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. 2017 Jun 23;19(2):119–128. doi: 10.3233/CBM-160319

MicroRNA in breast cancer: The association with BRCA1/2

Nina Petrovic 1,*, Radoslav Davidovic 1, Vladan Bajic 1, Milan Obradovic 1, R Esma Isenovic 1
PMCID: PMC13020722  PMID: 28128741

Abstract

Breast cancer (BC) is a heterogeneous disease in an urgent need for developing novel research, classification, and therapy approaches. Breast cancer 1 (BRCA1) and breast cancer 2 (BRCA2) proteins are well described tumor suppressors with great potential to be the subjects of different therapies. MicroRNAs (miRNAs) are genetic elements that might be used to solve the complex BC puzzle. BRCA1 was described to be the target of up to 100 miRNAs. BRCA1 may directly repress miR-155 activity. In addition, miR-15/107/182-mediated downregulation of BRCA1 interrupt DNA repair and may change the course of BC therapy. miR-146a and miR-146-5p silencing BRCA1 may trigger formation of triple-negative and basal-like sporadic BC cases. miR-182 might effect the therapy outcome. miR-21 targeted therapy might be useful for the treatment of BRCA2 mutation carriers. miR-342 overexpression and the absence of functional BRCA1 gene might cause synthetic lethality, which might be used as a base for future therapies. The present review discusses the latest data from studies that focus on the complex network of miRNAs and BRCA1/2 related BCs, which might be important for improving the therapy within the patients with triple-negative BC (TNBC) and basal-like BC, and for understanding the formation of TNBC.

Keywords: Breast cancer, miRNA, BRCA1, BRCA2, TNBC

References

  • [1]. Albiges L., André F., Balleyguier C., Gomez-Abuin G., Chompret A. and Delaloge S. (2005). Spectrum of breast cancer metastasis in BRCA1 mutation carriers: Highly increased incidence of brain metastases. Annals of Oncology 16(11): 1846-1847. [DOI] [PubMed] [Google Scholar]
  • [2]. Amir S., Simion C., Umeh-Garcia M., Krig S., Moss T., Carraway Iii K. L., et al. (2016). Regulation of the T-box transcription factor Tbx3 by the tumour suppressor microRNA-206 in breast cancer. Br J Cancer 114(10): 1125-1134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [3]. Aqeilan R. I., Calin G. A. and Croce C. M. (2010). miR-15a and miR-16-1 in cancer: Discovery, function and future perspectives. Cell Death Differ 17(2): 215-220. [DOI] [PubMed] [Google Scholar]
  • [4]. Bajic V., Milicevic Z., Biljana P. S. and Nedeljkovic-Kurepa A. (2003). Apoptotic versus genotoxic potential of anti-tumor agents: A concept of duality in unity. Medical Hypotheses 61(5): 643-650. [PubMed] [Google Scholar]
  • [5]. Bertoli G., Cava C. and Castiglioni I. (2015). MicroRNAs: New biomarkers for diagnosis, prognosis, therapy prediction and therapeutic tools for breast cancer. Theranostics 5(10): 1122-1143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [6]. Bertucci F., Finetti P., Cervera N., Esterni B., Hermitte F., Viens P., et al. (2008). How basal are triple-negative breast cancers? International Journal of Cancer 123(1): 236-240. [DOI] [PubMed] [Google Scholar]
  • [7]. Boukerroucha M., Josse C., ElGuendi S., Boujemla B., Frères P., Marée R., et al. (2015). Evaluation of BRCA1-related molecular features and microRNAs as prognostic factors for triple negative breast cancers. BMC Cancer 15(1): 1-10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [8]. Brewster B. L., Rossiello F., French J. D., Edwards S. L., Wong E. M., Whiley P., et al. (2012). Identification of a novel disease-associated variant in the BRCA1 3'UTR that introduces a functional miR-103 target site. Hereditary Cancer in Clinical Practice 10(Suppl 2): A88-A88. [Google Scholar]
  • [9]. Chang S. and Sharan S. K. (2012). Epigenetic control of an oncogenic microRNA, miR-155, by BRCA1. Oncotarget 3(1): 5-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [10]. Chang S. and Sharan S. K. (2012). BRCA1 and MicroRNAs: Emerging networks and potential therapeutic targets. Molecules and Cells 34(5): 425-432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [11]. Chang S., Wang R.-H., Akagi K., Kim K.-A., Martin B. K., Cavallone L., et al. (2011). Tumor suppressor BRCA1 epigenetically controls oncogenic microRNA-155. Nature Medicine 17(10): 1275-1282. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [12]. Chappuis P. O., Nethercot V. and Foulkes W. D. (2000). Clinico - pathological characteristics of BRCA1- and BRCA2-related breast cancer. Seminars in Surgical Oncology 18(4): 287-295. [DOI] [PubMed] [Google Scholar]
  • [13]. Chen P. S., Su J. L., Cha S. T., Tarn W. Y., Wang M. Y., Hsu H. C., et al. (2011). miR-107 promotes tumor progression by targeting the let-7 microRNA in mice and humans. Journal of Clinical Investigation 121(9): 3442-3455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [14]. Choi Y. E., Pan Y., Park E., Konstantinopoulos P., De S., D'Andrea A., et al. (2014). MicroRNAs down-regulate homologous recombination in the G1 phase of cycling cells to maintain genomic stability. eLife 3: e02445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [15]. Crippa E., Folini M., Pennati M., Zaffaroni N., Pierotti M. A. and Gariboldi M. (2016). miR-342 overexpression results in a synthetic lethal phenotype in BRCA1-mutant HCC1937 breast cancer cells. Oncotarget 7(14): 18594-18604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [16]. Crippa E., Lusa L., De Cecco L., Marchesi E., Calin G. A., Radice P., et al. (2014). miR-342 regulates BRCA1 expression through modulation of ID4 in breast cancer. PLoS ONE 9(1). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [17]. Da Silva L. and Lakhani S. R. (2010). Pathology of hereditary breast cancer. Modern Pathology 23: S46-S51. [DOI] [PubMed] [Google Scholar]
  • [18]. Dai X., Li T., Bai Z., Yang Y., Liu X., Zhan J., et al. (2015). Breast cancer intrinsic subtype classification, clinical use and future trends. American Journal of Cancer Research 5(10): 2929-2943. [PMC free article] [PubMed] [Google Scholar]
  • [19]. Davies O. R. and Pellegrini L. (2007). Interaction with the BRCA2 C terminus protects RAD51-DNA filaments from disassembly by BRC repeats. Nat Struct Mol Biol 14(6): 475-483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [20]. Davis B. N. and Hata A. (2009). Regulation of MicroRNA biogenesis: A miRiad of mechanisms. Cell Communication and Signaling 7(1): 1-22. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [21]. De Summa S., Pinto R., Pilato B., Sambiasi D., Porcelli L., Guida G., et al. (2014). Expression of base excision repair key factors and miR17 in familial and sporadic breast cancer. Cell Death & Disease 5(2): e1076. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [22]. Djuranovic S., Nahvi A. and Green R. (2012). miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 336(6078): 237-240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [23]. Dong G., Liang X., Wang D., Gao H., Wang L., Wang L., et al. (2014). High expression of miR-21 in triple-negative breast cancers was correlated with a poor prognosis and promoted tumor cell in vitro proliferation. Medical Oncology 31(7): 1-10. [DOI] [PubMed] [Google Scholar]
  • [24]. Esashi F., Galkin V. E., Yu X., Egelman E. H. and West S. C. (2007). Stabilization of RAD51 nucleoprotein filaments by the C-terminal region of BRCA2. Nat Struct Mol Biol 14(6): 468-474. [DOI] [PubMed] [Google Scholar]
  • [25]. Fkih M'hamed I., Privat M., Ponelle F., Penault-Llorca F., Kenani A. and Bignon Y.-J. (2015). Identification of miR-10b, miR-26a, miR-146a and miR-153 as potential triple-negative breast cancer biomarkers. Cellular Oncology 1-10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [26]. Futaki, M. and Liu, J. M. (2001). Chromosomal breakage syndromes and the BRCA1 genome surveillance complex. Trends in Molecular Medicine 7(12): 560-565. [DOI] [PubMed] [Google Scholar]
  • [27]. Garcia A. I., Buisson M., Bertrand P., Rimokh R., Rouleau E., Lopez B. S., et al. (2011). Down-regulation of BRCA1 expression by miR-146a and miR-146b-5p in triple negative sporadic breast cancers. EMBO Mol Med 3(5): 279-290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [28]. Gotte M. (2010). MicroRNAs in breast cancer pathogenesis. Minerva Ginecol 62(6): 559-571. [PubMed] [Google Scholar]
  • [29]. Hannemann J., Velds A., Halfwerk J. B. G., Kreike B., Peterse J. L. and van de Vijver M. J. (2006). Classification of ductal carcinoma in situ by gene expression profiling. Breast Cancer Research 8(5): R61-R61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [30]. Hausser J., Syed A. P., Selevsek N., van Nimwegen E., Jaskiewicz L., Aebersold R., et al. (2013). Timescales and bottlenecks in miRNA-dependent gene regulation. Molecular Systems Biology 9: 711-711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [31]. Iorio M. V. (2005). MicroRNA gene expression deregulation in human breast cancer. Cancer Research 65(16): 7065-7070. [DOI] [PubMed] [Google Scholar]
  • [32]. Jansson M. D. and Lund A. H. (2012). MicroRNA and cancer. Molecular Oncology 6(6): 590-610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [33]. Kaelin W. G. (2005). The concept of synthetic lethality in the context of anticancer therapy. Nat Rev Cancer 5(9): 689-698. [DOI] [PubMed] [Google Scholar]
  • [34]. Khvorova A., Reynolds A. and Jayasena S. D. (2003). Functional siRNAs and miRNAs exhibit strand bias. Cell 115(2): 209-216. [DOI] [PubMed] [Google Scholar]
  • [35]. Kim V. N. (2005). MicroRNA biogenesis: Coordinated cropping and dicing. Nat Rev Mol Cell Biol 6(5): 376-385. [DOI] [PubMed] [Google Scholar]
  • [36]. Kim Y. K., Kim B. and Kim V. N. (2016). Re-evaluation of the roles of DROSHA, Exportin 5, and DICER in microRNA biogenesis. Proc Natl Acad Sci USA 113(13): E1881-1889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [37]. Krützfeldt J. and Stoffel M. (2006). MicroRNAs: A new class of regulatory genes affecting metabolism. Cell Metabolism 4(1): 9-12. [DOI] [PubMed] [Google Scholar]
  • [38]. Lakhani S. R., Jacquemier J., Sloane J. P., Gusterson B. A., Anderson T. J., van de Vijver M. J., et al. (1999). Pathology of hereditary breast cancer in patients with BRCA1, BRCA2 & BRCAX mutations. Laboratory Investigation 79(1): 25a-25a. [Google Scholar]
  • [39]. Le Quesne J. and Caldas C. (2010). Micro-RNAs and breast cancer. Molecular Oncology 4(3): 230-241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [40]. Lehmann U. (2014). Aberrant DNA methylation of microRNA genes in human breast cancer - a critical appraisal. Cell and Tissue Research 356(3): 657-664. [DOI] [PubMed] [Google Scholar]
  • [41]. Lewis B. P., Burge C. B. and Bartel D. P. (2005). Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120(1): 15-20. [DOI] [PubMed] [Google Scholar]
  • [42]. Li X.-R., Chu H.-J., Lv T., Wang L., Kong S.-F. and Dai S.-Z. (2014). miR-342-3p suppresses proliferation, migration and invasion by targeting FOXM1 in human cervical cancer. Febs Letters 588(17): 3298-3307. [DOI] [PubMed] [Google Scholar]
  • [43]. MacKenzie T. A., Schwartz G. N., Calderone H. M., Graveel C. R., Winn M. E., Hostetter G., et al. (2014). Stromal expression of miR-21 identifies high-risk group in triple-negative breast cancer. The American Journal of Pathology 184(12): 3217-3225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [44]. Malvezzi M., Bertuccio P., Levi F., La Vecchia C. and Negri E. (2014). European cancer mortality predictions for the year 2014. Annals of Oncology. [DOI] [PubMed] [Google Scholar]
  • [45]. Malvezzi M., Bertuccio P., Rosso T., Rota M., Levi F., La Vecchia C., et al. (2015). European cancer mortality predictions for the year 2015: does lung cancer have the highest death rate in EU women? Annals of Oncology 26(4): 779-786. [DOI] [PubMed] [Google Scholar]
  • [46]. Martello G., Rosato A., Ferrari F., Manfrin A., Cordenonsi M., Dupont S., et al. (2010). A MicroRNA targeting dicer for metastasis control. Cell 141(7): 1195-1207. [DOI] [PubMed] [Google Scholar]
  • [47]. Mayer I. A., Abramson V. G., Lehmann B. D. and Pietenpol J. A. (2014). New strategies for triple-negative breast cancer - deciphering the heterogeneity. American Association for Cancer Research 20(4): 782-790. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [48]. Medimegh I., Omrane I., Privat M., Uhrhummer N., Ayari H., Belaiba F., et al. (2014). MicroRNAs expression in triple negative vs non triple negative breast cancer in tunisia: Interaction with clinical outcome. PLoS ONE 9(11): e111877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [49]. Millikan R. C., Newman B., Tse C.-K., Moorman P. G., Conway K., Smith L. V., et al. (2008). Epidemiology of basal-like breast cancer. Breast Cancer Research and Treatment 109(1): 123-139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [50]. Mogilyansky E. and Rigoutsos I. (2013). The miR-17/92 cluster: A comprehensive update on its genomics, genetics, functions and increasingly important and numerous roles in health and disease. Cell Death Differ 20(12): 1603-1614. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [51]. Moskwa P., Buffa F. M., Pan Y., Panchakshari R., Gottipati P., Muschel R. J., et al. (2011). miR-182-mediated downregulation of BRCA1 impacts DNA repair and sensitivity to PARP inhibitors. Molecular Cell 41(2): 210-220. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [52]. Murphy C. G. and Moynahan M. E. (2010). BRCA gene structure and function in tumor suppression: A repair-centric perspective. Cancer Journal 16(1): 39-47. [DOI] [PubMed] [Google Scholar]
  • [53]. Nelson P. T., Wang W.-X. and Rajeev B. W. (2008). MicroRNAs (miRNAs) in neurodegenerative diseases. Brain Pathology 18(1): 130-138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [54]. Palacios J., Honrado E., Osorio A., Cazorla A., Sarrió D., Barroso A., et al. (2005). Phenotypic characterization of BRCA1 and BRCA2 tumors based in a tissue microarray study with 37 immunohistochemical markers. Breast Cancer Research and Treatment 90(1): 5-14. [DOI] [PubMed] [Google Scholar]
  • [55]. Pastrello C., Polesel J., Della Puppa L., Viel A. and Maestro R. (2010). Association between hsa-mir-146a genotype and tumor age-of-onset in BRCA1/BRCA2-negative familial breast and ovarian cancer patients. Carcinogenesis 31(12): 2124-2126. [DOI] [PubMed] [Google Scholar]
  • [56]. Pellegrini L., Yu D. S., Lo T., Anand S., Lee M., Blundell T. L., et al. (2002). Insights into DNA recombination from the structure of a RAD51-BRCA2 complex. Nature 420(6913): 287-293. [DOI] [PubMed] [Google Scholar]
  • [57]. Petrovic N. (2016). miR-21 might be involved in breast cancer promotion and invasion rather than in initial events of breast cancer development. Molecular Diagnosis & Therapy 1-14. [DOI] [PubMed] [Google Scholar]
  • [58]. Petrovic N., Kolakovic A., Stankovic A., Lukic S., Sami A., Zivkovic M., et al. (2016). miR-155 expression level changes might be associated with initial phases of breast cancer pathogenesis and lymph-node metastasis. Cancer Biomark. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [59]. Petrovic N., Mandusic V., Stanojevic B., Lukic S., Todorovic L., Roganovic J., et al. (2014). The difference in miR-21 expression levels between invasive and non-invasive breast cancers emphasizes its role in breast cancer invasion. Medical Oncology 31(3). [DOI] [PubMed] [Google Scholar]
  • [60]. Polyak K. (2007). Breast cancer: Origins and evolution. Journal of Clinical Investigation 117(11): 3155-3163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [61]. Quann K., Jing Y. and Rigoutsos I. (2015). Post-transcriptional regulation of BRCA1 through its coding sequence by the miR-15/107 group of miRNAs. Frontiers in Genetics 6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [62]. Rajewsky N. (2006). microRNA target predictions in animals. Nature Genetics 38(6s): S8-S13. [DOI] [PubMed] [Google Scholar]
  • [63]. Reyisdottir S. T., Reynisdottir S. T., Stefansson O. A., Bödvarsdottir S. K., Palsson A. and Eyfjörd J. E. (2016). Abstract A33: Expression of BRCA2 and Mir-21 in sporadic and BRCA2 mutated breast cancer in Iceland. Molecular Cancer Research 14(2 Supplement): A33. [Google Scholar]
  • [64]. Ross J. S., Carlson J. A. and Brock G. (2007). miRNA the new gene silencer. American Journal of Clinical Pathology 128(5): 830-836. [DOI] [PubMed] [Google Scholar]
  • [65]. Shaver T. M., Lehmann B. D., Beeler J. S., Li C.-I., Li Z., Jin H., et al. (2016). Diverse, biologically relevant, and targetable gene rearrangements in triple-negative breast cancer and other malignancies. Cancer Research. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [66]. Shen J., Ambrosone C. B., DiCioccio R. A., Odunsi K., Lele S. B. and Zhao H. (2008). A functional polymorphism in the miR-146a gene and age of familial breast/ovarian cancer diagnosis. Carcinogenesis 29(10): 1963-1966. [DOI] [PubMed] [Google Scholar]
  • [67]. Shen J., Ambrosone C. B. and Zhao H. (2009). Novel genetic variants in microRNA genes and familial breast cancer. International Journal of Cancer 124(5): 1178-1182. [DOI] [PubMed] [Google Scholar]
  • [68]. Shin V. Y., Siu J. M., Cheuk I., Ng E. K. O. and Kwong A. (2015). Circulating cell-free miRNAs as biomarker for triple-negative breast cancer. Br J Cancer 112(11): 1751-1759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [69]. Shukla V., Coumoul X., Lahusen T., Wang R.-H., Xu X., Vassilopoulos A., et al. (2010). BRCA1 affects global DNA methylation through regulation of DNMT1. Cell Res 20(11): 1201-1215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [70]. Song B., Wang C., Liu J., Wang X., Lv L., Wei L., et al. (2010). Micro-RNA-21 regulates breast cancer invasion partly by targetingtissue inhibitor of metalloproteinase 3 expression. J Exp ClinCancer Res 29(1): 29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [71]. Song L., Dai T., Xie Y., Wang C., Lin C., Wu Z., et al. (2012). Up-regulation of miR-1245 by c-myc targets BRCA2 and impairs DNA repair. Journal of Molecular Cell Biology 4(2): 108-117. [DOI] [PubMed] [Google Scholar]
  • [72]. Srihari S., Singla J., Wong L. and Ragan M. A. (2015). Inferring synthetic lethal interactions from mutual exclusivity of genetic events in cancer. Biology Direct 10(1): 1-18. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [73]. Tan X., Peng J., Fu Y., An S., Rezaei K., Tabbara S., et al. (2014). miR-638 mediated regulation of BRCA1affects DNA repair and sensitivity to UV and cisplatin in triple-negative breast cancer. Breast Cancer Research 16(5): 1-14. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [74]. Tang J., Ahmad A. and Sarkar F. H. (2012). The role of MicroRNAs in breast cancer migration, invasion and metastasis. International Journal of Molecular Sciences 13(12): 13414-13437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [75]. Tanic M., Yanowski K., Gómez-López G., Socorro Rodriguez-Pinilla M., Marquez-Rodas I., Osorio A., et al. (2015). MicroRNA expression signatures for the prediction of BRCA1/2 mutation-associated hereditary breast cancer in paraffin-embedded formalin-fixed breast tumors. International Journal of Cancer 136(3): 593-602. [DOI] [PubMed] [Google Scholar]
  • [76]. Tanic M., Zajac M., Gómez-López G., Benítez J. and Martínez-Delgado B. (2012). Integration of BRCA1-mediated miRNA and mRNA profiles reveals microRNA regulation of TRAF2 and NFκ B pathway. Breast Cancer Research and Treatment 134(1): 41-51. [DOI] [PubMed] [Google Scholar]
  • [77]. Tili E., Croce C. M. and Michaille J.-J. (2009). miR-155: On the crosstalk between inflammation and cancer. International Reviews of Immunology 28(5): 264-284. [DOI] [PubMed] [Google Scholar]
  • [78]. Tomaskovic-Crook E., Thompson E. W. and Thiery J. (2009). Epithelial to mesenchymal transition and breast cancer. Breast Cancer Research 11(6): 213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [79]. Torre L. A., Bray F., Siegel R. L., Ferlay J., Lortet-Tieulent J. and Jemal A. (2015). Global cancer statistics, 2012. CA: A Cancer Journal for Clinicians 65(2): 87-108. [DOI] [PubMed] [Google Scholar]
  • [80]. Turner N., Tutt A. and Ashworth A. (2004). Hallmarks of `BRCAness' in sporadic cancers. Nat Rev Cancer 4(10): 814-819. [DOI] [PubMed] [Google Scholar]
  • [81]. Turner N. C., Reis-Filho J. S., Russell A. M., Springall R. J., Ryder K., Steele D., et al. (2006). BRCA1 dysfunction in sporadic basal-like breast cancer. Oncogene 26(14): 2126-2132. [DOI] [PubMed] [Google Scholar]
  • [82]. Tutt A., Connor F., Bertwistle D., Kerr P., Peacock J., Ross G., et al. (2003). Cell cycle and genetic background dependence of the effect of loss of BRCA2 on ionizing radiation sensitivity. Oncogene 22(19): 2926-2931. [DOI] [PubMed] [Google Scholar]
  • [83]. Valinezhad Orang A., Safaralizadeh R. and Kazemzadeh-Bavili M. (2014). Mechanisms of miRNA-mediated gene regulation from common downregulation to mRNA-specific upregulation. International Journal of Genomics 2014: 1-15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [84]. van der Groep P., Bouter A., van der Zanden R., Siccama I., Menko F. H., Gille J. J. P., et al. (2006). Distinction between hereditary and sporadic breast cancer on the basis of clinicopathological data. Journal of Clinical Pathology 59(6): 611-617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [85]. Vasudevan S. (2012). Posttranscriptional Upregulation by MicroRNAs. Wiley Interdisciplinary Reviews: RNA 3(3): 311-330. [DOI] [PubMed] [Google Scholar]
  • [86]. Vimalraj S., Miranda P. J., Ramyakrishna B. and Selvamurugan N. (2013). Regulation of breast cancer and bone metastasis by MicroRNAs. Disease Markers 35(5): 19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [87]. Vos S., Vesuna F., Raman V., van Diest P. J. and van der Groep P. (2015). miRNA expression patterns in normal breast tissue and invasive breast cancers of BRCA1 and BRCA2 germ-line mutation carriers. Oncotarget 6(31): 32115-32137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [88]. Wahid F., Shehzad A., Khan T. and Kim Y. Y. (2010). MicroRNAs: Synthesis, mechanism, function, and recent clinical trials. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 1803(11): 1231-1243. [DOI] [PubMed] [Google Scholar]
  • [89]. Weber B. L. (1998). Update on Breast Cancer Susceptibility Genes. Adjuvant Therapy of Primary Breast Cancer VI. Senn H.-J., Gelber R. D., Goldhirsch A. and Thürlimann B. Berlin, Heidelberg, Springer Berlin Heidelberg: 49-59.
  • [90]. Weigelt B. and Reis-Filho J. S. (2009). Histological and molecular types of breast cancer: Is there a unifying taxonomy? Nat Rev Clin Oncol 6(12): 718-730. [DOI] [PubMed] [Google Scholar]
  • [91]. Yan L.-X., Huang X.-F., Shao Q., Huang M. A. Y., Deng L., Wu Q.-L., et al. (2008). MicroRNA miR-21 overexpression in human breast cancer is associated with advanced clinical stage, lymph node metastasis and patient poor prognosis. Rna 14(11): 2348-2360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [92]. Yang Z., He M., Wang K., Sun G., Tang L. and Xu Z. (2014). Tumor suppressive microRNA-193b promotes breast cancer progression via targeting DNAJC13 and RAB22A. International Journal of Clinical and Experimental Pathology 7(11): 7563-7570. [PMC free article] [PubMed] [Google Scholar]
  • [93]. Yao E. and Ventura A. (2011). A new role for miR-182 in DNA repair. Molecular Cell 41(2): 135-137. [DOI] [PubMed] [Google Scholar]
  • [94]. Zeng Y. and Cullen B. R. (2004). Structural requirements for pre-microRNA binding and nuclear export by Exportin 5. Nucleic Acids Res 32. [DOI] [PMC free article] [PubMed] [Google Scholar]

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