Estrogen receptor-α directly regulates the hypoxiainducible factor 1 pathway associated with antiestrogen response in breast cancer

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 49, 2015, Pages 15172-15177

  Yang, Jun ^a,b   AlTahan, Alaa ^b   Jones, Dylan T ^a   Buffa, Francesca M ^a   Bridges, Esther ^a   Interiano, Rodrigo B ^b   Qu, Chunxu ^b   Vogt, Nathan ^b   Li, Ji Liang ^a   Baban, Dilair ^c   Ragoussis, Jiannis ^c,e   Nicholson, Robert ^d   Davidoff, Andrew M ^b   Harris, Adrian L ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d CARDIFF UNIVERSITY   (United Kingdom)

^e MCGILL UNIVERSITY   (Canada)

Author keywords

ER ; HIF 1 ; Tamoxifen

Indexed keywords

ESTROGEN RECEPTOR ALPHA; FULVESTRANT; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; HYPOXIA INDUCIBLE FACTOR 1ALPHA; TAMOXIFEN; HIF1A PROTEIN, HUMAN; SELECTIVE ESTROGEN RECEPTOR MODULATOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; BREAST CANCER; BREAST CANCER CELL LINE; CANCER GROWTH; CANCER HORMONE THERAPY; CANCER RESISTANCE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; FEMALE; GENE EXPRESSION PROFILING; HORMONE RESPONSE; HUMAN; HUMAN CELL; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; TREATMENT RESPONSE; BREAST NEOPLASMS; DRUG RESISTANCE; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHYSIOLOGY;

BREAST NEOPLASMS; DRUG RESISTANCE, NEOPLASM; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR MODULATORS; FEMALE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; SIGNAL TRANSDUCTION; TAMOXIFEN; TRANSCRIPTION, GENETIC;

EID: 84949255251     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1422015112     Document Type: Article

References (41)

1. Carroll JS, Brown M (2006) Estrogen receptor target gene: An evolving concept. Mol Endocrinol 20(8):1707-1714.
2. McDonnell DP, Norris JD (2002) Connections and regulation of the human estrogen receptor. Science 296(5573):1642-1644.
3. Harvey JM, Clark GM, Osborne CK, Allred DC (1999) Estrogen receptor status by im-munohistochemistry is superior to the ligand-binding assay for predicting response to adjuvant endocrine therapy in breast cancer. J Clin Oncol 17(5):1474-1481.
4. Jordan VC (1995) Third annual William L. McGuire Memorial Lecture. "Studies on the estrogen receptor in breast cancer"-20 years as a target for the treatment and prevention of cancer. Breast Cancer Res Treat 36(3):267-285.
5. Huang HJ, Norris JD, McDonnell DP (2002) Identification of a negative regulatory surface within estrogen receptor alpha provides evidence in support of a role for corepressors in regulating cellular responses to agonists and antagonists. Mol Endocrinol 16(8): 1778-1792.
6. Howell A, DeFriend D, Robertson J, Blamey R, Walton P (1995) Response to a specific antioestrogen (ICI 182780) in tamoxifen-resistant breast cancer. Lancet 345(8941):29-30.
7. Clarke R, Leonessa F, Welch JN, Skaar TC (2001) Cellular and molecular pharmacology of antiestrogen action and resistance. Pharmacol Rev 53(1):25-71.
8. Musgrove EA, Sutherland RL (2009) Biological determinants of endocrine resistance in breast cancer. Nat Rev Cancer 9(9):631-643.
9. Toy W, et al. (2013) ESR1 ligand-binding domain mutations in hormone-resistant breast cancer. Nat Genet 45(12):1439-1445.
10. Robinson DR, et al. (2013) Activating ESR1 mutations in hormone-resistant metastatic breast cancer. Nat Genet 45(12):1446-1451.
11. Hsu PY, et al. (2013) Amplification of distant estrogen response elements deregulates target genes associated with tamoxifen resistance in breast cancer. Cancer Cell 24(2): 197-212.
12. Generali D, et al. (2009) Phosphorylated ERalpha, HIF-1alpha, and MAPK signaling as predictors of primary endocrine treatment response and resistance in patients with breast cancer. J Clin Oncol 27(2):227-234.
13. Generali D, et al. (2006) Hypoxia-inducible factor-1alpha expression predicts a poor response to primary chemoendocrine therapy and disease-free survival in primary human breast cancer. Clin Cancer Res 12(15):4562-4568.
14. Semenza GL (1998) Hypoxia-inducible factor 1: Master regulator of O2 homeostasis. Curr Opin Genet Dev 8(5):588-594.
15. Bos R, et al. (2001) Levels of hypoxia-inducible factor-1 alpha during breast carcinogenesis. J Natl Cancer Inst 93(4):309-314.
16. Brunnberg S, et al. (2003) The basic helix-loop-helix-PAS protein ARNT functions as a potent coactivator of estrogen receptor-dependent transcription. Proc Natl Acad Sci USA 100(11):6517-6522.
17. Seifeddine R, et al. (2007) Hypoxia and estrogen co-operate to regulate gene expression in T-47D human breast cancer cells. J Steroid Biochem Mol Biol 104(3-5): 169-179.
18. Yang J, et al. (2010) The histone demethylase JMJD2B is regulated by estrogen receptor alpha and hypoxia, and is a key mediator of estrogen induced growth. Cancer Res 70(16):6456-6466.
19. Beyer S, Kristensen MM, Jensen KS, Johansen JV, Staller P (2008) The histone deme-thylases JMJD1A and JMJD2B are transcriptional targets of hypoxia-inducible factor HIF. J Biol Chem 283(52):36542-36552.
20. Sharma SV, et al. (2010) A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 141(1):69-80.
21. Cancer Genome Atlas Network (2012) Comprehensive molecular portraits of human breast tumours. Nature 490(7418):61-70.
22. Frietze S, Lan X, Jin VX, Farnham PJ (2010) Genomic targets of the KRAB and SCAN domain-containing zinc finger protein 263. J Biol Chem 285(2):1393-1403.
23. Hurtado A, Holmes KA, Ross-Innes CS, Schmidt D, Carroll JS (2011) FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat Genet 43(1): 27-33.
24. Schmidt D, et al. (2010) A CTCF-independent role for cohesin in tissue-specific transcription. Genome Res 20(5):578-588.
25. Schödel J, et al. (2011) High-resolution genome-wide mapping of HIF-binding sites by ChIP-seq. Blood 117(23):e207-e217.
26. Yang J, et al. (2009) Role of hypoxia-inducible factors in epigenetic regulation via histone demethylases. Ann N Y Acad Sci 1177:185-197.
27. Bouras T, et al. (2002) Stanniocalcin 2 is an estrogen-responsive gene coexpressed with the estrogen receptor in human breast cancer. Cancer Res 62(5):1289-1295.
28. Law AY, Wong CK (2010) Stanniocalcin-2 is a HIF-1 target gene that promotes cell proliferation in hypoxia. Exp Cell Res 316(3):466-476.
29. Forsythe JA, et al. (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16(9):4604-4613.
30. Mueller MD, et al. (2000) Regulation of vascular endothelial growth factor (VEGF) gene transcription by estrogen receptors alpha and beta. Proc Natl Acad Sci USA 97(20):10972-10977.
31. Yang J, et al. (2009) Small-molecule activation of p53 blocks hypoxia-inducible factor 1alpha and vascular endothelial growth factor expression in vivo and leads to tumor cell apoptosis in normoxia and hypoxia. Mol Cell Biol 29(8):2243-2253.
32. Buffa FM, Harris AL, West CM, Miller CJ (2010) Large meta-analysis of multiple cancers reveals a common, compact and highly prognostic hypoxia metagene. Br J Cancer 102(2):428-435.
33. Györffy B, et al. (2010) An online survival analysis tool to rapidly assess the effect of 22, 277 genes on breast cancer prognosis using microarray data of 1, 809 patients. Breast Cancer Res Treat 123(3):725-731.
34. Bos R, et al. (2004) Expression of hypoxia-inducible factor-1alpha and cell cycle proteins in invasive breast cancer are estrogen receptor related. Breast Cancer Res 6(4): R450-R459.
35. Rius J, et al. (2008) NF-kappaB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1alpha. Nature 453(7196):807-811.
36. Chen X, et al. (2014) XBP1 promotes triple-negative breast cancer by controlling the HIF1α pathway. Nature 508(7494):103-107.
37. Gomez BP, et al. (2007) Human X-box binding protein-1 confers both estrogen independence and antiestrogen resistance in breast cancer cell lines. FASEB J 21(14): 4013-4027.
38. de Hoon MJ, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20(9):1453-1454.
39. Gyorffy B, Lánczky A, Szállási Z (2012) Implementing an online tool for genome-wide validation of survival-associated biomarkers in ovarian-cancer using microarray data from 1287 patients. Endocr Relat Cancer 19(2):197-208.
40. Loi S, et al. (2007) Definition of clinically distinct molecular subtypes in estrogen receptor-positive breast carcinomas through genomic grade. J Clin Oncol 25(10):1239-1246.
41. Higgins GS, et al. (2010) Overexpression of POLQ confers a poor prognosis in early breast cancer patients. Oncotarget 1(3):175-184.