Tamoxifen-induced epigenetic silencing of oestrogen-regulated genes in anti-hormone resistant breast cancer

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Stone, Andrew ^a,b   Valdés Mora, Fatima ^b   Gee, Julia M W ^a   Farrow, Lynne ^a   McClelland, Richard A ^a   Fiegl, Heidi ^c   Dutkowski, Carol ^a   McCloy, Rachael A ^b   Sutherland, Robert L ^b,d   Musgrove, Elizabeth A ^b,d   Nicholson, Robert I ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^d UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AFIMOXIFENE; AZACITIDINE; EPIDERMAL GROWTH FACTOR RECEPTOR; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; FULVESTRANT; GEFITINIB; GROWTH DIFFERENTIATION FACTOR 15; PROGESTERONE RECEPTOR; PROTEIN PS2; TAMOXIFEN;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER INHIBITION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; DOWN REGULATION; DRUG RESISTANCE; DRUG SENSITIVITY; EPIGENETICS; GENE EXPRESSION; GENE IDENTIFICATION; GENE SILENCING; HUMAN; IN VITRO STUDY; PROMOTER REGION; PROTEIN EXPRESSION; UPREGULATION;

APOPTOSIS; AZACITIDINE; BREAST NEOPLASMS; CELL PROLIFERATION; DNA METHYLATION; DRUG RESISTANCE, NEOPLASM; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GENES, NEOPLASM; GROWTH DIFFERENTIATION FACTOR 15; HUMANS; MCF-7 CELLS; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, ESTROGEN; RECEPTORS, PROGESTERONE; RECOMBINANT PROTEINS; TAMOXIFEN; TUMOR SUPPRESSOR PROTEINS;

EID: 84863694083     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040466     Document Type: Article

References (61)

1. Schiff R, Massarweh S, Shou J, Osborne CK, (2003) Breast cancer endocrine resistance: how growth factor signaling and estrogen receptor coregulators modulate response. Clin Cancer Res 9: 447S-454S.
2. Musgrove EA, Sutherland RL, (2009) Biological determinants of endocrine resistance in breast cancer. Nat Rev Cancer 9: 631-643.
3. Ring A, Dowsett M, (2004) Mechanisms of tamoxifen resistance. Endocr Relat Cancer 11: 643-658.
4. Brunner N, Frandsen TL, Holst-Hansen C, Bei M, Thompson EW, et al. (1993) MCF7/LCC2: a 4-hydroxytamoxifen resistant human breast cancer variant that retains sensitivity to the steroidal antiestrogen ICI 182,780. Cancer Res 53: 3229-3232.
5. Johnston SR, Saccani-Jotti G, Smith IE, Salter J, Newby J, et al. (1995) Changes in estrogen receptor, progesterone receptor, and pS2 expression in tamoxifen-resistant human breast cancer. Cancer Res 55: 3331-3338.
6. Nicholson R, Hutcheson I, Jones H, Hiscox S, Giles M, et al. (2007) Growth factor signalling in endocrine and anti-growth factor resistant breast cancer. Reviews in Endocrine & Metabolic Disorders 8: 241-253.
7. Robertson JF, (2001) ICI 182,780 (Fulvestrant)-the first oestrogen receptor down-regulator-current clinical data. Br J Cancer 85: 11-14.
8. McClelland RA, Barrow D, Madden T-A, Dutkowski CM, Pamment J, et al. (2001) Enhanced Epidermal Growth Factor Receptor Signaling in MCF7 Breast Cancer Cells after Long-Term Culture in the Presence of the Pure Antiestrogen ICI 182,780 (Faslodex). Endocrinology 142: 2776-2788.
9. Gutteridge E, Agrawal A, Nicholson R, Leung Cheung K, Robertson J, et al. (2010) The effects of gefitinib in tamoxifen-resistant and hormone-insensitive breast cancer: A phase II study. International Journal of Cancer 126: 1806-1816.
10. Badia E, Duchesne MJ, Semlali A, Fuentes M, Giamarchi C, et al. (2000) Long-term hydroxytamoxifen treatment of an MCF-7-derived breast cancer cell line irreversibly inhibits the expression of estrogenic genes through chromatin remodeling. Cancer Res 60: 4130-4138.
11. Lavinsky RM, Jepsen K, Heinzel T, Torchia J, Mullen TM, et al. (1998) Diverse signaling pathways modulate nuclear receptor recruitment of N-CoR and SMRT complexes. Proc Natl Acad Sci U S A 95: 2920-2925.
12. Montano MM, Ekena K, Delage-Mourroux R, Chang W, Martini P, et al. (1999) An estrogen receptor-selective coregulator that potentiates the effectiveness of antiestrogens and represses the activity of estrogens. Proc Natl Acad Sci U S A 96: 6947-6952.
13. Norris JD, Fan D, Sherk A, McDonnell DP, (2002) A negative coregulator for the human ER. Mol Endocrinol 16: 459-468.
14. Oesterreich S, Zhang Q, Hopp T, Fuqua SA, Michaelis M, et al. (2000) Tamoxifen-bound estrogen receptor (ER) strongly interacts with the nuclear matrix protein HET/SAF-B, a novel inhibitor of ER-mediated transactivation. Mol Endocrinol 14: 369-381.
15. Wu L, Wu Y, Gathings B, Wan M, Li X, et al. (2003) Smad4 as a transcription corepressor for estrogen receptor alpha. J Biol Chem 278: 15192-15200.
16. Liu XF, Bagchi MK, (2004) Recruitment of distinct chromatin-modifying complexes by tamoxifen-complexed estrogen receptor at natural target gene promoters in vivo. J Biol Chem 279: 15050-15058.
17. Fuks F, Burgers WA, Brehm A, Hughes-Davies L, Kouzarides T, (2000) DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nat Genet 24: 88-91.
18. Bachman KE, Rountree MR, Baylin SB, (2001) Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J Biol Chem 276: 32282-32287.
19. Rountree MR, Bachman KE, Baylin SB, (2000) DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat Genet 25: 269-277.
20. Fan M, Yan PS, Hartman-Frey C, Chen L, Paik H, et al. (2006) Diverse gene expression and DNA methylation profiles correlate with differential adaptation of breast cancer cells to the antiestrogens tamoxifen and fulvestrant. Cancer Res 66: 11954-11966.
21. Treeck O, Zhou R, Diedrich K, Ortmann O, (2004) Tamoxifen long-term treatment in vitro alters the apoptotic response of MCF-7 breast cancer cells. Anticancer Drugs 15: 787-793.
22. Wu M, Soler DR, Abba MC, Nunez MI, Baer R, et al. (2007) CtIP silencing as a novel mechanism of tamoxifen resistance in breast cancer. Mol Cancer Res 5: 1285-1295.
23. Knowlden JM, Hutcheson IR, Jones HE, Madden T, Gee JM, et al. (2003) Elevated levels of epidermal growth factor receptor/c-erbB2 heterodimers mediate an autocrine growth regulatory pathway in tamoxifen-resistant MCF-7 cells. Endocrinology 144: 1032-1044.
24. Clark SJ, Harrison J, Paul CL, Frommer M, (1994) High sensitivity mapping of methylated cytosines. Nucleic Acids Res 22: 2990-2997.
25. Clark SJ, Statham A, Stirzaker C, Molloy PL, Frommer M, (2006) DNA methylation: bisulphite modification and analysis. Nat Protoc 1: 2353-2364.
26. Patterson K, Molloy L, Qu W, Clark S, (2011) DNA methylation: bisulphite modification and analysis. J Vis Exp.
27. Hutcheson IR, Knowlden JM, Madden TA, Barrow D, Gee JM, et al. (2003) Oestrogen receptor-mediated modulation of the EGFR/MAPK pathway in tamoxifen-resistant MCF-7 cells. Breast Cancer Res Treat 81: 81-93.
28. Gutierrez MC, Detre S, Johnston S, Mohsin SK, Shou J, et al. (2005) Molecular changes in tamoxifen-resistant breast cancer: relationship between estrogen receptor, HER-2, and p38 mitogen-activated protein kinase. J Clin Oncol 23: 2469-2476.
29. van Agthoven T, van Agthoven T, Dekker A, Foekens J, Dorssers L, (1994) Induction of estrogen independence of ZR-75-1 human breast cancer cells by epigenetic alterations. Mol Endocrinol 8: 1474-1483.
30. Sadikovic B, Haines TR, Butcher DT, Rodenhiser DI, (2004) Chemically induced DNA hypomethylation in breast carcinoma cells detected by the amplification of intermethylated sites. Breast Cancer Res 6: R329-337.
31. Mossman D, Kim KT, Scott RJ, (2010) Demethylation by 5-aza-2′-deoxycytidine in colorectal cancer cells targets genomic DNA whilst promoter CpG island methylation persists. BMC Cancer 10: 366.
32. Mossman D, Scott RJ, (2011) Long term transcriptional reactivation of epigenetically silenced genes in colorectal cancer cells requires DNA hypomethylation and histone acetylation. PLoS One 6: 4.
33. Lim HW, Iwatani M, Hattori N, Tanaka S, Yagi S, et al. (2010) Resistance to 5-aza-2′-deoxycytidine in genic regions compared to non-genic repetitive sequences. J Reprod Dev 56: 86-93.
34. Naughton C, MacLeod K, Kuske B, Clarke R, Cameron DA, et al. (2007) Progressive Loss of Estrogen Receptor α Cofactor Recruitment in Endocrine Resistance. Molecular Endocrinology 21: 2615-2626.
35. Gee JMW, Shaw VE, Hiscox SE, McClelland RA, Rushmere NK, et al. (2006) Deciphering antihormone-induced compensatory mechanisms in breast cancer and their therapeutic implications. Endocr Relat Cancer 13: S77-88.
36. Gardiner-Garden M, Frommer M, (1987) CpG islands in vertebrate genomes. J Mol Biol 196: 261-282.
37. Carroll JS, Meyer CA, Song J, Li W, Geistlinger TR, et al. (2006) Genome-wide analysis of estrogen receptor binding sites. Nat Genet 38: 1289-1297.
38. Hostanska K, Nisslein T, Freudenstein J, Reichling J, Saller R, (2004) Cimicifuga racemosa Extract Inhibits Proliferation of Estrogen Receptor-positive and Negative Human Breast Carcinoma Cell Lines by Induction of Apoptosis. Breast Cancer Research and Treatment 84: 151-160.
39. Song RX-D, Mor G, Naftolin F, McPherson RA, Song J, et al. (2001) Effect of Long-Term Estrogen Deprivation on Apoptotic Responses of Breast Cancer Cells to 17β-Estradiol. Journal of the National Cancer Institute 93: 1714-1723.
40. Lewis JS, Meeke K, Osipo C, Ross EA, Kidawi N, et al. (2005) Intrinsic Mechanism of Estradiol-Induced Apoptosis in Breast Cancer Cells Resistant to Estrogen Deprivation. Journal of the National Cancer Institute 97: 1746-1759.
41. Levenson AS, Jordan VC, (1994) Transfection of human estrogen receptor (ER) cDNA into ER-negative mammalian cell lines. J Steroid Biochem Mol Biol 51: 229-239.
42. Licznar A, Caporali S, Lucas A, Weisz A, Vignon F, et al. (2003) Identification of genes involved in growth inhibition of breast cancer cells transduced with estrogen receptor. FEBS Lett 553: 445-450.
43. Peethambaram PP, Ingle JN, Suman VJ, Hartmann LC, Loprinzi CL, (1999) Randomized trial of diethylstilbestrol vs. tamoxifen in postmenopausal women with metastatic breast cancer. An updated analysis. Breast Cancer Res Treat 54: 117-122.
44. Frasor J, Danes JM, Komm B, Chang KCN, Lyttle CR, et al. (2003) Profiling of Estrogen Up- and Down-Regulated Gene Expression in Human Breast Cancer Cells: Insights into Gene Networks and Pathways Underlying Estrogenic Control of Proliferation and Cell Phenotype. Endocrinology 144: 4562-4574.
45. Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, et al. (2009) The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet 41: 178-186.
46. Tan M, Wang Y, Guan K, Sun Y, (2000) PTGF-β, a type β transforming growth factor (TGF-β) superfamily member, is a p53 target gene that inhibits tumor cell growth via TGF-β signaling pathway. Proceedings of the National Academy of Sciences 97: 109-114.
47. Bootcov MR, Bauskin AR, Valenzuela SM, Moore AG, Bansal M, et al. (1997) MIC-1, a novel macrophage inhibitory cytokine, is a divergent member of the TGF-beta superfamily. Proc Natl Acad Sci U S A 94: 11514-11519.
48. Ibanez de Caceres I, Dulaimi E, Hoffman AM, Al-Saleem T, Uzzo RG, et al. (2006) Identification of Novel Target Genes by an Epigenetic Reactivation Screen of Renal Cancer. Cancer Research 66: 5021-5028.
49. Baek SJ, Kim K-S, Nixon JB, Wilson LC, Eling TE, (2001) Cyclooxygenase Inhibitors Regulate the Expression of a TGF-β Superfamily Member That Has Proapoptotic and Antitumorigenic Activities. Molecular Pharmacology 59: 901-908.
50. Li P-X, Wong J, Ayed A, Ngo D, Brade AM, et al. (2000) Placental Transforming Growth Factor-β Is a Downstream Mediator of the Growth Arrest and Apoptotic Response of Tumor Cells to DNA Damage and p53 Overexpression. Journal of Biological Chemistry 275: 20127-20135.
51. Graichen R, Liu D, Sun Y, Lee K-O, Lobie PE, (2002) Autocrine Human Growth Hormone Inhibits Placental Transforming Growth Factor-β Gene Transcription to Prevent Apoptosis and Allow Cell Cycle Progression of Human Mammary Carcinoma Cells. Journal of Biological Chemistry 277: 26662-26672.
52. Albertoni M, Shaw PH, Nozaki M, Godard S, Tenan M, et al. (2002) Anoxia induces macrophage inhibitory cytokine-1 (MIC-1) in glioblastoma cells independently of p53 and HIF-1. Oncogene 21: 4212-4219.
53. Abd El-Aziz SH, Endo Y, Miyamaori H, Takino T, Sato H, (2007) Cleavage of growth differentiation factor 15 (GDF15) by membrane type 1-matrix metalloproteinase abrogates GDF15-mediated suppression of tumor cell growth. Cancer Science 98: 1330-1335.
54. Mosesson Y, Mills GB, Yarden Y, (2008) Derailed endocytosis: an emerging feature of cancer. Nat Rev Cancer 8: 835-850.
55. Jin H, Wang X, Ying J, Wong AH, Cui Y, et al. (2007) Epigenetic silencing of a Ca(2+)-regulated Ras GTPase-activating protein RASAL defines a new mechanism of Ras activation in human cancers. Proc Natl Acad Sci U S A 104: 12353-12358.
56. Keyse SM, (2008) Dual-specificity MAP kinase phosphatases (MKPs) and cancer. Cancer Metastasis Rev 27: 253-261.
57. Aung CS, Ye W, Plowman G, Peters AA, Monteith GR, et al. (2009) Plasma membrane calcium ATPase 4 and the remodeling of calcium homeostasis in human colon cancer cells. Carcinogenesis.
58. Reisner PD, Brandt PC, Vanaman TC, (1997) Analysis of plasma membrane Ca(2+)-ATPase expression in control and SV40-transformed human fibroblasts. Cell Calcium 21: 53-62.
59. Zhang L, Zhong K, Dai Y, Zhou H, (2009) Genome-wide analysis of histone H3 lysine 27 trimethylation by ChIP-chip in gastric cancer patients. Journal of Gastroenterology 44: 305-312.
60. Gupta M, McDougal A, Safe S, (1998) Estrogenic and antiestrogenic activities of 16alpha- and 2-hydroxy metabolites of 17beta-estradiol in MCF-7 and T47D human breast cancer cells. J Steroid Biochem Mol Biol 67: 413-419.
61. Leu Y-W, Yan PS, Fan M, Jin VX, Liu JC, et al. (2004) Loss of Estrogen Receptor Signaling Triggers Epigenetic Silencing of Downstream Targets in Breast Cancer. Cancer Research 64: 8184-8192.