Re-expression of microRNA-375 reverses both tamoxifen resistance and accompanying EMT-like properties in breast cancer

Oncogene

Volumn 32, Issue 9, 2013, Pages 1173-1182

  Ward, A ^a   Balwierz, A ^a   Zhang, J D ^a,c   Kublbeck M ^a   Pawitan, Y ^b   Hielscher, T ^a   Wiemann, S ^a   Sahin, O ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b KAROLINSKA INSTITUTE   (Sweden)

^c F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

breast cancer; epithelialmesenchymal transition; metadherin; microRNAs; tamoxifen resistance

Indexed keywords

MESSENGER RNA; MICRORNA 375; TAMOXIFEN;

ARTICLE; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; MICROARRAY ANALYSIS; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION;

BREAST NEOPLASMS; CELL ADHESION MOLECULES; CELL LINE, TUMOR; DISEASE-FREE SURVIVAL; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; NEOPLASM INVASIVENESS; QUINAZOLINES; TAMOXIFEN;

EID: 84874735111     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.128     Document Type: Article

References (36)

1. Vargo-Gogola T, Rosen JM. Modelling breast cancer: one size does not fit all. Nat 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, Sheen YY. 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: 231-543.
4. Ring A, Dowsett M. Mechanisms of tamoxifen resistance. Endocr Relat Cancer. 2004; 11: 643-658.
5. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139: 871-890.
6. Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 2009; 9: 265-273.
7. Miller TE, Ghoshal K, Ramaswamy B, Roy S, Datta J, Shapiro CL et al. MicroRNA- 221/222 confers tamoxifen resistance in breast cancer by targeting p27Kip1. J Biol Chem 2008; 283: 29897-29903.
8. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008; 10: 593-601.
9. Berstein LM, Wang JP, Zheng H, Yue W, Conaway M, Santen RJ. Long-term exposure to tamoxifen induces hypersensitivity to estradiol. Clin Cancer Res 2004; 10: 1530-1534.
10. Shou J, Massarweh S, Osborne CK, Wakeling AE, Ali S, Weiss H 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.
11. Hiscox S, Morgan L, Green TP, Barrow D, Gee J, Nicholson RI. Elevated Src activity promotes cellular invasion and motility in tamoxifen resistant breast cancer cells. Breast Cancer Res Treat 2006; 97: 263-274.
12. Cariou S, Donovan JC, Flanagan WM, Milic A, Bhattacharya N, Slingerland JM. Downregulation of p21WAF1/CIP1 or p27Kip1 abrogates antiestrogen-mediated cell cycle arrest in human breast cancer cells. Proc Natl Acad Sci USA. 2000; 97: 9042-9046.
13. Folkman J, Moscona A. Role of cell shape in growth control. Nature 1978; 273: 345-349.
14. de Souza Rocha Simonini P, Breiling A, Gupta N, Malekpour M, Youns M, Omranipour R et al. Epigenetically deregulated microRNA-375 is involved in a positive feedback loop with estrogen receptor alpha in breast cancer cells. Cancer Res 2010; 70: 9175-9184.
15. Mazar J, DeBlasio D, Govindarajan SS, Zhang S, Perera RJ. Epigenetic regulation of microRNA-375 and its role in melanoma development in humans. FEBS Lett 2011; 585: 2467-2476.
16. Blick T, Widodo E, Hugo H, Waltham M, Lenburg ME, Neve RM et al. Epithelial mesenchymal transition traits in human breast cancer cell lines. Clin Exp Metastasis 2008; 25: 629-642.
17. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, Fevr T et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006; 10: 515-527.
18. Park SM, Gaur AB, Lengyel E, Peter ME. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 2008; 22: 894-907.
19. Hu G, Chong RA, Yang Q, Wei Y, Blanco MA, Li F et al. MTDH activation by 8q22 genomic gain promotes chemoresistance and metastasis of poor-prognosis breast cancer. Cancer Cell 2009; 15: 9-20.
20. Bergamaschi A, Katzenellenbogen BS. Tamoxifen downregulation of miR-451 increases 14-3-3zeta and promotes breast cancer cell survival and endocrine resistance. Oncogene 2012; 31: 39-47.
21. Kim MR, Choi HK, Cho KB, Kim HS, Kang KW. Involvement of Pin1 induction in epithelial-mesenchymal transition of tamoxifen-resistant breast cancer cells. Cancer Sci 2009; 100: 1834-1841.
22. Eger A, Aigner K, Sonderegger S, Dampier B, Oehler S, Schreiber M et al. DeltaEF1 is a transcriptional repressor of E-cadherin and regulates epithelial plasticity in breast cancer cells. Oncogene 2005; 24: 2375-2385.
23. Hiscox S, Jiang WG, Obermeier K, Taylor K, Morgan L, Burmi R et al. Tamoxifen resistance in MCF7 cells promotes EMT-like behaviour and involves modulation of beta-catenin phosphorylation. Int J Cancer 2006; 118: 290-301.
24. Li Y, VandenBoom 2nd TG, Kong D, Wang Z, Ali S, Philip PA et al. Up-regulation of miR-200 and let-7 by natural agents leads to the reversal of epithelial-tomesenchymal transition in gemcitabine-resistant pancreatic cancer cells. Cancer Res 2009; 69: 6704-6712.
25. Sun L, Yao Y, Liu B, Lin Z, Lin L, Yang M et al. MiR-200b and miR-15b regulate chemotherapy-induced epithelial-mesenchymal transition in human tongue cancer cells by targeting BMI1. Oncogene 2012; 31: 432-445.
26. Tsukamoto Y, Nakada C, Noguchi T, Tanigawa M, Nguyen LT, Uchida T et al. MicroRNA-375 is downregulated in gastric carcinomas and regulates cell survival by targeting PDK1 and 14-3-3zeta. Cancer Res 2010; 70: 2339-2349.
27. Ladeiro Y, Couchy G, Balabaud C, Bioulac-Sage P, Pelletier L, Rebouissou S et al. MicroRNA profiling in hepatocellular tumors is associated with clinical features and oncogene/tumor suppressor gene mutations. Hepatology 2008; 47: 1955-1963.
28. Kong KL, Kwong DL, Chan TH, Law SY, Chen L, Li Y et al. MicroRNA-375 inhibits tumour growth and metastasis in oesophageal squamous cell carcinoma through repressing insulin-like growth factor 1 receptor. Gut 2012; 61: 33-42.
29. Li X, Kong X, Huo Q, Guo H, Yan S, Yuan C et al. Metadherin enhances the invasiveness of breast cancer cells by inducing epithelial to mesenchymal transition. Cancer Sci 2011; 102: 1151-1157.
30. Uhlmann S, Zhang JD, Schwager A, Mannsperger H, Riazalhosseini Y, Burmester S 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.
31. Sahin O, Frohlich H, Lobke C, Korf U, Burmester S, Majety M et al. Modeling ERBB receptor-regulated G1/S transition to find novel targets for de novo trastuzumab resistance. BMC Syst Biol 2009; 3: 1.
32. Dweep H, Sticht C, Pandey P, Gretz N. miRWalk - Database: Prediction of possible miRNA binding sites by "walking" the genes of three genomes. J Biomed Inform 2011 14.
33. Enerly E, Steinfeld I, Kleivi K, Leivonen SK, Aure MR, Russnes HG et al. miRNAmRNA integrated analysis reveals roles for miRNAs in primary breast tumors. PLoS One 2011; 6: e16915.
34. Buffa FM, Camps C, Winchester L, Snell CE, Gee HE, Sheldon H et al. microRNAassociated progression pathways and potential therapeutic targets identified by integrated mRNA and microRNA expression profiling in breast cancer. Cancer Res 2011; 71: 5635-5645.
35. Ma XJ, Wang Z, Ryan PD, Isakoff SJ, Barmettler A, Fuller A et al. A two-gene expression ratio predicts clinical outcome in breast cancer patients treated with tamoxifen. Cancer Cell 2004; 5: 607-616.
36. Pawitan Y, Bjohle J, Amler L, Borg AL, Egyhazi S, Hall P et al. Gene expression profiling spares early breast cancer patients from adjuvant therapy: derived and validated in two population-based cohorts. Breast Cancer Res 2005; 7: R953-R964.