Research progress on the relationship between estrogen metabolism and breast cancer_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

FANG Ling , YANG Xiaoqin ,  LI Hongjiang

Department of Breast Surgery, West China Hospital, Sichuan University, Chengdu 610041, R. P. China;

Corresponding author：

LI Hongjiang, Email: lihongjiang@sohu.com

Keywords：

estrogen; breast cancer; review

DOI：

10.7507/1007-9424.201909102

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To investigate the relationship between female estrogen metabolism and breast cancer.Method By searching the contents of Chinese Knowledge Network, Wanfang Database, PubMed and other databases, the relationship between breast cancer hormone receptor status, menstrual status and estrogen metabolism and breast cancer, estrogen metabolism pathway and signal in vivo a review of the transduction aspects.Results Estrogen and its metabolites was closely related to the occurrence and development of breast cancer. Among the main metabolic pathways of estrogen, 2-methoxyestradiol in the 2-hydroxy metabolic pathway had a potential protective effect on breast cancer; 4-hydroxyestradiol, 16α-hydroxyestrone might induce breast cancer; the ratio of 4-hydroxyestradiol to 2-hydroxyestradiol might be used as a biomarker for predicting malignant breast tumors. However, the estrogen metabolism patterns before and after menopause were different, and the effects on hormone receptor status were also different. Different hormone receptor status might affect the treatment and prognosis of breast cancer.Conclusions The relationship between estrogen and its metabolites and breast cancer in different receptor states is not completely clear. More large-scale prospective studies are needed to help us find out the rules to promote early diagnosis and early prevention of breast cancer.

Citation： FANG Ling, YANG Xiaoqin, LI Hongjiang. Research progress on the relationship between estrogen metabolism and breast cancer. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2020, 27(3): 374-378. doi: 10.7507/1007-9424.201909102 Copy

1.	Momenimovahed Z, Salehiniya H. Epidemiological characteristics of and risk factors for breast cancer in the world. Breast Cancer, 2019, 11: 151-164.
2.	Gu X, Zheng R, Xia C, et al. 中国预期寿命与癌症发病率和死亡率的相互影响: 基于人群的聚类分析. 癌症, 2019, 38(1): 23-38.
3.	李贺, 郑荣寿, 张思维, 等. 2014年中国女性乳腺癌发病与死亡分析. 中华肿瘤杂志, 2018, 40(3): 166-171.
4.	Ziegler RG, Faupel-Badger JM, Sue LY, et al. A new approach to measuring estrogen exposure and metabolism in epidemiologic studies. J Steroid Biochem Mol Biol, 2010, 121(3-5): 538-545.
5.	You J, Shi Y, Li JQ, et al. Rapid quantification of human urinary estrogens and estrogen metabolites by HPLC mass spectrometry. Microchem J, 2019, 147: 157-162.
6.	孙向洁, 杨文涛. 免疫组织化学在乳腺癌分子分型中的作用及目前存在的问题. 中国癌症杂志, 2019, 29(3): 161-165.
7.	高纪东, 王靖, 冯晓丽, 等. 5758例女性乳腺癌激素受体状态及其相关因素分析. 中华肿瘤杂志, 2009, 31(9): 683-686.
8.	Perou CM, Sørlie T, Eisen MB, et al. Molecular portraits of human breast tumours. Nature, 2000, 406(6797): 747-752.
9.	Need EF, Atashgaran V, Ingman WV, et al. Hormonal regulation of the immune microenvironment in the mammary gland. J Mammary Gland Biol Neoplasia, 2014, 19(2): 229-239.
10.	Cantini L, Pistelli M, Merloni, et al. Body mass index and hormone receptor status influence recurrence risk in HER2-positive early breast cancer patients. Clin Breast Cancer, 2019 Jul 11.[Epub ahead of print].
11.	Visvanathan K, Fabian CJ, Bantug E, et al. Use of endocrine therapy for breast cancer risk reduction: ASCO clinical practice guideline update. J Clin Oncol, 2019, 37(33): 3152-3165.
12.	Sinpson ER. Sources of estrogen and their importance. J Steroid Biochem Mol Biol, 2003, 86(3-5): 225-230.
13.	程泽能, 周宏灏. 雌激素的代谢机制及其与疾病的相关性. 中国临床药理学杂志, 2000, 16(4): 304-308.
14.	Samavat H, Kurzer MS. Estrogen metabolism and breast cancer. Cancer Letters, 2015, 356(2, Part A): 231-243.
15.	Ziegler RG, Fuhrman BJ, Moore SC, et al. Epidemiologic studies of estrogen metabolism and breast cancer. Steroids, 2015, 99(Pt A): 67-75.
16.	Wen CJ, Wu LX, Fu LJ, et al. Preferential induction of CYP1A1 over CYP1B1 in human breast cancer MCF-7 cells after exposure to berberine. Asian Pac J Cancer Prev, 2014, 15(1): 495-499.
17.	Wang S, Dunlap TL, Howell CE, et al. Hop (Humulus lupulus L.) extract and 6-prenylnaringenin induce P450 1A1 catalyzed estrogen 2-hydroxylation. Chem Res Toxicol, 2016, 29(7): 1142-1150.
18.	Ruan X, Seeger H, Wallwiener D, et al. The ratio of the estradiol metabolites 2-hydroxyestrone (2-OHE1) and 16α-hydroxyestrone (16-OHE1) may predict breast cancer risk in postmenopausal but not in premenopausal women: two case–control studies. Arch Gynecol Obstet, 2015, 291(5): 1141-1146.
19.	Choi HJ, Zhu BT. Critical role of cyclin B1/Cdc2 up-regulation in the induction of mitotic prometaphase arrest in human breast cancer cells treated with 2-methoxyestradiol. Biochim Biophys Acta, 2012, 1823(8): 1306-1315.
20.	Zou X, Zhang L, Yuan J, et al. Endogenous hormone 2-methoxyestradiol suppresses venous hypertension-induced angiogenesis through up- and down-regulating p53 and id-1. J Cell Mol Med, 2018, 22(2): 957-967.
21.	Tan J, Le A. Breast cancer metabolism. Adv Exp Med Biol, 2018, 1063: 83-93.
22.	Gupta M, Mcdougal A, Safe S. Estrogenic and antiestrogenic activities of 16α- and 2-hydroxy metabolites of 17β-estradiol in MCF-7 and T47D human breast cancer cells. J Steroid Biochem Mol Biol, 1998, 67(5): 413-419.
23.	Suto A, Telang NT, Tanino H, et al. In vitro and in vivo modulation of growth regulation in the human breast cancer cell line MCF-7 by estradiol metabolites. Breast Cancer, 1999, 6(2): 87-92.
24.	Yager JD. Mechanisms of estrogen carcinogenesis: the role of E2/E1- quinone metabolites suggests new approaches to preventive intervention – a review. Steroids, 2015, 99: 56-60.
25.	Moore SC, Matthews CE, Ou Shu X, et al. Endogenous estrogens, estrogen metabolites, and breast cancer risk in postmenopausal chinese women. J Natl Cancer Inst, 2016, 108(10): djw103.
26.	Arslan AA, Koenig KL, Lenner P, et al. Circulating estrogen metabolites and risk of breast cancer in postmenopausal women. Cancer Epidemiol Biomarkers Prev, 2014, 23(7): 1290-1297.
27.	Sood D, Johnson N, Jain P, et al. CYP3A7*1C allele is associated with reduced levels of 2-hydroxylation pathway oestrogen metabolites. Br J Cancer, 2017, 116(3): 382-388.
28.	Niwa T, Murayama N, Imagawa Y, et al. Regioselective hydroxylation of steroid hormones by human cytochromes P450. Drug Metab Rev, 2015, 47(2): 89-110.
29.	Cavalieri EL, Rogan EG. Unbalanced metabolism of endogenous estrogens in the etiology and prevention of human cancer. J Steroid Biochem Mol Biol, 2011, 125(3-5): 169-180.
30.	Liehr JG, Ricci MJ. 4-Hydroxylation of estrogens as marker of human mammary tumors. Proc Natl Acad Sci U S A, 1996, 93(8): 3294-3296.
31.	Bradlow HL, Hershcopf R, Martuuci C, et al. 16 alpha-hydroxylation of estradiol: a possible risk marker for breast cancer. Ann N Y Acad Sci, 1986, 464: 138-151.
32.	Kim SH, Lee SU, Kim MH, et al. Mitogenic estrogen metabolites alter the expression of 17 beta-estradiol-regulated proteins including heat shock proteins in human MCF-7 breast cancer cells. Mol Cells, 2005, 20(3): 378-384.
33.	Osborne MP, Bradlow HL, Wong YC, et al. Upregulation of estradiol C16α-hydroxylation in human breast tissue: a potential biomarker of breast cancer risk. J Natl Cancer Inst, 1993, 85(23): 1917-1920.
34.	王俊玲, 黄思敏, 梁启瑶, 等. 雌激素的来源及其在骨代谢中的作用. 中国骨质疏松杂志, 2015, 21(6): 729-732.
35.	Hall JE. Endocrinology of the menopause. Endocrinol Metab Clin North Am, 2015, 44(3): 485-496.
36.	Goedecke JH, Tootla M, Keswell D. Ethnic differences in regional adipose tissue oestrogen receptor gene expression. Endocr Connect, 2019, 8(1): 32-38.
37.	Savolainen H, Vihma V, Wang F, et al. Estrogen biosynthesis in breast adipose tissue during menstrual cycle in women with and without breast cancer. Gynecol Endocrinol, 2018, 34(12): 1039-1043.
38.	Brown KA, Iyengar NM, Zhou XK, et al. Menopause is a determinant of breast aromatase expression and its associations with BMI, inflammation, and systemic markers. J Clin Endocrinol Metab, 2017, 102(5): 1692-1701.
39.	Premenopausal Breast Cancer Collaborative Group, Schoemaker MJ, Nichols HB, et al. Association of body mass index and age with subsequent breast cancer risk in premenopausal women. JAMA Oncol, 2018, 4(11): e181771.
40.	Engin A. Obesity-associated breast cancer: analysis of risk factors. Adv Exp Med Biol, 2017, 960: 571-606.
41.	谢梅青, 陈蓉, 任慕兰. 中国绝经管理与绝经激素治疗指南(2018). 协和医学杂志, 2018, 9(6): 512-525.
42.	Purohit A, Reed MJ. Regulation of estrogen synthesis in postmenopausal women. Steroids, 2002, 67(12): 979-983.
43.	Dehal SS, Brodie AM, Kupfer D. The aromatase inactivator 4-hydroxyandrostenedione (4-OH-A) inhibits tamoxifen metabolism by rat hepatic cytochrome P-450 3A: potential for drug-drug interaction of tamoxifen and 4-OH-A in combined anti-breast cancer therapy. Drug Metab Dispos, 1999, 27(3): 389-394.
44.	Avvaru SP, Noolvi MN, Aminbhavi TM, et al. Aromatase inhibitors evolution as potential class of drugs in the treatment of postmenopausal breast cancer women. Mini Rev Med Chem, 2018, 18(7): 609-621.
45.	Rossouw JE, Anderson GL, Prentice RL, 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.
46.	D'Alonzo M, Bounous VE, Villa M, et al. Current evidence of the oncological benefit-risk profile of hormone replacement therapy. Medicina (Kaunas), 2019, 55(9): pii: E573.
47.	Li CI, Daling JR, Malone KE. Incidence of invasive breast cancer by hormone receptor status from 1992 to 1998. J Clin Oncol, 2003, 21(1): 28-34.
48.	Hartley MC, Mckinley BP, Rogers EA, et al. Differential expression of prognostic factors and effect on survival in young (≤40) breast cancer patients: a case-control study. Am Surg, 2006, 72(12): 1189-1194.
49.	Eric I, Petek A, Kristek J, et al. Breast cancer in young women:pathologic and immunohistochemical features. Acta Clin Croat, 2018, 57(3): 497-502.
50.	Cui Y, Deming SL, Shrubsole MJ, et al. Associations of hormone-related factors with breast cancer risk according to hormone receptor status among white and African American women. Clin Breast Cancer, 2014, 14(6): 417-425.
51.	Tarone RE, Chu KC. The greater impact of menopause on ER- than ER+ breast cancer incidence: a possible explanation (United States). Cancer Causes Control, 2002, 13(1): 7-14.
52.	Chung IY, Lee JW, Lee JS, et al. Interaction between body mass index and hormone-receptor status as a prognostic factor in lymph-node-positive breast cancer. PloS One, 2017, 12(3): e0170311.
53.	Dunlap TL, Howell CE, Mukand N, et al. Red clover aryl hydrocarbon receptor (AhR) and estrogen receptor (ER) agonists enhance genotoxic estrogen metabolism. Chem Res Toxicol, 2017, 30(11): 2084-2092.
54.	Paterni I, Granchi C, Katzenellenbogen JA, et al. Estrogen receptors alpha (ERα) and beta (ERβ): subtype-selective ligands and clinical potential. Steroids, 2014, 90: 13-29.
55.	Heldring N, Pike A, Andersson S, et al. Estrogen receptors: how do they signal and what are their targets. Physiol Rev, 2007, 87(3): 905-931.
56.	Willams C, Lin CY. Estrogen receptors in breast cancer: basic mechanisms and clinical implications. Ecancermedicalscience, 2013, 7: 370.
57.	Giudice A, Barbieri A, BimonteI S, et al. Dissecting the prevention of estrogen-dependent breast carcinogenesis through Nrf2-dependent and independent mechanisms. Onco Targets Ther, 2019, 12: 4937-4953.
58.	Kulkoyluoglu E, Arac A, Madak Z. Crosstalk between estrogen signaling and breast cancer metabolism. Trends in Endocrinol Metab, 2019, 30(1): 25-38.
59.	Loboda A, Nebozhyn M, Klinghoffer R, et al. A gene expression signature of RAS pathway dependence predicts response to PI3K and RAS pathway inhibitors and expands the population of RAS pathway activated tumors. BMC Med Genomics, 2010, 3: 26.
60.	Dey N, De P, Leylang B. PI3K-AKT-mTOR inhibitors in breast cancers: from tumor cell signaling to clinical trials. Pharmacol Ther, 2017, 175: 91-106.
61.	Yndestad S, Austreid E, Svanberg IR, et al. Activation of Akt characterizes estrogen receptor positive human breast cancers which respond to anthracyclines. Oncotarget, 2017, 8(25): 41227-41241.
62.	Hayes MJ, Thomas D, Emmons A, et al. Genetic changes of Wnt pathway genes are common events in metaplastic carcinomas of the breast. Clin Cancer Res, 2008, 14(13): 4038-4044.
63.	Bado I, Nikolos F, Rajapaksa G, et al. Somatic loss of estrogen receptor beta and p53 synergize to induce breast tumorigenesis. Breast Cancer Res, 2017, 19(1): 79.
64.	Lu W, Katzenellenbogen BS. Estrogen receptor-β modulation of the ERα-p53 Loop regulating gene expression, proliferation, and apoptosis in breast cancer. Horm Cancer, 2017, 8(4): 230-242.
65.	Yang J, Altahan A, Jones DT, et al. Estrogen receptor-α directly regulates the hypoxia-inducible factor 1 pathway associated with antiestrogen response in breast cancer. Proc Natl Acad Sci U S A, 2015, 112(49): 15172-15177.
66.	Huang B, Omoto Y, Iwase H, et al. Differential expression of estrogen receptor α, β1, and β2 in lobular and ductal breast cancer. Proc Natl Acad Sci U S A, 2014, 111(5): 1933-1938.

1. Momenimovahed Z, Salehiniya H. Epidemiological characteristics of and risk factors for breast cancer in the world. Breast Cancer, 2019, 11: 151-164.
2. Gu X, Zheng R, Xia C, et al. 中国预期寿命与癌症发病率和死亡率的相互影响: 基于人群的聚类分析. 癌症, 2019, 38(1): 23-38.
3. 李贺, 郑荣寿, 张思维, 等. 2014年中国女性乳腺癌发病与死亡分析. 中华肿瘤杂志, 2018, 40(3): 166-171.
4. Ziegler RG, Faupel-Badger JM, Sue LY, et al. A new approach to measuring estrogen exposure and metabolism in epidemiologic studies. J Steroid Biochem Mol Biol, 2010, 121(3-5): 538-545.
5. You J, Shi Y, Li JQ, et al. Rapid quantification of human urinary estrogens and estrogen metabolites by HPLC mass spectrometry. Microchem J, 2019, 147: 157-162.
6. 孙向洁, 杨文涛. 免疫组织化学在乳腺癌分子分型中的作用及目前存在的问题. 中国癌症杂志, 2019, 29(3): 161-165.
7. 高纪东, 王靖, 冯晓丽, 等. 5758例女性乳腺癌激素受体状态及其相关因素分析. 中华肿瘤杂志, 2009, 31(9): 683-686.
8. Perou CM, Sørlie T, Eisen MB, et al. Molecular portraits of human breast tumours. Nature, 2000, 406(6797): 747-752.
9. Need EF, Atashgaran V, Ingman WV, et al. Hormonal regulation of the immune microenvironment in the mammary gland. J Mammary Gland Biol Neoplasia, 2014, 19(2): 229-239.
10. Cantini L, Pistelli M, Merloni, et al. Body mass index and hormone receptor status influence recurrence risk in HER2-positive early breast cancer patients. Clin Breast Cancer, 2019 Jul 11.[Epub ahead of print].
11. Visvanathan K, Fabian CJ, Bantug E, et al. Use of endocrine therapy for breast cancer risk reduction: ASCO clinical practice guideline update. J Clin Oncol, 2019, 37(33): 3152-3165.
12. Sinpson ER. Sources of estrogen and their importance. J Steroid Biochem Mol Biol, 2003, 86(3-5): 225-230.
13. 程泽能, 周宏灏. 雌激素的代谢机制及其与疾病的相关性. 中国临床药理学杂志, 2000, 16(4): 304-308.
14. Samavat H, Kurzer MS. Estrogen metabolism and breast cancer. Cancer Letters, 2015, 356(2, Part A): 231-243.
15. Ziegler RG, Fuhrman BJ, Moore SC, et al. Epidemiologic studies of estrogen metabolism and breast cancer. Steroids, 2015, 99(Pt A): 67-75.
16. Wen CJ, Wu LX, Fu LJ, et al. Preferential induction of CYP1A1 over CYP1B1 in human breast cancer MCF-7 cells after exposure to berberine. Asian Pac J Cancer Prev, 2014, 15(1): 495-499.
17. Wang S, Dunlap TL, Howell CE, et al. Hop (Humulus lupulus L.) extract and 6-prenylnaringenin induce P450 1A1 catalyzed estrogen 2-hydroxylation. Chem Res Toxicol, 2016, 29(7): 1142-1150.
18. Ruan X, Seeger H, Wallwiener D, et al. The ratio of the estradiol metabolites 2-hydroxyestrone (2-OHE1) and 16α-hydroxyestrone (16-OHE1) may predict breast cancer risk in postmenopausal but not in premenopausal women: two case–control studies. Arch Gynecol Obstet, 2015, 291(5): 1141-1146.
19. Choi HJ, Zhu BT. Critical role of cyclin B1/Cdc2 up-regulation in the induction of mitotic prometaphase arrest in human breast cancer cells treated with 2-methoxyestradiol. Biochim Biophys Acta, 2012, 1823(8): 1306-1315.
20. Zou X, Zhang L, Yuan J, et al. Endogenous hormone 2-methoxyestradiol suppresses venous hypertension-induced angiogenesis through up- and down-regulating p53 and id-1. J Cell Mol Med, 2018, 22(2): 957-967.
21. Tan J, Le A. Breast cancer metabolism. Adv Exp Med Biol, 2018, 1063: 83-93.
22. Gupta M, Mcdougal A, Safe S. Estrogenic and antiestrogenic activities of 16α- and 2-hydroxy metabolites of 17β-estradiol in MCF-7 and T47D human breast cancer cells. J Steroid Biochem Mol Biol, 1998, 67(5): 413-419.
23. Suto A, Telang NT, Tanino H, et al. In vitro and in vivo modulation of growth regulation in the human breast cancer cell line MCF-7 by estradiol metabolites. Breast Cancer, 1999, 6(2): 87-92.
24. Yager JD. Mechanisms of estrogen carcinogenesis: the role of E2/E1- quinone metabolites suggests new approaches to preventive intervention – a review. Steroids, 2015, 99: 56-60.
25. Moore SC, Matthews CE, Ou Shu X, et al. Endogenous estrogens, estrogen metabolites, and breast cancer risk in postmenopausal chinese women. J Natl Cancer Inst, 2016, 108(10): djw103.
26. Arslan AA, Koenig KL, Lenner P, et al. Circulating estrogen metabolites and risk of breast cancer in postmenopausal women. Cancer Epidemiol Biomarkers Prev, 2014, 23(7): 1290-1297.
27. Sood D, Johnson N, Jain P, et al. CYP3A7*1C allele is associated with reduced levels of 2-hydroxylation pathway oestrogen metabolites. Br J Cancer, 2017, 116(3): 382-388.
28. Niwa T, Murayama N, Imagawa Y, et al. Regioselective hydroxylation of steroid hormones by human cytochromes P450. Drug Metab Rev, 2015, 47(2): 89-110.
29. Cavalieri EL, Rogan EG. Unbalanced metabolism of endogenous estrogens in the etiology and prevention of human cancer. J Steroid Biochem Mol Biol, 2011, 125(3-5): 169-180.
30. Liehr JG, Ricci MJ. 4-Hydroxylation of estrogens as marker of human mammary tumors. Proc Natl Acad Sci U S A, 1996, 93(8): 3294-3296.
31. Bradlow HL, Hershcopf R, Martuuci C, et al. 16 alpha-hydroxylation of estradiol: a possible risk marker for breast cancer. Ann N Y Acad Sci, 1986, 464: 138-151.
32. Kim SH, Lee SU, Kim MH, et al. Mitogenic estrogen metabolites alter the expression of 17 beta-estradiol-regulated proteins including heat shock proteins in human MCF-7 breast cancer cells. Mol Cells, 2005, 20(3): 378-384.
33. Osborne MP, Bradlow HL, Wong YC, et al. Upregulation of estradiol C16α-hydroxylation in human breast tissue: a potential biomarker of breast cancer risk. J Natl Cancer Inst, 1993, 85(23): 1917-1920.
34. 王俊玲, 黄思敏, 梁启瑶, 等. 雌激素的来源及其在骨代谢中的作用. 中国骨质疏松杂志, 2015, 21(6): 729-732.
35. Hall JE. Endocrinology of the menopause. Endocrinol Metab Clin North Am, 2015, 44(3): 485-496.
36. Goedecke JH, Tootla M, Keswell D. Ethnic differences in regional adipose tissue oestrogen receptor gene expression. Endocr Connect, 2019, 8(1): 32-38.
37. Savolainen H, Vihma V, Wang F, et al. Estrogen biosynthesis in breast adipose tissue during menstrual cycle in women with and without breast cancer. Gynecol Endocrinol, 2018, 34(12): 1039-1043.
38. Brown KA, Iyengar NM, Zhou XK, et al. Menopause is a determinant of breast aromatase expression and its associations with BMI, inflammation, and systemic markers. J Clin Endocrinol Metab, 2017, 102(5): 1692-1701.
39. Premenopausal Breast Cancer Collaborative Group, Schoemaker MJ, Nichols HB, et al. Association of body mass index and age with subsequent breast cancer risk in premenopausal women. JAMA Oncol, 2018, 4(11): e181771.
40. Engin A. Obesity-associated breast cancer: analysis of risk factors. Adv Exp Med Biol, 2017, 960: 571-606.
41. 谢梅青, 陈蓉, 任慕兰. 中国绝经管理与绝经激素治疗指南(2018). 协和医学杂志, 2018, 9(6): 512-525.
42. Purohit A, Reed MJ. Regulation of estrogen synthesis in postmenopausal women. Steroids, 2002, 67(12): 979-983.
43. Dehal SS, Brodie AM, Kupfer D. The aromatase inactivator 4-hydroxyandrostenedione (4-OH-A) inhibits tamoxifen metabolism by rat hepatic cytochrome P-450 3A: potential for drug-drug interaction of tamoxifen and 4-OH-A in combined anti-breast cancer therapy. Drug Metab Dispos, 1999, 27(3): 389-394.
44. Avvaru SP, Noolvi MN, Aminbhavi TM, et al. Aromatase inhibitors evolution as potential class of drugs in the treatment of postmenopausal breast cancer women. Mini Rev Med Chem, 2018, 18(7): 609-621.
45. Rossouw JE, Anderson GL, Prentice RL, 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.
46. D'Alonzo M, Bounous VE, Villa M, et al. Current evidence of the oncological benefit-risk profile of hormone replacement therapy. Medicina (Kaunas), 2019, 55(9): pii: E573.
47. Li CI, Daling JR, Malone KE. Incidence of invasive breast cancer by hormone receptor status from 1992 to 1998. J Clin Oncol, 2003, 21(1): 28-34.
48. Hartley MC, Mckinley BP, Rogers EA, et al. Differential expression of prognostic factors and effect on survival in young (≤40) breast cancer patients: a case-control study. Am Surg, 2006, 72(12): 1189-1194.
49. Eric I, Petek A, Kristek J, et al. Breast cancer in young women:pathologic and immunohistochemical features. Acta Clin Croat, 2018, 57(3): 497-502.
50. Cui Y, Deming SL, Shrubsole MJ, et al. Associations of hormone-related factors with breast cancer risk according to hormone receptor status among white and African American women. Clin Breast Cancer, 2014, 14(6): 417-425.
51. Tarone RE, Chu KC. The greater impact of menopause on ER- than ER+ breast cancer incidence: a possible explanation (United States). Cancer Causes Control, 2002, 13(1): 7-14.
52. Chung IY, Lee JW, Lee JS, et al. Interaction between body mass index and hormone-receptor status as a prognostic factor in lymph-node-positive breast cancer. PloS One, 2017, 12(3): e0170311.
53. Dunlap TL, Howell CE, Mukand N, et al. Red clover aryl hydrocarbon receptor (AhR) and estrogen receptor (ER) agonists enhance genotoxic estrogen metabolism. Chem Res Toxicol, 2017, 30(11): 2084-2092.
54. Paterni I, Granchi C, Katzenellenbogen JA, et al. Estrogen receptors alpha (ERα) and beta (ERβ): subtype-selective ligands and clinical potential. Steroids, 2014, 90: 13-29.
55. Heldring N, Pike A, Andersson S, et al. Estrogen receptors: how do they signal and what are their targets. Physiol Rev, 2007, 87(3): 905-931.
56. Willams C, Lin CY. Estrogen receptors in breast cancer: basic mechanisms and clinical implications. Ecancermedicalscience, 2013, 7: 370.
57. Giudice A, Barbieri A, BimonteI S, et al. Dissecting the prevention of estrogen-dependent breast carcinogenesis through Nrf2-dependent and independent mechanisms. Onco Targets Ther, 2019, 12: 4937-4953.
58. Kulkoyluoglu E, Arac A, Madak Z. Crosstalk between estrogen signaling and breast cancer metabolism. Trends in Endocrinol Metab, 2019, 30(1): 25-38.
59. Loboda A, Nebozhyn M, Klinghoffer R, et al. A gene expression signature of RAS pathway dependence predicts response to PI3K and RAS pathway inhibitors and expands the population of RAS pathway activated tumors. BMC Med Genomics, 2010, 3: 26.
60. Dey N, De P, Leylang B. PI3K-AKT-mTOR inhibitors in breast cancers: from tumor cell signaling to clinical trials. Pharmacol Ther, 2017, 175: 91-106.
61. Yndestad S, Austreid E, Svanberg IR, et al. Activation of Akt characterizes estrogen receptor positive human breast cancers which respond to anthracyclines. Oncotarget, 2017, 8(25): 41227-41241.
62. Hayes MJ, Thomas D, Emmons A, et al. Genetic changes of Wnt pathway genes are common events in metaplastic carcinomas of the breast. Clin Cancer Res, 2008, 14(13): 4038-4044.
63. Bado I, Nikolos F, Rajapaksa G, et al. Somatic loss of estrogen receptor beta and p53 synergize to induce breast tumorigenesis. Breast Cancer Res, 2017, 19(1): 79.
64. Lu W, Katzenellenbogen BS. Estrogen receptor-β modulation of the ERα-p53 Loop regulating gene expression, proliferation, and apoptosis in breast cancer. Horm Cancer, 2017, 8(4): 230-242.
65. Yang J, Altahan A, Jones DT, et al. Estrogen receptor-α directly regulates the hypoxia-inducible factor 1 pathway associated with antiestrogen response in breast cancer. Proc Natl Acad Sci U S A, 2015, 112(49): 15172-15177.
66. Huang B, Omoto Y, Iwase H, et al. Differential expression of estrogen receptor α, β1, and β2 in lobular and ductal breast cancer. Proc Natl Acad Sci U S A, 2014, 111(5): 1933-1938.

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Research progress on the relationship between estrogen metabolism and breast cancer

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