002, 288(3):321-333.
61. Anderson G.L., Limacher M., Assaf A.R., et al. Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled trial. JAMA 2004, 291(14):1701-1712.
62. Ness R.B., Albano J.D., McTiernan A., et al. Influence of estrogen plus testosterone supplementation on breast cancer. Arch Intern Med 2009, 169(1):41-46.
63. Tamimi R.M., Hankinson S.E., Chen W.Y., et al. Combined estrogen and testosterone use and risk of breast cancer in postmenopausal women. Arch Intern Med 2006, 166(14):1483-1489.
64. Nahleh Z. Androgen receptor as a target for the treatment of hormone receptor-negative breast cancer: an unchartered territory. Future Oncol 2008, 4(1):15-21.
65. Somboonporn W., Davis S.R. Testosterone effects on the breast: implications for testosterone therapy for women. Endocr Rev 2004, 25(3):374-388.
66. Hofling M., Hirschberg A.L., Skoog L., et al. Testosterone inhibits estrogen/progestogen-induced breast cell proliferation in postmenopausal women. Menopause 2007, 14(2):183-190.
67. Conner P. Breast response to menopausal hormone therapy-aspects on proliferation, apoptosis and mammographic density. Ann Med 2007, 39(1):28-41.
68. Dimitrakakis C., Jones R.A., Liu A., et al. Breast cancer incidence in postmenopausal women using testosterone in addition to usual hormone therapy. Menopause 2004, 11(5):531-535.
69. Beral V. Breast cancer and hormone-replacement therapy in the Million Women Study. Lancet 2003, 362(9382):419-427.
70. Pritchard T.J., Pankowsky D.A., Crowe J.P., et al. Breast cancer in a male-to-female transsexual. A case report. JAMA 1988, 259(15):2278-2280.
71. Ganly I., Taylor E.W. Breast cancer in a trans-sexual man receiving hormone replacement therapy. Br J Surg 1995, 82(3):341.
72. Mueller A., Gooren L. Hormone-related tumors in transsexuals receiving treatment with cross-sex hormones. Eur J Endocrinol 2008, 159(3):197-202.