Integrative analyses of gene expression and DNA methylation profiles in breast cancer cell line models of tamoxifen-resistance indicate a potential role of cells with stem-like properties

Breast Cancer Research

Volumn 15, Issue 6, 2013, Pages

  Lin, Xue ^a,b   Li, Jian ^a,b,c,d   Yin, Guangliang ^a,c   Zhao, Qian ^e   Elias, Daniel ^a,d   Lykkesfeldt, Anne E ^a,f   Stenvang, Jan ^a,g   Brünner, Nils ^a,g   Wang, Jun ^a,c   Yang, Huanming ^a,c,h   Bolund, Lars ^a,b,c   Ditzel, Henrik J ^a,d,i  

^a Sino Danish Breast Cancer Research Centre   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

^c BGI SHENZHEN   (China)

^d UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^e TONGJI UNIVERSITY   (China)

^f DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^g UNIVERSITY OF COPENHAGEN   (Denmark)

^h James D Watson of Institute of Genome Sciences   (China)

ⁱ ODENSE UNIVERSITY HOSPITAL   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

TAMOXIFEN; TOSYLARGININE METHYL ESTER; TRANSCRIPTION FACTOR SOX2; CYCLIN D1; ERB2 PROTEIN; ESR2 PROTEIN; FIS1 PROTEIN; HECA PROTEIN; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; MYC PROTEIN; NFKB1 PROTEIN; NOTCH3 RECEPTOR; PGR PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PRKCA PROTEIN; PROTEIN; PROTEIN P130; RECEPTOR INTERACTING PROTEIN 140; TRANSCRIPTION FACTOR E2F; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR E2F2; TRANSCRIPTION FACTOR E2F3; TRANSCRIPTION FACTOR E2F4; TRANSCRIPTION FACTOR SOX13; TRANSCRIPTION FACTOR SOX3; TRANSCRIPTION FACTOR SOX4; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; ANTINEOPLASTIC HORMONE AGONISTS AND ANTAGONISTS; PRKCA PROTEIN, HUMAN; PROTEIN KINASE C ALPHA; SOX2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX;

ARTICLE; BREAST CANCER; CANCER RESISTANCE; DNA METHYLATION; GENE EXPRESSION; HUMAN; HUMAN CELL; KARYOTYPING; MULTIGENE FAMILY; PROMOTER REGION; STEM CELL; BREAST CANCER CELL LINE; CANCER STEM CELL; CELL DIFFERENTIATION; CONTROLLED STUDY; DIGITAL GENE EXPRESSION; DNA METHYLATION SPECIFIC DIGITAL KARYOTYPING; HUMAN GENOME; NUCLEOTIDE SEQUENCE; SIGNAL TRANSDUCTION; BREAST NEOPLASMS; DRUG EFFECTS; DRUG RESISTANCE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MCF 7 CELL LINE; PATHOLOGY; PRINCIPAL COMPONENT ANALYSIS; REPRODUCIBILITY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS, HORMONAL; BREAST NEOPLASMS; CELL LINE, TUMOR; DNA METHYLATION; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MCF-7 CELLS; NEOPLASTIC STEM CELLS; PRINCIPAL COMPONENT ANALYSIS; PROTEIN KINASE C-ALPHA; REPRODUCIBILITY OF RESULTS; SOXB1 TRANSCRIPTION FACTORS; TAMOXIFEN;

EID: 84890377527     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr3588     Document Type: Article

References (69)

1. Clark GM, Osborne CK, McGuire WL. Correlations between estrogen receptor, progesterone receptor, and patient characteristics in human breast cancer. J Clin Oncol 1984, 2:1102-1109.
2. Talman ML, Rasmussen BB, Andersen J, Christensen IJ. Estrogen receptor analyses in the Danish Breast Cancer Cooperative Group. History, methods, prognosis and clinical implications. Acta Oncol 2008, 47:789-794. 10.1080/02841860801982741, 18465350.
3. Jordan VC, O'Malley BW. Selective estrogen-receptor modulators and antihormonal resistance in breast cancer. J Clin Oncol 2007, 25:5815-5824. 10.1200/JCO.2007.11.3886, 17893378.
4. Clarke R, Liu MC, Bouker KB, Gu Z, Lee RY, Zhu Y, Skaar TC, Gomez B, O'Brien K, Wang Y, Hilakivi-Clarke LA. Antiestrogen resistance in breast cancer and the role of estrogen receptor signaling. Oncogene 2003, 22:7316-7339. 10.1038/sj.onc.1206937, 14576841.
5. Davies C, Godwin J, Gray R, Clarke M, Cutter D, Darby S, McGale P, Pan HC, Taylor C, Wang YC, Dowsett M, Ingle J, Peto R, Early Breast Cancer Trialists' Collaborative Group Relevance of breast cancer hormone receptors and other factors to the efficacy of adjuvant tamoxifen: patient-level meta-analysis of randomised trials. Lancet 2011, 378:771-784. 3163848, 21802721, Early Breast Cancer Trialists' Collaborative Group.
6. Musgrove EA, Sutherland RL. Biological determinants of endocrine resistance in breast cancer. Nat Rev Cancer 2009, 9:631-643. 10.1038/nrc2713, 19701242.
7. Ring A, Dowsett M. Mechanisms of tamoxifen resistance. Endocr Relat Cancer 2004, 11:643-658. 10.1677/erc.1.00776, 15613444.
8. Osborne CK, Schiff R. Mechanisms of endocrine resistance in breast cancer. Annu Rev Med 2011, 62:233-247. 10.1146/annurev-med-070909-182917, 3656649, 20887199.
9. Soule HD, Vazguez J, Long A, Albert S, Brennan M. A human cell line from a pleural effusion derived from a breast carcinoma. J Natl Cancer Inst 1973, 51:1409-1416.
10. Lippman M, Bolan G, Huff K. The effects of estrogens and antiestrogens on hormone-responsive human breast cancer in long-term tissue culture. Cancer Res 1976, 36:4595-4601.
11. Lykkesfeldt AE, Madsen MW, Briand P. Altered expression of estrogen-regulated genes in a tamoxifen-resistant and ICI 164,384 and ICI 182,780 sensitive human breast cancer cell line, MCF-7/TAMR-1. Cancer Res 1994, 54:1587-1595.
12. Madsen MW, Reiter BE, Larsen SS, Briand P, Lykkesfeldt AE. Estrogen receptor messenger RNA splice variants are not involved in antiestrogen resistance in sublines of MCF-7 human breast cancer cells. Cancer Res 1997, 57:585-589.
13. Frogne T, Jepsen JS, Larsen SS, Fog CK, Brockdorff BL, Lykkesfeldt AE. Antiestrogen-resistant human breast cancer cells require activated protein kinase B/Akt for growth. Endocr Relat Cancer 2005, 12:599-614. 10.1677/erc.1.00946, 16172194.
14. Nabha SM, Glaros S, Hong M, Lykkesfeldt AE, Schiff R, Osborne K, Reddy KB. Upregulation of PKC-delta contributes to antiestrogen resistance in mammary tumor cells. Oncogene 2005, 24:3166-3176. 10.1038/sj.onc.1208502, 15735693.
15. Pancholi S, Lykkesfeldt AE, Hilmi C, Banerjee S, Leary A, Drury S, Johnston S, Dowsett M, Martin LA. ERBB2 influences the subcellular localization of the estrogen receptor in tamoxifen-resistant MCF-7 cells leading to the activation of AKT and RPS6KA2. Endocr Relat Cancer 2008, 15:985-1002. 10.1677/ERC-07-0240, 18824559.
16. Perez-Tenorio G, Stal O, Southeast Sweden Breast Cancer G Activation of AKT/PKB in breast cancer predicts a worse outcome among endocrine treated patients. Br J Cancer 2002, 86:540-545. 10.1038/sj.bjc.6600126, 2375266, 11870534, Southeast Sweden Breast Cancer G.
17. Rasmussen BB, Regan MM, Lykkesfeldt AE, Dell'Orto P, Del Curto B, Henriksen KL, Mastropasqua MG, Price KN, Mery E, Lacroix-Triki M, Braye S, Altermatt HJ, Gelber RD, Castiglione-Gertsch M, Goldhirsch A, Gusterson BA, Thürlimann B, Coates AS, Viale G, BIG 1-98 Collaborative and International Breast Cancer Study Groups Adjuvant letrozole versus tamoxifen according to centrally-assessed ERBB2 status for postmenopausal women with endocrine-responsive early breast cancer: supplementary results from the BIG 1-98 randomised trial. Lancet Oncol 2008, 9:23-28. 10.1016/S1470-2045(07)70386-8, 18083065, BIG 1-98 Collaborative and International Breast Cancer Study Groups.
18. Frogne T, Laenkholm AV, Lyng MB, Henriksen KL, Lykkesfeldt AE. Determination of HER2 phosphorylation at tyrosine 1221/1222 improves prediction of poor survival for breast cancer patients with hormone receptor-positive tumors. Breast Cancer Res 2009, 11:R11. 10.1186/bcr2230, 2687716, 19239686.
19. Brunner N, Frandsen TL, Holst-Hansen C, Bei M, Thompson EW, Wakeling AE, Lippman ME, Clarke R. MCF7/LCC2: a 4-hydroxytamoxifen resistant human breast cancer variant that retains sensitivity to the steroidal antiestrogen ICI 182,780. Cancer Res 1993, 53:3229-3232.
20. Bernstein BE, Meissner A, Lander ES. The mammalian epigenome. Cell 2007, 128:669-681. 10.1016/j.cell.2007.01.033, 17320505.
21. Heyn H, Esteller M. DNA methylation profiling in the clinic: applications and challenges. Nat Rev Genet 2012, 13:679-692. 10.1038/nrg3270, 22945394.
22. Fan M, Yan PS, Hartman-Frey C, Chen L, Paik H, Oyer SL, Salisbury JD, Cheng AS, Li L, Abbosh PH, Huang TH, Nephew KP. Diverse gene expression and DNA methylation profiles correlate with differential adaptation of breast cancer cells to the antiestrogens tamoxifen and fulvestrant. Cancer Res 2006, 66:11954-11966. 10.1158/0008-5472.CAN-06-1666, 17178894.
23. van Agthoven T, van Agthoven TL, Dekker A, Foekens JA, Dorssers LC. Induction of estrogen independence of ZR-75-1 human breast cancer cells by epigenetic alterations. Mol Endocrinol 1994, 8:1474-1483.
24. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005, 5:275-284. 10.1038/nrc1590, 15803154.
25. Li J, Gao F, Li N, Li S, Yin G, Tian G, Jia S, Wang K, Zhang X, Yang H, Nielsen AL, Bolund L. An improved method for genome wide DNA methylation profiling correlated to transcription and genomic instability in two breast cancer cell lines. BMC Genomics 2009, 10:223. 10.1186/1471-2164-10-223, 2696471, 19439076.
26. Briand P, Lykkesfeldt AE. Long-term cultivation of a human breast cancer cell line, MCF-7, in a chemically defined medium. Effect of estradiol. Anticancer Res 1986, 6:85-90.
27. Lykkesfeldt AE, Briand P. Indirect mechanism of oestradiol stimulation of cell proliferation of human breast cancer cell lines. Br J Cancer 1986, 53:29-35. 10.1038/bjc.1986.5, 2001475, 3947513.
28. Thrane S, Lykkesfeldt AE, Larsen MS, Sorensen BS, Yde CW. Estrogen receptor α is the major driving factor for growth in tamoxifen-resistant breast cancer and supported by HER/ERK signaling. Breast Cancer Res Treat 2013, 139:71-80. 10.1007/s10549-013-2485-2, 23609470.
29. Clarke R, Brunner N, Katzenellenbogen BS, Thompson EW, Norman MJ, Koppi C, Paik S, Lippman ME, Dickson RB. Progression of human breast cancer cells from hormone-dependent to hormone-independent growth both in vitro and in vivo. Proc Natl Acad Sci U S A 1989, 86:3649-3653. 10.1073/pnas.86.10.3649, 287195, 2726742.
30. Brunner N, Boulay V, Fojo A, Freter CE, Lippman ME, Clarke R. Acquisition of hormone-independent growth in MCF-7 cells is accompanied by increased expression of estrogen-regulated genes but without detectable DNA amplifications. Cancer Res 1993, 53:283-290.
31. Tempel S. Using and understanding RepeatMasker. Methods Mol Biol 2012, 859:29-51. 10.1007/978-1-61779-603-6_2, 22367864.
32. FASTX-Toolkit. [http://hannonlab.cshl.edu/fastx_toolkit/index.html].
33. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760. 10.1093/bioinformatics/btp324, 2705234, 19451168.
34. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. Integrative genomics viewer. Nat Biotechnol 2011, 29:24-26. 10.1038/nbt.1754, 3346182, 21221095.
35. UCSC Genome Bioinformatics. [http://genome.ucsc.edu].
36. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 2005, 102:15545-15550. 10.1073/pnas.0506580102, 1239896, 16199517.
37. Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 2011, 27:1571-1572. 10.1093/bioinformatics/btr167, 3102221, 21493656.
38. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
39. Li Z, Liu C, Xie Z, Song P, Zhao RC, Guo L, Liu Z, Wu Y. Epigenetic dysregulation in mesenchymal stem cell aging and spontaneous differentiation. PLoS One 2011, 6:e20526. 10.1371/journal.pone.0020526, 3111432, 21694780.
40. Brockdorff BL, Heiberg I, Lykkesfeldt AE. Resistance to different antiestrogens is caused by different multi-factorial changes and is associated with reduced expression of IGF receptor Iα. Endocr Relat Cancer 2003, 10:579-590. 10.1677/erc.0.0100579, 14713268.
41. Primer3. [http://frodo.wi.mit.edu/].
42. de Cremoux P, Tran-Perennou C, Brockdorff BL, Boudou E, Brunner N, Magdelenat H, Lykkesfeldt AE. Validation of real-time RT-PCR for analysis of human breast cancer cell lines resistant or sensitive to treatment with antiestrogens. Endocr Relat Cancer 2003, 10:409-418. 10.1677/erc.0.0100409, 14503918.
43. Petersen OW, Polyak K. Stem cells in the human breast. Cold Spring Harb Perspect Biol 2010, 2:a003160. 2857168, 20452965.
44. Scheel C, Eaton EN, Li SH, Chaffer CL, Reinhardt F, Kah KJ, Bell G, Guo W, Rubin J, Richardson AL, Weinberg RA. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell 2011, 145:926-940. 10.1016/j.cell.2011.04.029, 21663795.
45. Al-Hajj M, Becker MW, Wicha M, Weissman I, Clarke MF. Therapeutic implications of cancer stem cells. Curr Opin Genet Dev 2004, 14:43-47. 10.1016/j.gde.2003.11.007, 15108804.
46. Leis O, Eguiara A, Lopez-Arribillaga E, Alberdi MJ, Hernandez-Garcia S, Elorriaga K, Pandiella A, Rezola R, Martin AG. Sox2 expression in breast tumours and activation in breast cancer stem cells. Oncogene 2012, 31:1354-1365. 10.1038/onc.2011.338, 21822303.
47. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676. 10.1016/j.cell.2006.07.024, 16904174.
48. O'Brien C, Howell S, Gee J, Lykkesfeldt A, Nicholson R, Clarke R. Tamoxifen resistance in ER+ breast cancer is driven by ER- cancer stem-like cells [Abstract 5125]. Cancer Res 2009, 69(24 Suppl). Abstract nr 5125.
49. Chen Y, Shi L, Zhang L, Li R, Liang J, Yu W, Sun L, Yang X, Wang Y, Zhang Y, Shang Y. The molecular mechanism governing the oncogenic potential of SOX2 in breast cancer. J Biol Chem 2008, 283:17969-17978. 10.1074/jbc.M802917200, 18456656.
50. Lefebvre V, Dumitriu B, Penzo-Mendez A, Han Y, Pallavi B. Control of cell fate and differentiation by Sry-related high-mobility-group box (Sox) transcription factors. Int J Biochem Cell Biol 2007, 39:2195-2214. 10.1016/j.biocel.2007.05.019, 2080623, 17625949.
51. Gjerstorff MF, Johansen LE, Nielsen O, Kock K, Ditzel HJ. Restriction of GAGE protein expression to subpopulations of cancer cells is independent of genotype and may limit the use of GAGE proteins as targets for cancer immunotherapy. Br J Cancer 2006, 94:1864-1873. 10.1038/sj.bjc.6603163, 2361341, 16773077.
52. Alles MC, Gardiner-Garden M, Nott DJ, Wang Y, Foekens JA, Sutherland RL, Musgrove EA, Ormandy CJ. Meta-analysis and gene set enrichment relative to er status reveal elevated activity of MYC and E2F in the 'basal' breast cancer subgroup. PLoS One 2009, 4:e4710. 10.1371/journal.pone.0004710, 2650420, 19270750.
53. Topol L, Chen W, Song H, Day TF, Yang Y. Sox9 inhibits Wnt signaling by promoting beta-catenin phosphorylation in the nucleus. J Biol Chem 2009, 284:3323-3333. 2631972, 19047045.
54. Wong J, Farlie P, Holbert S, Lockhart P, Thomas PQ. Polyalanine expansion mutations in the X-linked hypopituitarism gene SOX3 result in aggresome formation and impaired transactivation. Front Biosci 2007, 12:2085-2095. 10.2741/2213, 17127446.
55. Bernard P, Harley VR. Acquisition of SOX transcription factor specificity through protein-protein interaction, modulation of Wnt signalling and post-translational modification. Int J Biochem Cell Biol 2010, 42:400-410. 10.1016/j.biocel.2009.10.017, 19854293.
56. Ivanova IA, D'Souza SJ, Dagnino L. Signalling in the epidermis: the E2F cell cycle regulatory pathway in epidermal morphogenesis, regeneration and transformation. Int J Biol Sci 2005, 1:87-95. 1142216, 15951853.
57. Becker KA, Stein JL, Lian JB, van Wijnen AJ, Stein GS. Establishment of histone gene regulation and cell cycle checkpoint control in human embryonic stem cells. J Cell Physiol 2007, 210:517-526. 10.1002/jcp.20903, 17096384.
58. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, Wicha MS. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003, 17:1253-1270. 10.1101/gad.1061803, 196056, 12756227.
59. Sansone P, Storci G, Giovannini C, Pandolfi S, Pianetti S, Taffurelli M, Santini D, Ceccarelli C, Chieco P, Bonafe M. p66Shc/Notch-3 interplay controls self-renewal and hypoxia survival in human stem/progenitor cells of the mammary gland expanded in vitro as mammospheres. Stem Cells 2007, 25:807-815.
60. Shipitsin M, Campbell LL, Argani P, Weremowicz S, Bloushtain-Qimron N, Yao J, Nikolskaya T, Serebryiskaya T, Beroukhim R, Hu M, Halushka MK, Sukumar S, Parker LM, Anderson KS, Harris LN, Garber JE, Richardson AL, Schnitt SJ, Nikolsky Y, Gelman RS, Polyak K. Molecular definition of breast tumor heterogeneity. Cancer Cell 2007, 11:259-273. 10.1016/j.ccr.2007.01.013, 17349583.
61. Dowejko A, Bauer R, Bauer K, Muller-Richter UD, Reichert TE. The human HECA interacts with cyclins and CDKs to antagonize Wnt-mediated proliferation and chemoresistance of head and neck cancer cells. Exp Cell Res 2012, 318:489-499. 10.1016/j.yexcr.2011.11.004, 22100912.
62. Sastre-Serra J, Nadal-Serrano M, Pons DG, Roca P, Oliver J. Mitochondrial dynamics is affected by 17β-estradiol in the MCF-7 breast cancer cell line. Effects on fusion and fission related genes. Int J Biochem Cell Biol 2012, 44:1901-1905. 10.1016/j.biocel.2012.07.012, 22824300.
63. Ghoussaini M, Fletcher O, Michailidou K, Turnbull C, Schmidt MK, Dicks E, Dennis J, Wang Q, Humphreys MK, Luccarini C, Baynes C, Conroy D, Maranian M, Ahmed S, Driver K, Johnson N, Orr N, Dos Santos Silva I, Waisfisz Q, Meijers-Heijboer H, Uitterlinden AG, Rivadeneira F, Hall P, Czene K, Irwanto A, Liu J, Nevanlinna H, Aittomäki K, Blomqvist C, Meindl A, Schmutzler RK, , et al. Netherlands Collaborative Group on Hereditary Breast and Ovarian Cancer (HEBON) Genome-wide association analysis identifies three new breast cancer susceptibility loci. Nat Genet 2012, 44:312-318. 10.1038/ng.1049, 3653403, 22267197, Netherlands Collaborative Group on Hereditary Breast and Ovarian Cancer (HEBON).
64. Xu J, Pope SD, Jazirehi AR, Attema JL, Papathanasiou P, Watts JA, Zaret KS, Weissman IL, Smale ST. Pioneer factor interactions and unmethylated CpG dinucleotides mark silent tissue-specific enhancers in embryonic stem cells. Proc Natl Acad Sci U S A 2007, 104:12377-12382. 10.1073/pnas.0704579104, 1941477, 17640912.
65. Lupien M, Eeckhoute J, Meyer CA, Wang Q, Zhang Y, Li W, Carroll JS, Liu XS, Brown M. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 2008, 132:958-970. 10.1016/j.cell.2008.01.018, 2323438, 18358809.
66. Hurtado A, Holmes KA, Ross-Innes CS, Schmidt D, Carroll JS. FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat Genet 2011, 43:27-33. 10.1038/ng.730, 3024537, 21151129.
67. Augello MA, Hickey TE, Knudsen KE. FOXA1: master of steroid receptor function in cancer. EMBO J 2011, 30:3885-3894. 10.1038/emboj.2011.340, 3209791, 21934649.
68. Kong SL, Li G, Loh SL, Sung WK, Liu ET. Cellular reprogramming by the conjoint action of ERalpha, FOXA1, and GATA3 to a ligand-inducible growth state. Mol Syst Biol 2011, 7:526. 3202798, 21878914.
69. Fu X, Huang C, Schiff R. More on FOX News: FOXA1 on the horizon of estrogen receptor function and endocrine response. Breast Cancer Res 2011, 13:307. 10.1186/bcr2849, 3219191, 21575280.