MicroRNA-519a is a novel oncomir conferring tamoxifen resistance by targeting a network of tumour-suppressor genes in ER+ breast cancer

Journal of Pathology

Volumn 233, Issue 4, 2014, Pages 368-379

  Ward, Aoife ^a   Shukla, Kirti ^a   Balwierz, Aleksandra ^a   Soons, Zita ^a,d   König, Rainer ^a,b,c   Sahin, Özgür ^a,e   Wiemann, Stefan ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b JENA UNIVERSITY HOSPITAL   (Germany)

^c HANS KNÖLL INSTITUTE   (Germany)

^d MAASTRICHT UNIVERSITY   (Netherlands)

^e BILKENT UNIVERSITY   (Turkey)

Author keywords

breast cancer; C19MC cluster; cell cycle network; microRNAs; tamoxifen resistance

Indexed keywords

ESTROGEN RECEPTOR ALPHA; MICRORNA; MICRORNA 519A; PHOSPHATIDYLINOSITOL 3 KINASE; SMALL UNTRANSLATED RNA; TAMOXIFEN; UNCLASSIFIED DRUG;

ALGORITHM; APOPTOSIS; ARTICLE; BREAST CANCER; CELL CYCLE PROGRESSION; CELL VIABILITY; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE SPECIFIC SURVIVAL; ESTROGEN RECEPTOR POSITIVE BREAST CANCER; GAIN OF FUNCTION MUTATION; GENE CONTROL; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; LOSS OF FUNCTION MUTATION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TUMOR SUPPRESSOR GENE;

BREAST CANCER; C19MC CLUSTER; CELL CYCLE NETWORK; MICRORNAS; TAMOXIFEN RESISTANCE;

ANTINEOPLASTIC AGENTS, HORMONAL; APOPTOSIS; BREAST NEOPLASMS; CELL CYCLE; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; HUMANS; MICRORNAS; PHARMACOGENETICS; PHOSPHATIDYLINOSITOL 3-KINASES; SIGNAL TRANSDUCTION; TAMOXIFEN; TUMOR MARKERS, BIOLOGICAL;

EID: 84904259547     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4363     Document Type: Article

References (44)

1. Vargo-Gogola T, Rosen JM,. Modelling breast cancer: one size does not fit all. Nature Rev Cancer 2007; 7: 659-672.
2. Jordan VC, Murphy CS,. Endocrine pharmacology of antiestrogens as antitumor agents. Endocr Rev 1990; 11: 578-610.
3. Katzenellenbogen BS, Miller MA, Mullick A, et al., Antiestrogen action in breast cancer cells: modulation of proliferation and protein synthesis, and interaction with estrogen receptors and additional antiestrogen binding sites. Breast Cancer Res Treat 1985; 5: 231-243.
4. Ring A, Dowsett M,. Mechanisms of tamoxifen resistance. Endocr Relat Cancer 2004; 11: 643-658.
5. Shiau AK, Barstad D, Loria PM, et al., The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell 1998; 95: 927-937.
6. Thiantanawat A, Long BJ, Brodie AM,. Signaling pathways of apoptosis activated by aromatase inhibitors and antiestrogens. Cancer Res 2003; 63: 8037-8050.
7. Hui R, Finney GL, Carroll JS, et al., Constitutive overexpression of cyclin D1 but not cyclin E confers acute resistance to antiestrogens in T-47D breast cancer cells. Cancer Res 2002; 62: 6916-6923.
8. Shou J, Massarweh S, Osborne CK, et al., Mechanisms of tamoxifen resistance: increased estrogen receptor-HER2/neu cross-talk in ER/HER2-positive breast cancer. J Natl Cancer Inst 2004; 96: 926-935.
9. Gonzalez-Malerva L, Park J, Zou L, et al., High-throughput ectopic expression screen for tamoxifen resistance identifies an atypical kinase that blocks autophagy. Proc Natl Acad Sci U S A 2011; 108: 2058-2063.
10. Rodriguez A, Griffiths-Jones S, Ashurst JL, et al., Identification of mammalian microRNA host genes and transcription units. Genome Res 2004; 14: 1902-1910.
11. Ma J, Dong C, Ji C,. MicroRNA and drug resistance. Cancer Gene Ther 2010; 17: 523-531.
12. Ward A, Balwierz A, Zhang JD, et al., Re-expression of microRNA-375 reverses both tamoxifen resistance and accompanying EMT-like properties in breast cancer. Oncogene 2013; 32: 1173-1182.
13. Miller TE, Ghoshal K, Ramaswamy B, et al., MicroRNA-221/222 confers tamoxifen resistance in breast cancer by targeting p27Kip1. J Biol Chem 2008; 283: 29897-29903.
14. Baek D, Villen J, Shin C, et al., The impact of microRNAs on protein output. Nature 2008; 455: 64-71.
15. Uhlmann S, Mannsperger H, Zhang JD, et al., Global microRNA level regulation of EGFR-driven cell-cycle protein network in breast cancer. Mol Syst Biol 2012; 8: 570.
16. Uhlmann S, Zhang JD, Schwager A, et al., miR-200bc/429 cluster targets PLCgamma1 and differentially regulates proliferation and EGF-driven invasion than miR-200a/141 in breast cancer. Oncogene 2010; 29: 4297-4306.
17. 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.
18. Phuong NT, Kim SK, Lim SC, et al., Role of PTEN promoter methylation in tamoxifen-resistant breast cancer cells. Breast Cancer Res Treat 2011; 130: 73-83.
19. Riccardi C, Nicoletti I,. Analysis of apoptosis by propidium iodide staining and flow cytometry. Nature Protoc 2006; 1: 1458-1461.
20. Dweep H, Sticht C, Pandey P, et al., miRWalk-database: prediction of possible miRNA binding sites by 'walking' the genes of three genomes. J Biomed Inform 2011; 44: 839-847.
21. Kozomara A, Griffiths-Jones S,. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 2011; 39: D152-D157.
22. Flor I, Bullerdiek J,. The dark side of a success story: microRNAs of the C19MC cluster in human tumours. J Pathol 2012; 227: 270-274.
23. Huang da W, Sherman BT, Lempicki RA,. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009; 37: 1-13.
24. Miller TW, Balko JM, Arteaga CL,. Phosphatidylinositol 3-kinase and antiestrogen resistance in breast cancer. J Clin Oncol 2011; 29: 4452-4461.
25. Osborne CK, Schiff R,. Mechanisms of endocrine resistance in breast cancer. Annu Rev Med 2011; 62: 233-247.
26. Buffa FM, Camps C, Winchester L, et al., MicroRNA-associated progression pathways and potential therapeutic targets identified by integrated mRNA and microRNA expression profiling in breast cancer. Cancer Res 2011; 71: 5635-5645.
27. Enerly E, Steinfeld I, Kleivi K, et al., miRNA-mRNA integrated analysis reveals roles for miRNAs in primary breast tumors. PLoS One 2011; 6: e16915.
28. Sahin O, Lobke C, Korf U, et al., Combinatorial RNAi for quantitative protein network analysis. Proc Natl Acad Sci U S A 2007; 104: 6579-6584.
29. Ishwaran H, Kogalur UB, Blackstone EH, et al., Random survival forests. Ann Appl Statistics 2008; 2: 841-860.
30. Curtis C, Shah SP, Chin SF, et al., The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 2012; 486: 346-352.
31. Treeck O, Zhou R, Diedrich K, et al., Tamoxifen long-term treatment in vitro alters the apoptotic response of MCF-7 breast cancer cells. Anticancer Drugs 2004; 15: 787-793.
32. Pfeiler G, Horn F, Lattrich C, et al., Apoptotic effects of signal transduction inhibitors on human tumor cells with different PTEN expression. Oncol Rep 2007; 18: 1305-1309.
33. Kumar R, Mandal M, Lipton A, et al., Overexpression of HER2 modulates bcl-2, bcl-XL, and tamoxifen-induced apoptosis in human MCF-7 breast cancer cells. Clin Cancer Res 1996; 2: 1215-1219.
34. Knight WA, Livingston RB, Gregory EJ, et al., Estrogen receptor as an independent prognostic factor for early recurrence in breast cancer. Cancer Res 1977; 37: 4669-4671.
35. Abdelmohsen K, Srikantan S, Kuwano Y, et al., miR-519 reduces cell proliferation by lowering RNA-binding protein HuR levels. Proc Natl Acad Sci U S A 2008; 105: 20297-20302.
36. Kim TH, Kim YK, Kwon Y, et al., Deregulation of miR-519a, 153, and 485-5p and its clinicopathological relevance in ovarian epithelial tumours. Histopathology 2010; 57: 734-743.
37. Fornari F, Milazzo M, Chieco P, et al., In hepatocellular carcinoma miR-519d is up-regulated by p53 and DNA hypomethylation and targets CDKN1A/p21, PTEN, AKT3 and TIMP2. J Pathol 2012; 227: 275-285.
38. Foekens JA, Sieuwerts AM, Smid M, et al., Four miRNAs associated with aggressiveness of lymph node-negative, estrogen receptor-positive human breast cancer. Proc Natl Acad Sci U S A 2008; 105: 13021-13026.
39. Lyng MB, Laenkholm AV, Sokilde R, et al., Global microRNA expression profiling of high-risk ER + breast cancers from patients receiving adjuvant tamoxifen mono-therapy: a DBCG study. PLoS One 2012; 7: e36170.
40. Abukhdeir AM, Vitolo MI, Argani P, et al., Tamoxifen-stimulated growth of breast cancer due to p21 loss. Proc Natl Acad Sci U S A 2008; 105: 288-293.
41. Wu S, Huang S, Ding J, et al., Multiple microRNAs modulate p21Cip1/Waf1 expression by directly targeting its 3′ untranslated region. Oncogene 2010; 29: 2302-2308.
42. Bosco EE, Wang Y, Xu H, et al., The retinoblastoma tumor suppressor modifies the therapeutic response of breast cancer. J Clin Invest 2007; 117: 218-228.
43. Cittelly DM, Das PM, Spoelstra NS, et al., Downregulation of miR-342 is associated with tamoxifen resistant breast tumors. Mol Cancer 2010; 9: 317.
44. Sahin O, Frohlich H, Lobke C, et al., Modeling ERBB receptor-regulated G1/S transition to find novel targets for de novo trastuzumab resistance. BMC Syst Biol 2009; 3: 1.