Breast cancer cell apoptosis with phytoestrogens is dependent on an estrogen-deprived state

Cancer Prevention Research

Volumn 7, Issue 9, 2014, Pages 939-949

  Obiorah, Ifeyinwa E ^a   Fan, Ping ^a   Jordan, V Craig ^a  

^a GEORGETOWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AFIMOXIFENE; CASPASE 4; CONJUGATED ESTROGEN; COUMESTROL; DEXAMETHASONE; EQUILIN; EQUOL; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FULVESTRANT; GENISTEIN; INITIATION FACTOR 2ALPHA; LYMPHOTOXIN BETA; MESSENGER RNA; PROTEIN IRE1; SMALL INTERFERING RNA; ESTROGEN; PHYTOESTROGEN;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER INHIBITION; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ESTROGEN ACTIVITY; ESTROGEN DEFICIENCY; INFLAMMATION; MCF 7 CELL LINE; POSTMENOPAUSE; BREAST TUMOR; DRUG EFFECTS; GENETIC TRANSFECTION; HUMAN; IMMUNOBLOTTING; IN VITRO STUDY; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION;

APOPTOSIS; BREAST NEOPLASMS; ESTROGENS; HUMANS; IMMUNOBLOTTING; IN VITRO TECHNIQUES; MCF-7 CELLS; PHYTOESTROGENS; POSTMENOPAUSE; REAL-TIME POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 84907297504     PISSN: 19406207     EISSN: 19406215     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-14-0061     Document Type: Article

References (57)

1. Gottardis MM, Jordan VC. Development of tamoxifen-stimulated growth of MCF-7 Tumors in athymic mice after long-term antiestrogen administration. Cancer Res 1988;48:5183-7.
2. Osborne CK, Coronado EB, Robinson J. Human breast cancer in the athymic nude mouse: cytostatic effects of long-term antiestrogen therapy. Eur J Cancer Clin Oncol 1987;23:1189-96.
3. Yao K, Lee E, Bentrem D, England G, Schafer J, O'Regan R, et al. Antitumor action of physiological estradiol on tamoxifen-stimulated breast tumors grown in athymic mice. Clin Cancer Res 2000;6: 2028-36.
4. Lewis JS, Meeke K, Osipo C, Ross EA, Kidawi N, Li T, et al. Intrinsic mechanism of estradiol-induced apoptosis in breast cancer cells resistant to estrogen deprivation. J Natl Cancer Inst 2005;97: 1746-59.
5. Lewis JS, Osipo C, Meeke K, Jordan VC. Estrogen-induced apoptosis in a breast cancer model resistant to long-term estrogen withdrawal. J Steroid Biochem Mol Biol 2005;94:131-41.
6. Lønning P, Taylor P, Anker G, Iddon J, Wie L. High-dose estrogen treatment in postmenopausal breast cancer patients heavily exposed to endocrine therapy. Breast Cancer Res Treat 2001;67:111-6.
7. Ellis M, Gao F, Dehdashti F, Jeffe D, Marcom P, Carey L, et al. Lowerdose vs. high-dose oral estradiol therapy of hormone receptor-positive, aromatase inhibitor-resistant advanced breast cancer: a phase 2 randomized study. JAMA 2009;302:774-80.
8. Anderson GL, Limacher M, Assaf AR, Bassford T, Beresford SA, Black H, et al. Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled trial. JAMA 2004;291:1701-12.
9. Anderson G, Chlebowski R, Aragaki A, Kuller L, Manson J, Gass M, et al. Conjugated equine oestrogen and breast cancer incidence and mortality in postmenopausal women with hysterectomy: extended follow-up of the Women's Health Initiative randomised placebo-controlled trial. Lancet Oncol 2012;13:476-86.
10. Obiorah I, Jordan VC. 2012 NAMS/PFIZER-Wulf H. utian endowed lecture. The scientific rationale for a delay after menopause in the use of conjugated equine estrogens in postmenopausalwomenthat causes a reduction in breast cancer incidence and mortality. Menopause 2013;20:372-82.
11. Wu AH, Yu MC, Tseng CC, Pike MC. Epidemiology of soy exposures and breast cancer risk. Br J Cancer 2008;98:9-14.
12. Nagata C, Mizoue T, Tanaka K, Tsuji I, Tamakoshi A, Matsuo K, et al. Soy intake and breast cancer risk: an evaluation based on a systematic review of epidemiologic evidence among the Japanese population. Jpn J Clin Oncol 2014;44:282-95.
13. Chen M, Rao Y, Zheng Y, Wei S, Li Y, Guo T, et al. Association between soy isoflavone intake and breast cancer risk for pre-and post-menopausal women: a meta-analysis of epidemiological studies. PLoS ONE 2014;9:e89288.
14. Trock BJ, Hilakivi-Clarke L, Clarke R. Meta-analysis of soy intake and breast cancer risk. J Natl Cancer Inst 2006;98:459-71.
15. Lee SA, Shu XO, Li H, Yang G, Cai H, Wen W, et al. Adolescent and adult soy food intake and breast cancer risk: results from the Shanghai Women's Health Study. Am J Clin Nutr 2009;89:1920-6.
16. Thanos J, Cotterchio M, Boucher BA, Kreiger N, Thompson LU. Adolescent dietary phytoestrogen intake and breast cancer risk (Canada). Cancer Causes Control 2006;17:1253-61.
17. Wu AH, Wan P, Hankin J, Tseng CC, Yu MC, Pike MC. Adolescent and adult soy intake and risk of breast cancer in Asian-Americans. Carcinogenesis 2002;23:1491-6.
18. Whitsett TG Jr, Lamartiniere CA. Genistein and resveratrol: mammary cancer chemoprevention and mechanisms of action in the rat. Expert Rev Anticancer Ther 2006;6:1699-706.
19. Murrill WB, Brown NM, Zhang JX, Manzolillo PA, Barnes S, Lamartiniere CA. Prepubertal genistein exposure suppresses mammary cancer and enhances gland differentiation in rats. Carcinogenesis 1996;17:1451-7.
20. Hsieh C-Y, Santell RC, Haslam SZ, Helferich WG. Estrogenic effects of genistein on the growth of estrogen receptor-positive human breast cancer (MCF-7) cells in vitro and in vivo. Cancer Res 1998;58:3833-8.
21. Le Bail J-C, Champavier Y, Chulia A-J, Habrioux G. Effects of phytoestrogens on aromatase, 3b and 17b-hydroxysteroid dehydrogenase activities and human breast cancer cells. Life Sci 2000;66: 1281-91.
22. Zava DT, Duwe G. Estrogenic and antiproliferative properties of genistein and other flavonoids in human breast cancer cells in vitro. Nutr Cancer 1997;27:31-40.
23. Pagliacci MC, Smacchia M, Migliorati G, Grignani F, Riccardi C, Nicoletti I. Growth-inhibitory effects of the natural phyto-oestrogen genistein in MCF-7 human breast cancer cells. Eur J Cancer 1994;30:1675-82.
24. Shao ZM, Shen ZZ, Fontana JA, Barsky SH. Genistein's "ER-dependent and independent" actions are mediated through ER pathways in ER-positive breast carcinoma cell lines. Anticancer Res 2000; 20:2409-16.
25. McMichael-Phillips DF, Harding C, Morton M, Roberts SA, Howell A, Potten CS, et al. Effects of soy-protein supplementation on epithelial proliferation in the histologically normal human breast. Am J Clin Nutr 1998;68:1431S-5S.
26. Petrakis NL, Barnes S, King EB, Lowenstein J, Wiencke J, Lee MM, et al. Stimulatory influence of soy protein isolate on breast secretion in pre-and postmenopausal women. Cancer Epidemiol Bio Prev 1996;5:785-94.
27. Hargreaves DF, Potten CS, Harding C, Shaw LE, Morton MS, Roberts SA, et al. Two-week dietary soy supplementation has an estrogenic effect on normal premenopausal breast. J Clin Endocrinol Metabol 1999;84:4017-24.
28. Thompson LU, Chen JM, Li T, Strasser-Weippl K, Goss PE. Dietary flaxseed alters tumor biological markers in postmenopausal breast cancer. Clin Cancer Res 2005;11:3828-35.
29. Sartippour MR, Rao JY, Apple S, Wu D, Henning S, Wang H, et al. A pilot clinical study of short-term isoflavone supplements in breast cancer patients. Nutr Cancer 2004;49:59-65.
30. Palomares MR, Hopper L, Goldstein L, Lehman CD, Storer BE, Gralow JR. Effect of soy isoflavones on breast proliferation in postmenopausal breast cancer survivors. Breast Cancer Res Treat 2004;88:4002.
31. Cheng G, Wilczek B, Warner M, Gustafsson J, Landgren B. Isoflavone treatment for acute menopausal symptoms. Menopause 2007; 14:468-73.
32. Fink BN, Steck SE, Wolff MS, Britton JA, Kabat GC, Gaudet MM, et al. Dietary flavonoid intake and breast cancer survival among women on Long Island. Cancer Epidemiol Biomarkers Prev 2007;16:2285-92.
33. Swann R, Perkins KA, Velentzis LS, Ciria C, Dutton SJ, Mulligan AA, et al. The DietCompLyf study: a prospective cohort study of breast cancer survival and phytoestrogen consumption. Maturitas 2013; 75:232-40.
34. Shu XO, Zheng Y, Cai H, Gu K, Chen Z, Zheng W, et al. Soy food intake and breast cancer survival. JAMA 2009;302:2437-43.
35. Jiang SY, Wolf DM, Yingling JM, Chang C, Jordan VC. An estrogen receptor-positive MCF-7 clone that is resistant to antiestrogens and estradiol. Mol Cell Endocrinol 1992;90:77-86.
36. Ariazi E, Cunliffe H, Lewis-Wambi JS, Slifker M, Willis A, Ramos P, et al. Estrogen induces apoptosis in estrogen deprivation-resistant breast cancer through stress responses as identified by global gene expression across time. Proc Natl Acad Sci U S A 2011;108:18879-86.
37. Fan P, Agboke FA, McDaniel RE, Sweeney EE, Zou X, Creswell K, et al. Inhibition of c-Src blocks oestrogen-induced apoptosis and restores oestrogen-stimulated growth in long-term oestrogen-deprived breast cancer cells. Eur J Cancer 2014;50:457-68.
38. Sengupta S, Sharma C, Jordan VC. Estrogen regulation of X-box binding protein-1 and its role in estrogen induced growth of breast and endometrial cancer cells. Horm Mol Biol Clin Investig 2010;2: 235-43.
39. Traganos F, Ardelt B, Halko N, Bruno S, Darzynkiewicz Z. Effects of genistein on the growth and cell cycle progression of normal human lymphocytes and human leukemic MOLT-4 and HL-60 cells. Cancer Res 1992;52:6200-8.
40. Sakamoto T, Horiguchi H, Oguma E, Kayama F. Effects of diverse dietary phytoestrogens on cell growth, cell cycle and apoptosis in estrogen receptor-positive breast cancer cells. J Nutr Biochem 2010;21:856-64.
41. Fritz WA, Coward L, Wang J, Lamartiniere CA. Dietary genistein: perinatal mammary cancer prevention, bioavailability and toxicity testing in the rat. Carcinogenesis 1998;19:2151-8.
42. Lamartiniere CA, Wang J, Smith-Johnson M, Eltoum IE. Daidzein: bioavailability, potential for reproductive toxicity, and breast cancer chemoprevention in female rats. Toxicol Sci 2002;65:228-38.
43. Andrade JE, Ju YH, Baker C, Doerge DR, Helferich WG. Long-term exposure to dietary sources of genistein induces estrogen-independence in the human breast cancer (MCF-7) xenograft model. Mol Nutr Food Res 2014;24:201300780.
44. Peterson G, Barnes S. Genistein inhibits both estrogen and growth factor-stimulated proliferation of human breast cancer cells. Cell Growth Differ 1996;7:1345-51.
45. Peterson G. Evaluation of the biochemical targets of genistein in tumor cells. J Nutr 1995;125:784S-9S.
46. Diel P, Geis R-B, Caldarelli A, Schmidt S, Leschowsky UL, Voss A, et al. The differential ability of the phytoestrogen genistein and of estradiol to induce uterine weight and proliferation in the rat is associated with a substance specific modulation of uterine gene expression. Mol Cell Endocrinol 2004;221:21-32.
47. Kostelac D, Rechkemmer G, Briviba K. Phytoestrogens modulate binding response of estrogen receptors alpha and beta to the estrogen response element. J Agric Food Chem 2003;51:7632-5.
48. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 2000;5:897-904.
49. Fan P, Griffith OL, Agboke F, Anur P, Zou X, McDaniel RE, et al. c-Src modulates estrogen-induced stress and apoptosis in estrogendeprived breast cancer cells. Cancer Res 2013;73:4510-20.
50. Verfaillie T, Rubio N, Garg AD, Bultynck G, Rizzuto R, Decuypere JP, et al. PERK is required at the ER-mitochondrial contact sites to convey apoptosis after ROS-based ER stress. Cell Death Differ 2012;19: 1880-91.
51. Ron D, Habener JF. CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes Dev 1992;6:439-53.
52. Styner M, Meyer MB, Galior K, Case N, Xie Z, Sen B, et al. Mechanical strain downregulates C/EBPbeta in MSC and decreases endoplasmic reticulum stress. PLoS ONE 2012;7:12.
53. Haddow A, Watkinson JM, Patterson E. Influence of synthetic oestrogens upon advanced malignant disease. BMJ 1944;2:393-8.
54. Haddow A, David A. Karnosky memorial lecture: thoughts on chemical therapy. Cancer Res 1970;26:737-54.
55. Stoll B. Palliation by castration or by hormone administration. InStoll B, ed. Breast cancer management early and late. London, UK: William Herman Medical Books Ltd; 1977;133-146.
56. Davies C, Pan H, Godwin J, Gray R, Arriagada R, Raina V, et al. Longterm effects of continuing adjuvant tamoxifen to 10 years versus stopping at 5 years after diagnosis of oestrogen receptor-positive breast cancer: ATLAS, a randomised trial. Lancet 2013;381:805-16.
57. Wolf DM, Jordan VC. A laboratory model to explain the survival advantage observed in patients taking adjuvant tamoxifen therapy. Recent Results Cancer Res 1993;127:23-33.