SIRT1 positively regulates breast cancer associated human aromatase (CYP19A1) expression

Molecular Endocrinology

Volumn 27, Issue 3, 2013, Pages 480-490

  Holloway, Kimberly R ^a   Barbieri, Andreia ^a   Malyarchuk, Svitlana ^a   Saxena, Madhurima ^a   Nedeljkovic Kurepa, Ana ^a   Mehl, Mathieu Cameron ^a   Wang, Allison ^a   Gu, Xin ^b   Pruitt, Kevin ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b Department of Pathology ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATASE; CAMBINOL; ESTRADIOL; ESTROGEN; ESTROGEN RELATED RECEPTOR ALPHA; HYDROLASE INHIBITOR; INHIBITOR VII; MESSENGER RNA; SIRTUIN 1; SIRTUIN 2; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; BREAST CANCER; BREAST CARCINOMA; CELL POPULATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CORPUS LUTEUM; ENZYME ACTIVITY; ENZYME REGULATION; EPITHELIUM CELL; ESTROGEN SYNTHESIS; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STROMA CELL; PARACRINE SIGNALING; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SPERMATOGENESIS; TUMOR GROWTH; UPREGULATION;

AROMATASE; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASM INVASIVENESS; PROMOTER REGIONS, GENETIC; SIRTUIN 1; SIRTUIN 2;

EID: 84874538962     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2012-1347     Document Type: Article

References (55)

1. Kuperwasser C. The tumor stromal microenvironment as modulator of malignant behavior. J Mammary Gland Biol Neoplasia. 2010;15:377-379.
2. Stephens PJ, McBride DJ, Lin ML, et al. Complex landscapes of somatic rearrangement in human breast cancer genomes. Nature. 2009;462:1005-1010.
3. Portela A, Esteller M. Epigenetic modifications and human disease. Nat Biotechnol. 2010;28:1057-1068.
4. Jovanovic J, Ronneberg JA, Tost J, Kristensen V. The epigenetics of breast cancer. Mol Oncol. 2010;4:242-254.
5. Johnston SR, Dowsett M. Aromatase inhibitors for breast cancer: lessons from the laboratory. Nat Rev Cancer. 2003;3:821-831.
6. Bulun SE, Lin Z, Imir G, et al. Regulation of aromatase expression in estrogen-responsive breast and uterine disease: from bench to treatment. Pharmacol Rev. 2005;57:359-383.
7. Yue W, Wang JP, Li Y, et al. Effects of estrogen on breast cancer development: role of estrogen receptor independent mechanisms. Int J Cancer. 2010;127:1748-1757.
8. Bulun SE, Lin Z, Zhao H, et al. Regulation of aromatase expression in breast cancer tissue. Ann NY Acad Sci. 2009;1155:121-131.
9. Bonneterre J, Buzdar A, Nabholtz JM, et al. Anastrozole is superior to tamoxifen as first-line therapy in hormone receptor positive advanced breast carcinoma. Cancer. 2001;92:2247-2258.
10. Nabholtz JM, Buzdar A, Pollak M, et al. Anastrozole is superior to tamoxifen as first-line therapy for advanced breast cancer in postmenopausal women: results of a North American multicenter randomized trial. Arimidex Study Group. J Clin Oncol. 2000;18: 3758-3767.
11. Mouridsen H, Gershanovich M, Sun Y, et al. Superior efficacy of letrozole versus tamoxifen as first-line therapy for postmenopausal women with advanced breast cancer: results of a phase III study of the International Letrozole Breast Cancer Group. J Clin Oncol. 2001;19:2596-2606.
12. Burstein HJ, Prestrud AA, Seidenfeld J, et al. American Society of Clinical Oncology clinical practice guideline: update on adjuvant endocrine therapy for women with hormone receptor-positive breast cancer. J Clin Oncol. 2010;28:3784-3796.
13. Santen RJ, Brodie H, Simpson ER, Siiteri PK, Brodie A. History of aromatase: saga of an important biological mediator and therapeutic target. Endocr Rev. 2009;30:343-375.
14. Harada N. [Estrogen synthetase (P-450. aromatase) as a regulatory factor concerning sexual differentiation of brain and sexual behavior-physiological functions and regulation of gene expression of aromatase]. Seikagaku. 1993;65:67-85.
15. Agarwal VR, Bulun SE, Leitch M, Rohrich R, Simpson ER. Use of alternative promoters to express the aromatase cytochrome P450 (CYP19) gene in breast adipose tissues of cancer-free and breast cancer patients. J Clin Endocrinol Metab. 1996;81:3843-3849.
16. Clyne CD, Speed CJ, Zhou J, Simpson ER. Liver receptor homologue-1 (LRH-1) regulates expression of aromatase in preadipocytes. J Biol Chem. 2002;277:20591-20597.
17. Chand AL, Wijayakumara DD, Knower KC, Herridge KA, Howard TL, Lazarus KA, Clyne CD. The orphan nuclear receptor LRH-1 and ERα activate GREB1 expression to induce breast cancer cell proliferation. PLoS One. 2012;7:e31593.
18. Liu T, Liu PY, Marshall GM. The critical role of the class III histone deacetylase SIRT1 in cancer. Cancer Res. 2009;69:1702-1705.
19. Pruitt K, Zinn RL, Ohm JE, et al. Inhibition of SIRT1 reactivates silenced cancer genes without loss of promoter DNA hypermethylation. PLoS Genet. 2006;2:e40.
20. Hussain M, Rao M, Humphries AE, et al. Tobacco smoke induces polycomb-mediated repression of Dickkopf-1 in lung cancer cells. Cancer Res. 2009;69:3570-3578.
21. Holloway KR, Calhoun TN, Saxena M, et al. SIRT1 regulates Dishevelled proteins and promotes transient and constitutive Wnt signaling. Proc Natl Acad Sci USA. 2010;107:9216-9221.
22. Zhang Y, Zhang M, Dong H, et al. Deacetylation of cortactin by SIRT1 promotes cell migration. Oncogene. 2008.
23. Wilson BJ, Tremblay AM, Deblois G, Sylvain-Drolet G, Giguere V. An acetylation switch modulates the transcriptional activity of estrogen-related receptor α. Mol Endocrinol. 2010;24:1349-1358.
24. Yao Y, Li H, Gu Y, Davidson NE, Zhou Q. Inhibition of SIRT1 deacetylase suppresses estrogen receptor signaling. Carcinogenesis. 2010;31:382-387.
25. Elangovan S, Ramachandran S, Venkatesan N, et al. SIRT1 is essential for oncogenic signaling by estrogen/estrogen receptor α in breast cancer. Cancer Res. 2011;71:6654-6664.
26. Li H, Rajendran GK, Liu N, Ware C, Rubin BP, Gu Y. SirT1 modulates the estrogen-insulin-like growth factor-1 signaling for postnatal development of mammary gland in mice. Breast Cancer Res. 2007;9:R1.
27. McBurney MW, Yang X, Jardine K, et al. The mammalian SIR2α protein has a role in embryogenesis and gametogenesis. Mol Cell Biol. 2003;23:38-54.
28. Coussens M, Maresh JG, Yanagimachi R, Maeda G, Allsopp R. Sirt1 deficiency attenuates spermatogenesis and germ cell function. PLoS One. 2008;3:e1571.
29. Chen D, Reierstad S, Lu M, Lin Z, Ishikawa H, Bulun SE. Regulation of breast cancer-associated aromatase promoters. Cancer Lett. 2009;273:15-27.
30. Brisken C, O'Malley B. Hormone action in the mammary gland. Cold Spring Harb Perspect Biol. 2010;2:a003178.
31. Miki Y, Suzuki T, Tazawa C, et al. Aromatase localization in human breast cancer tissues: possible interactions between intratumoral stromal and parenchymal cells. Cancer Res. 2007;67:3945-3954.
32. Wiseman BS, Werb Z. Stromal effects on mammary gland development and breast cancer. Science. 2002;296:1046-1049.
33. Dunbier AK, Martin LA, Dowsett M. New and translational perspectives of oestrogen deprivation in breast cancer. Mol Cell Endocrinol. 2011;340:137-141.
34. Heltweg B, Gatbonton T, Schuler AD, et al. Antitumor activity of a small-molecule inhibitor of human silent information regulator 2 enzymes. Cancer Res. 2006;66:4368-4377.
35. Okubo T, Truong TK, Yu B, et al. Down-regulation of promoter 1.3 activity of the human aromatase gene in breast tissue by zincfinger protein, snail (SnaH). Cancer Res. 2001;61:1338-1346.
36. Tseng L, Malbon CC, Lane B, et al. Progestin-dependent effect of forskolin on human endometrial aromatase activity. Hum Reprod. 1987;2:371-377.
37. Yang C, Zhou D, Chen S. Modulation of aromatase expression in the breast tissue by ERRα-1 orphan receptor. Cancer Res. 1998;58: 5695-5700.
38. Ariazi EA, Clark GM, Mertz JE. Estrogen-related receptor α and estrogen-related receptor γ associate with unfavorable and favorable biomarkers, respectively, in human breast cancer. Cancer Res. 2002;62:6510-6518.
39. Suzuki T, Miki Y, Moriya T, et al. Estrogen-related receptor α in human breast carcinoma as a potent prognostic factor. Cancer Res. 2004;64:4670-4676.
40. Yeung F, Hoberg JE, Ramsey CS, et al. Modulation of NF-κBdependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 2004;23:2369-2380.
41. Simpson ER, Mahendroo MS, Means GD, et al. Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr Rev. 1994;15:342-355.
42. Sebastian S, Bulun SE. A highly complex organization of the regulatory region of the human CYP19 (aromatase) gene revealed by the Human Genome Project. J Clin Endocrinol Metab. 2001;86:4600-4602.
43. Zhao H, Innes J, Brooks DC, et al. A novel promoter controls Cyp19a1 gene expression in mouse adipose tissue. Reprod Biol Endocrinol. 2009;7:37.
44. Chen S, Ye J, Kijima I, Evans D. The HDAC inhibitor LBH589 (panobinostat) is an inhibitory modulator of aromatase gene expression. Proc Natl Acad Sci USA. 2010;107:11032-11037.
45. Sabnis GJ, Goloubeva OG, Chumsri S, Nguyen N, Sukumar S, Brodie AH. Functional activation of ER-α and aromatase by the HDAC inhibitor entinostat increases the sensitivity of ER-negative tumors to letrozole. Cancer Res. 2011;71(5):1893-1903.
46. Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, Puigserver P. Nutrient control of glucose homeostasis through a complex of PGC-1α and SIRT1. Nature. 2005;434:113-118.
47. Parakh TN, Hernandez JA, Grammer JC, et al. Follicle-stimulating hormone/cAMP regulation of aromatase gene expression requires β-catenin. Proc Natl Acad Sci USA. 2006;103:12435-12440.
48. Safi R, Kovacic A, Gaillard S, et al. Coactivation of liver receptor homologue-1 by peroxisome proliferator-activated receptor γ coactivator-1α on aromatase promoter II and its inhibition by activated retinoid X receptor suggest a novel target for breast-specific antiestrogen therapy. Cancer Res. 2005;65:11762-11770.
49. DiMeo TA, Anderson K, Phadke P, et al. A novel lung metastasis signature links Wnt signaling with cancer cell self-renewal and epithelial-mesenchymal transition in basal-like breast cancer. Cancer Res. 2009;69:5364-5373.
50. Lee H, Kim KR, Noh SJ, et al. Expression of DBC1 and SIRT1 is associated with poor prognosis for breast carcinoma. Hum Pathol. 2011;42:204-213.
51. Chen J, Zhang B, Wong N, et al. Sirtuin 1 is upregulated in a subset of hepatocellular carcinomas where it is essential for telomere maintenance and tumor cell growth. Cancer Res. 2011;71:4138-4149.
52. Jang KY, Hwang SH, Kwon KS, et al. SIRT1 expression is associated with poor prognosis of diffuse large B-cell lymphoma. Am J Surg Pathol. 2008;32:1523-1531.
53. Cha EJ, Noh SJ, Kwon KS, et al. Expression of DBC1 and SIRT1 is associated with poor prognosis of gastric carcinoma. Clin Cancer Res. 2009;15:4453-4459.
54. Nosho K, Shima K, Irahara N, et al. SIRT1 histone deacetylase expression is associated with microsatellite instability and CpG island methylator phenotype in colorectal cancer. Mod Pathol. 2009;22:922-932.
55. Deblois G, Hall JA, Perry MC, et al. Genome-wide identification of direct target genes implicates estrogen-related receptor α as a determinant of breast cancer heterogeneity. Cancer Res. 2009;69:6149-6157.