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A comprehensive review on oncogenic miRNAs in breast cancer

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Abstract

A growing body of evidence demonstrates that the oncogenic miRNAs are critical components that are involved in breast cancer (BC) progression. Thus, they are attracting a great deal of consideration as they provide opportunities for the novel avenues for developing BC targeted therapy. In the current review, we try to discuss the key oncogenic miRNAs implicated in cell migration, invasion and metastasis (e.g., miR-9, miR-10b, miR-10b-5p, miR-17/9, miR-21, miR-103/107, miR-181b-1, miR-301, miR-301a, miR-373, miR-489, miR-495 and miR-520c), apoptosis inhibition (e.g., miR-21, miR-155, miR-181, miR-182 and miR-221/222), cell proliferation (e.g., miR-221/222, miR-17/92, miR-21, miR-301a, miR-155, miR-181 b, miR-182, miR-214, miR-20b, miR-29a, miR-196, miR-199a-3p, miR-210, miR-301a, miR-375, miR-378-3p and miR-489), and angiogenesis (e.g., miR-9, miR-17/92 cluster, miR-93 and miR-210). In particular, here, we considered miRNA‐based therapeutic approaches to summarize the evidence for their potential therapeutic uses in clinical practice. Therefore, miRNA mimics (i.e., replacement and restoration of miRNAs) and inhibition therapy (e.g., anti‐miRNA oligonucleotides (AMO), antagomiRs or antisense oligonucleotides (ASOs): cholesterol-conjugated anti-miRs and locked nucleic acid (LNA)), miRNA sponges, nanoparticles (NPs), multiple-target anti-mirna antisense oligonucleotide technology (MTg-AMOs), and artificial miRNAs (amiRNAs) have been indicated throughout the article as much as possible.

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References

  • Ahmadzada T., Reid G. and McKenzie D. R. 2018 Fundamentals of siRNA and miRNA therapeutics and a review of targeted nanoparticle delivery systems in breast cancer. Biophys. Rev. 10, 69–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alshalalfa M., Bader G. D., Goldenberg A., Morris Q. and Alhajj R. 2012 Detecting microRNAs of high influence on protein functional interaction networks: a prostate cancer case study. BMC Syst. Biol. 6, 112.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baar J., Silverman P., Lyons J., Fu P., Abdul-Karim F., Ziats N. et al. 2009 A vasculature-targeting regimen of preoperative docetaxel with or without bevacizumab for locally advanced breast cancer: impact on angiogenic biomarkers. Clin. Cancer Res. 15, 3583–3590.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bader A. G., Brown D. and Winkler M. 2010 The promise of microRNA replacement therapy. Cancer Res. 70, 7027–7030.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bak R. O. and Mikkelsen J. G. 2014 miRNA sponges: soaking up miRNAs for regulation of gene expression. Wiley Interdiscip. Rev. RNA 5, 317–333.

    Article  CAS  PubMed  Google Scholar 

  • Baldassarre G., Battista S., Belletti B., Thakur S., Pentimalli F., Trapasso F. et al. 2003 Negative regulation of BRCA1 gene expression by HMGA1 proteins accounts for the reduced BRCA1 protein levels in sporadic breast carcinoma. Mol. Cell. Biol. 23, 2225–2238.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bar I., Merhi A., Abdel-Sater F., Ben Addi A., Sollennita S., Canon J.-L. et al. 2017 The MicroRNA miR-210 is expressed by cancer cells but also by the tumour microenvironment in triple-negative breast Cancer. J. Histochem. Cytochem. 65, 335–346.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbano R., Pasculli B., Rendina M., Fontana A., Fusilli C., Copetti M. et al. 2017 Stepwise analysis of MIR9 loci identifies miR-9-5p to be involved in Oestrogen regulated pathways in breast cancer patients. Sci. Rep. 7, 1–12.

    Article  Google Scholar 

  • Baroni S., Romero-Cordoba S., Plantamura I., Dugo M., D’ippolito E., Cataldo A. et al. 2016 Exosome-mediated delivery of miR-9 induces cancer-associated fibroblast-like properties in human breast fibroblasts. Cell Death Dis. 7, e2312–e2312.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bavelloni A., Ramazzotti G., Poli A., Piazzi M., Focaccia E., Blalock W. et al. 2017 MiRNA-210: a current overview. Anticancer Res. 37, 6511–6521.

    CAS  PubMed  Google Scholar 

  • Bisso A., Faleschini M., Zampa F., Capaci V., De Santa J., Santarpia L. et al. 2013 Oncogenic miR-181a/b affect the DNA damage response in aggressive breast cancer. Cell Cycle 12, 1679–1687.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouyssou J. M., Manier S., Huynh D., Issa S., Roccaro A. M. and Ghobrial I. M. 2014 Regulation of microRNAs in cancer metastasis. BBA-Rev. Cancer 1845, 255–265.

    CAS  Google Scholar 

  • Bueno M. J., de Castro I. P. and Malumbres M. 2008 Control of cell proliferation pathways by microRNAs. Cell Cycle 7, 3143–3148.

    Article  CAS  PubMed  Google Scholar 

  • Buscaglia L. E. B. and Li Y. 2011 Apoptosis and the target genes of microRNA-21. Chin. J. Cancer 30, 371.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao M., Nie W., Li J., Zhang Y., Yan X., Guan X. et al. 2014 MicroRNA-495 induces breast cancer cell migration by targeting JAM-A. Protein Cell 5, 862–872.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cascio S., D’Andrea A., Ferla R., Surmacz E., Gulotta E., Amodeo V. et al. 2010 miR-20b modulates VEGF expression by targeting HIF-1α and STAT3 in MCF-7 breast cancer cells. J. Cell. Physiol. 224, 242–249.

    CAS  PubMed  Google Scholar 

  • Cassavaugh J. M., Hale S. A., Wellman T. L., Howe A. K., Wong C. and Lounsbury K. M. 2011 Negative regulation of HIF-1α by an FBW7-mediated degradation pathway during hypoxia. J. Cell. Biochem. 112, 3882–3890.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castellano L., Giamas G., Jacob J., Coombes R. C., Lucchesi W., Thiruchelvam P. et al. 2009 The estrogen receptor-α-induced microRNA signature regulates itself and its transcriptional response. Proc. Natl. Acad. Sci. USA 106, 15732–15737.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castelli D. D., Terreno E., Cabella C., Chaabane L., Lanzardo S., Tei L. et al. 2009 Evidence for in vivo macrophage mediated tumor uptake of paramagnetic/fluorescent liposomes. NMR Biomed. 22, 1084–1092.

    Article  PubMed  Google Scholar 

  • Ceteci F., Ceteci S., Karreman C., Kramer B. W., Asan E., Götz R. et al. 2007 Disruption of tumor cell adhesion promotes angiogenic switch and progression to micrometastasis in RAF-driven murine lung cancer. Cancer Cell 12, 145–159.

    Article  CAS  PubMed  Google Scholar 

  • Chalhoub N. and Baker S. J. 2009 PTEN and the PI3-kinase pathway in cancer. Annu. Rev. Pathol.-Mech. Dis. 4, 127–150.

    Article  CAS  Google Scholar 

  • Chamorro-Jorganes A., Lee M. Y., Araldi E., Landskroner-Eiger S., Fernández-Fuertes M., Sahraei M. et al. 2016 VEGF-induced expression of miR-17–92 cluster in endothelial cells is mediated by ERK/ELK1 activation and regulates angiogenesis. Circ. Res. 118, 38–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang S. and Sharan S. K. 2012 BRCA1 and microRNAs: emerging networks and potential therapeutic targets. Mol. Cell. 34, 425–432.

    Article  CAS  Google Scholar 

  • 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. Nat. Med. 17, 1275.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen H.-Y., Lin Y.-M., Chung H.-C., Lang Y.-D., Lin C.-J., Huang J. et al. 2012 miR-103/107 promote metastasis of colorectal cancer by targeting the metastasis suppressors DAPK and KLF4. Cancer Res. 72, 3631–3641.

    Article  CAS  PubMed  Google Scholar 

  • Chen H., Wang X., Bai J. and He A. 2017a Expression, regulation and function of miR-495 in healthy and tumor tissues. Oncol. Lett. 13, 2021–2026.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. J. Clin. Invest. 121, 3442.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y., Gao D.-Y. and Huang L. 2015 In vivo delivery of miRNAs for cancer therapy: challenges and strategies. Adv. Drug Deliv. Rev. 81, 128–141.

    Article  CAS  PubMed  Google Scholar 

  • Chen Y., Luo D., Tian W., Li Z. and Zhang X. 2017b Demethylation of miR-495 inhibits cell proliferation, migration and promotes apoptosis by targeting STAT-3 in breast cancer. Oncol. Rep. 37, 3581–3589.

    Article  CAS  PubMed  Google Scholar 

  • Chiang C.-H., Chu P.-Y., Hou M.-F. and Hung W.-C. 2016 MiR-182 promotes proliferation and invasion and elevates the HIF-1α-VEGF-A axis in breast cancer cells by targeting FBXW7. Am. J. Cancer Res. 6, 1785.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ciruelos E., Pascual T., Vozmediano M. L. A., Blanco M., Manso L., Parrilla L. et al. 2014 The therapeutic role of fulvestrant in the management of patients with hormone receptor-positive breast cancer. Breast 23, 201–208.

    Article  PubMed  Google Scholar 

  • Conde J., Edelman E. R. and Artzi N. 2015 Target-responsive DNA/RNA nanomaterials for microRNA sensing and inhibition: The jack-of-all-trades in cancer nanotheranostics? Adv. Drug Deliv. Rev. 81, 169–183.

    Article  CAS  PubMed  Google Scholar 

  • Covello K. L., Kehler J., Yu H., Gordan J. D., Arsham A. M., Hu C.-J. et al. 2006 HIF-2α regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev. 20, 557–570.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Rinaldis E., Gazinska P., Mera A., Modrusan Z., Fedorowicz G. M., Burford B. et al. 2013 Integrated genomic analysis of triple-negative breast cancers reveals novel microRNAs associated with clinical and molecular phenotypes and sheds light on the pathways they control. BMC Genom. 14, 643.

    Article  Google Scholar 

  • Dentelli P., Traversa M., Rosso A., Togliatto G., Olgasi C., Marchio C. et al. 2014 miR-221/222 control luminal breast cancer tumor progression by regulating different targets. Cell Cycle 13, 1811–1826.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Derksen P. W., Liu X., Saridin F., van der Gulden H., Zevenhoven J., Evers B. et al. 2006 Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 10, 437–449.

    Article  CAS  PubMed  Google Scholar 

  • Devulapally R., Sekar N. M., Sekar T. V., Foygel K., Massoud T. F., Willmann J. R. K. et al. 2015 Polymer nanoparticles mediated codelivery of antimiR-10b and antimiR-21 for achieving triple negative breast cancer therapy. ACS Nano 9, 2290–2302.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Leva G., Gasparini P., Piovan C., Ngankeu A., Garofalo M., Taccioli C. et al. 2010 MicroRNA cluster 221–222 and estrogen receptor α interactions in breast cancer. JNCI J. Natl. Cancer Inst. 102, 706–721.

    Article  PubMed  Google Scholar 

  • Edmonds M. D., Hurst D. R., Vaidya K. S., Stafford L. J., Chen D. and Welch D. R. 2009 Breast cancer metastasis suppressor 1 coordinately regulates metastasis-associated microRNA expression. Int. J. Cancer 125, 1778–1785.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Essex S., Navarro G., Sabhachandani P., Chordia A., Trivedi M., Movassaghian S. et al. 2015 Phospholipid-modified PEI-based nanocarriers for in vivo siRNA therapeutics against multidrug-resistant tumors. Gene Ther. 22, 257–266.

    Article  PubMed  Google Scholar 

  • Fang L., Deng Z., Shatseva T., Yang J., Peng C., Du W. et al. 2011 MicroRNA miR-93 promotes tumor growth and angiogenesis by targeting integrin-β8. Oncogene 30, 806.

    Article  CAS  PubMed  Google Scholar 

  • Fang L., Du W. W., Yang W., Rutnam Z. J., Peng C., Li H. et al. 2012 MiR-93 enhances angiogenesis and metastasis by targeting LATS2. Cell Cycle 11, 4352–4365.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fasanaro P., D’Alessandra Y., Di Stefano V., Melchionna R., Romani S., Pompilio G. et al. 2008 MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J. Biol. Chem. 283, 15878–15883.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flügel D., Görlach A. and Kietzmann T. 2012 GSK-3β regulates cell growth, migration, and angiogenesis via Fbw7 and USP28-dependent degradation of HIF-1α. Blood 119, 1292–1301.

    Article  PubMed  PubMed Central  Google Scholar 

  • Frankel L. B., Christoffersen N. R., Jacobsen A., Lindow M., Krogh A. and Lund A. H. 2008 Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J. Biol. Chem. 283, 1026–1033.

    Article  CAS  PubMed  Google Scholar 

  • Gan R., Yang Y., Yang X., Zhao L., Lu J. and Meng Q. H. 2014 Downregulation of miR-221/222 enhances sensitivity of breast cancer cells to tamoxifen through upregulation of TIMP 3. Cancer Gene Ther. 21, 290–296.

    Article  CAS  PubMed  Google Scholar 

  • Garofalo M., Di Leva G., Romano G., Nuovo G., Suh S.-S., Ngankeu A. et al. 2009 miR-221and 222 regulate TRAIL resistance and enhance tumorigenicity through PTEN and TIMP3 downregulation. Cancer Cell 16, 498–509.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garofalo M., Quintavalle C., Romano G., Croce C. M. and Condorelli G. 2012 miR221/222 in cancer: their role in tumor progression and response to therapy. Curr. Mol. Med. 12, 27–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gillies J. K. and Lorimer I. A. 2007 Regulation of p27Kip1 by miRNA 221/222 in glioblastoma. Cell Cycle 6, 2005–2009.

    Article  CAS  PubMed  Google Scholar 

  • Goh J. N., Loo S. Y., Datta A., Siveen K. S., Yap W. N., Cai W. et al. 2016 microRNAs in breast cancer: regulatory roles governing the hallmarks of cancer. Biol. Rev. 91, 409–428.

    Article  PubMed  Google Scholar 

  • Gong C., Nie Y., Qu S., Liao J.-Y., Cui X., Yao H. et al. 2014 miR-21 induces myofibroblast differentiation and promotes the malignant progression of breast phyllodes tumors. Cancer Res. 74, 4341–4352.

    Article  CAS  PubMed  Google Scholar 

  • Gramantieri L., Fornari F., Ferracin M., Veronese A., Sabbioni S., Calin G. A. et al. 2009 MicroRNA-221 targets Bmf in hepatocellular carcinoma and correlates with tumor multifocality. Clin. Cancer Res. 15, 5073–5081.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guttilla I. K. and White B. A. 2009 Coordinate regulation of FOXO1 by miR-27a, miR-96, and miR-182 in breast cancer cells. J. Biol. Chem. 284, 23204–23216.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gwak J. M., Kim H. J., Kim E. J., Chung Y. R., Yun S., Seo A. N. et al. 2014 MicroRNA-9 is associated with epithelial-mesenchymal transition, breast cancer stem cell phenotype, and tumor progression in breast cancer. Breast Cancer Res. Treat. 147, 39–49.

    Article  CAS  PubMed  Google Scholar 

  • Han M., Liu M., Wang Y., Chen X., Xu J., Sun Y. et al. 2012 Antagonism of miR-21 reverses epithelial-mesenchymal transition and cancer stem cell phenotype through AKT/ERK1/2 inactivation by targeting PTEN. PLoS One 7, e39520.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han X., Yan S., Weijie Z., Feng W., Liuxing W., Mengquan L. et al. 2014 Critical role of miR-10b in transforming growth factor-β1-induced epithelial–mesenchymal transition in breast cancer. Cancer Gene Ther. 21, 60–67.

    Article  PubMed  Google Scholar 

  • Heddleston J. M., Li Z., McLendon R. E., Hjelmeland A. B. and Rich J. N. 2009 The hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotype. Cell Cycle 8, 3274–3284.

    Article  CAS  PubMed  Google Scholar 

  • Hesari A., Azizian M., Darabi H., Nesaei A., Hosseini S. A., Salarinia R. et al. 2019 Expression of circulating miR-17, miR-25, and miR-133 in breast cancer patients. J. Cell. Biochem. 120, 7109–7114.

    Article  CAS  Google Scholar 

  • Hosseinahli N., Aghapour M., Duijf P. H. and Baradaran B. 2018 Treating cancer with microRNA replacement therapy: a literature review. J. Cell. Physiol. 233, 5574–5588.

    Article  CAS  PubMed  Google Scholar 

  • Howe E. N., Cochrane D. R. and Richer J. K. 2012 The miR-200 and miR-221/222 microRNA families: opposing effects on epithelial identity. J. Mam. Gland Biol. Neoplas. 17, 65–77.

    Article  Google Scholar 

  • Huang D. W., Sherman B. T. and Lempicki R. A. 2009a Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1–13.

    Article  Google Scholar 

  • Huang Q., Gumireddy K., Schrier M., Le Sage C., Nagel R., Nair S. et al. 2008 The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat. Cell Biol. 10, 202–210.

    Article  CAS  PubMed  Google Scholar 

  • Huang T.-H., Wu F., Loeb G. B., Hsu R., Heidersbach A., Brincat A. et al. 2009b Up-regulation of miR-21 by HER2/neu signaling promotes cell invasion. J. Biol. Chem. 284, 18515–18524.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang X. and Zuo J. 2014 Emerging roles of miR-210 and other non-coding RNAs in the hypoxic response. Acta Biochim. Biophys. Sin. 46, 220–232.

    Article  CAS  PubMed  Google Scholar 

  • Hwang M. S., Yu N., Stinson S. Y., Yue P., Newman R. J., Allan B. B. et al. 2013 miR-221/222 targets adiponectin receptor 1 to promote the epithelial-to-mesenchymal transition in breast cancer. PLoS One 8, e66502.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang-Verslues W., Chang P., Wei P., Yang C., Huang C., Kuo W. et al. 2011 miR-495 is upregulated by E12/E47 in breast cancer stem cells, and promotes oncogenesis and hypoxia resistance via downregulation of E-cadherin and REDD1. Oncogene 30, 2463–2474.

    Article  CAS  PubMed  Google Scholar 

  • Iranshahi N., Zafari P., Yari K. H. and Alizadeh E. 2016 The most common genes involved in epigenetics modifications among Iranian patients with breast cancer: a systematic review. Cell Mol. Biol. 62, 116–122.

    CAS  PubMed  Google Scholar 

  • Ito Y., Motoo Y., Yoshida H., Iovanna J. L., Takamura Y., Miya A. et al. 2006 Decreased expression of tumor protein p53-induced nuclear protein 1 (TP53INP1) in breast carcinoma. Anticancer Res. 26, 4391–4395.

    CAS  PubMed  Google Scholar 

  • Jha P., Agrawal R., Pathak P., Kumar A., Purkait S., Mallik S. et al. 2015 Genome-wide small noncoding RNA profiling of pediatric high-grade gliomas reveals deregulation of several mi RNAs, identifies downregulation of sno RNA cluster HBII-52 and delineates H3F3A and TP53 mutant-specific mi RNAs and sno RNAs. Int. J. Cancer 137, 2343–2353.

    Article  CAS  PubMed  Google Scholar 

  • Ji W., Sun B. and Su C. 2017 Targeting microRNAs in cancer gene therapy. Genes 8, 21.

    Article  PubMed Central  Google Scholar 

  • Jiang S., Zhang H.-W., Lu M.-H., He X.-H., Li Y., Gu H. et al. 2010 MicroRNA-155 functions as an OncomiR in breast cancer by targeting the suppressor of cytokine signaling 1 gene. Cancer Res. 70, 3119–3127.

    Article  CAS  PubMed  Google Scholar 

  • Jiang S., Zhang L. F., Zhang H. W., Hu S., Lu M. H., Liang S. et al. 2012 A novel miR-155/miR-143 cascade controls glycolysis by regulating hexokinase 2 in breast cancer cells. EMBO J. 31, 1985–1998.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiao X., Zhao L., Ma M., Bai X., He M., Yan Y. et al. 2013 MiR-181a enhances drug sensitivity in mitoxantone-resistant breast cancer cells by targeting breast cancer resistance protein (BCRP/ABCG2). Breast Cancer Res. Treat. 139, 717–730.

    Article  CAS  PubMed  Google Scholar 

  • Jin L., Lim M., Zhao S., Sano Y., Simone B. A., Savage J. E. et al. 2014 The metastatic potential of triple-negative breast cancer is decreased via caloric restriction-mediated reduction of the miR-17~92 cluster. Breast Cancer Res. Treat. 146, 41–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin Y.-Y., Andrade J. and Wickstrom E. 2015 Non-specific blocking of miR-17-5p guide strand in triple negative breast cancer cells by amplifying passenger strand activity. PLoS One 10, e0142574.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kabilova T. O., Meschaninova M. I., Venyaminova A. G., Nikolin V. P., Zenkova M. A., Vlassov V. V. et al. 2012 Short double-stranded RNA with immunostimulatory activity: sequence dependence. Nucleic Acid Ther. 22, 196–204.

    Article  CAS  PubMed  Google Scholar 

  • Kaboli P. J., Rahmat A., Ismail P. and Ling K.-H. 2015 MicroRNA-based therapy and breast cancer: a comprehensive review of novel therapeutic strategies from diagnosis to treatment. Pharmacol. Res. 97, 104–121.

    Article  CAS  PubMed  Google Scholar 

  • Keklikoglou I., Koerner C., Schmidt C., Zhang J., Heckmann D., Shavinskaya A. et al. 2012 MicroRNA-520/373 family functions as a tumor suppressor in estrogen receptor negative breast cancer by targeting NF-κB and TGF-β signaling pathways. Oncogene 31, 4150–4163.

    Article  CAS  PubMed  Google Scholar 

  • Kim K., Chadalapaka G., Lee S., Yamada D., Sastre-Garau X., Defossez P.-A. et al. 2012 Identification of oncogenic microRNA-17-92/ZBTB4/specificity protein axis in breast cancer. Oncogene 31, 1034–1044.

    Article  CAS  PubMed  Google Scholar 

  • Kong W., Yang H., He L., Zhao J.-J., Coppola D., Dalton W. S. et al. 2008 MicroRNA-155 is regulated by the transforming growth factor β/Smad pathway and contributes to epithelial cell plasticity by targeting RhoA. Mol. Cell. Biol. 28, 6773–6784.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kota S. K. and Balasubramanian S. 2010 Cancer therapy via modulation of micro RNA levels: a promising future. Drug Discov. Today 15, 733–740.

    Article  CAS  PubMed  Google Scholar 

  • Kumar M. S., Lu J., Mercer K. L., Golub T. R. and Jacks T. 2007 Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat. Genet. 39, 673–677.

    Article  CAS  PubMed  Google Scholar 

  • Le Sage C., Nagel R., Egan D. A., Schrier M., Mesman E., Mangiola A. et al. 2007 Regulation of the p27Kip1 tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO J. 26, 3699–3708.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lehmann S. M., Krüger C., Park B., Derkow K., Rosenberger K., Baumgart J. et al. 2012 An unconventional role for miRNA: let-7 activates Toll-like receptor 7 and causes neurodegeneration. Nat. Neurosci. 15, 827.

    Article  CAS  PubMed  Google Scholar 

  • Lennox K. and Behlke M. 2011 Chemical modification and design of anti-miRNA oligonucleotides. Gene Ther. 18, 1111–1120.

    Article  CAS  PubMed  Google Scholar 

  • Lettlova S., Brynychova V., Blecha J., Vrana D., Vondrusova M., Soucek P. et al. 2018 MiR-301a-3p suppresses estrogen signaling by directly inhibiting ESR1 in ERα positive breast cancer. Cell. Physiol. Biochem. 46, 2601–2615.

    Article  CAS  PubMed  Google Scholar 

  • Li B., Lu Y., Yu L., Han X., Wang H., Mao J. et al. 2017a miR-221/222 promote cancer stem-like cell properties and tumor growth of breast cancer via targeting PTEN and sustained Akt/NF-κB/COX-2 activation. Chem.-Biol. Interact. 277, 33–42.

    Article  CAS  PubMed  Google Scholar 

  • Li C., Li L. and Keates A. C. 2012 Targeting cancer gene therapy with magnetic nanoparticles. Oncotarget 3, 365.

    Article  PubMed  PubMed Central  Google Scholar 

  • Li D., Ilnytskyy Y., Kovalchuk A., Khachigian L. M., Bronson R. T., Wang B. et al. 2013a Crucial role for early growth response-1 in the transcriptional regulation of miR-20b in breast cancer. Oncotarget 4, 1373.

    Article  PubMed  PubMed Central  Google Scholar 

  • Li H., Bian C., Liao L., Li J. and Zhao R. C. 2011 miR-17-5p promotes human breast cancer cell migration and invasion through suppression of HBP1. Breast Cancer Res. Treat. 126, 565–575.

    Article  CAS  PubMed  Google Scholar 

  • Li J., Lai Y., Ma J., Liu Y., Bi J., Zhang L. et al. 2017b miR-17-5p suppresses cell proliferation and invasion by targeting ETV1 in triple-negative breast cancer. BMC Cancer 17, 745.

    Article  PubMed  PubMed Central  Google Scholar 

  • Li X., Xu F., Chang C., Byon J., Papayannopoulou T., Deeg H. J. et al. 2013b Transcriptional regulation of miR-10a/b by TWIST-1 in myelodysplastic syndromes. Haematologica 98, 414–419.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y., Kuscu C., Banach A., Zhang Q., Pulkoski-Gross A., Kim D. et al. 2015 miR-181a-5p inhibits cancer cell migration and angiogenesis via downregulation of matrix metalloproteinase-14. Cancer Res. 75, 2674–2685.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang Y.-K., Lin H.-Y., Dou X.-W., Chen M., Wei X.-L., Zhang Y.-Q. et al. 2018 MiR-221/222 promote epithelial-mesenchymal transition by targeting Notch3 in breast cancer cell lines. NPJ Breast Cancer 4, 1–9.

    Article  Google Scholar 

  • Liang Z., Wu H., Reddy S., Zhu A., Wang S., Blevins D. et al. 2007 Blockade of invasion and metastasis of breast cancer cells via targeting CXCR4 with an artificial microRNA. Biochem. Biophys. Res. Commun. 363, 542–546.

    Article  CAS  PubMed  Google Scholar 

  • Liu H., Wang Y., Li X., Zhang Y.-J., Li J., Zheng Y.-Q. et al. 2013 Expression and regulatory function of miRNA-182 in triple-negative breast cancer cells through its targeting of profilin 1. Tumor Biol. 34, 1713–1722.

    Article  CAS  Google Scholar 

  • Liu P. and Wilson M. J. 2012 miR-520c and miR-373 upregulate MMP9 expression by targeting mTOR and SIRT1, and activate the Ras/Raf/MEK/Erk signaling pathway and NF-κB factor in human fibrosarcoma cells. J. Cell. Physiol. 227, 867–876.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu R., Li H., Liu L., Yu J. and Ren X. 2012 Fibroblast activation protein: A potential therapeutic target in cancer. Cancer Biol. Ther. 13, 123–129.

    Article  PubMed  Google Scholar 

  • Liu S., Goldstein R. H., Scepansky E. M. and Rosenblatt M. 2009 Inhibition of rho-associated kinase signaling prevents breast cancer metastasis to human bone. Cancer Res. 69, 8742–8751.

    Article  CAS  PubMed  Google Scholar 

  • Liu S., Wang Z., Liu Z., Shi S., Zhang Z., Zhang J. et al. 2018 miR-221/222 activate the Wnt/β-catenin signaling to promote triple-negative breast cancer. J. Mol. Cell Biol. 10, 302–315.

    Article  CAS  PubMed  Google Scholar 

  • Lu J., Getz G., Miska E. A., Alvarez-Saavedra E., Lamb J., Peck D. et al. 2005 MicroRNA expression profiles classify human cancers. Nature 435, 834–838.

    Article  CAS  PubMed  Google Scholar 

  • Luengo-Gil G., González-Billalabeitia E., Chaves-Benito A., Martínez E. G., Garre E. G., Vicente V. et al. 2015 Effects of conventional neoadjuvant chemotherapy for breast cancer on tumor angiogenesis. Breast Cancer Res. Treat. 151, 577–587.

    Article  CAS  PubMed  Google Scholar 

  • Luengo-Gil G., Gonzalez-Billalabeitia E., Perez-Henarejos S. A., Manzano E. N., Chaves-Benito A., Garcia-Martinez E. et al. 2018 Angiogenic role of miR-20a in breast cancer. PLoS One 13, e0194638.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma F., Zhang J., Zhong L., Wang L., Liu Y., Wang Y. et al. 2014 Upregulated microRNA-301a in breast cancer promotes tumor metastasis by targeting PTEN and activating Wnt/β-catenin signaling. Gene 535, 191–197.

    Article  CAS  PubMed  Google Scholar 

  • Ma L. 2010 Role of miR-10b in breast cancer metastasis. Breast Cancer Res. 12, 210.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma L., Reinhardt F., Pan E., Soutschek J., Bhat B., Marcusson E. G. et al. 2010a Therapeutic silencing of miR-10b inhibits metastasis in a mouse mammary tumor model. Nat. Biotechnol. 28, 341.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma L., Teruya-Feldstein J. and Weinberg R. A. 2007 Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449, 682–688.

    Article  CAS  PubMed  Google Scholar 

  • Ma L., Young J., Prabhala H., Pan E., Mestdagh P., Muth D. et al. 2010b miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat. Cell Biol. 12, 247–256.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma X., Kumar M., Choudhury S. N., Buscaglia L. E. B., Barker J. R., Kanakamedala K. et al. 2011 Loss of the miR-21 allele elevates the expression of its target genes and reduces tumorigenesis. Proce. Natl. Acad. Sci. USA 108, 10144–10149.

    Article  CAS  Google Scholar 

  • Mandal C. C., Ghosh-Choudhury T., Dey N., Choudhury G. G. and Ghosh-Choudhury N. 2012 miR-21 is targeted by omega-3 polyunsaturated fatty acid to regulate breast tumor CSF-1 expression. Carcinogenesis 33, 1897–1908.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mani S. A., Yang J., Brooks M., Schwaninger G., Zhou A., Miura N. et al. 2007 Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers. Proce. Natl. Acad. Sci. USA 104, 10069–10074.

    Article  CAS  Google Scholar 

  • Mansueto G., Forzati F., Ferraro A., Pallante P., Bianco M., Esposito F. et al. 2010 Identification of a new pathway for tumor progression: MicroRNA-181b up-regulation and CBX7 down-regulation by HMGA1 protein. Genes Cancer 1, 210–224.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martello G., Rosato A., Ferrari F., Manfrin A., Cordenonsi M., Dupont S. et al. 2010 A MicroRNA targeting dicer for metastasis control. Cell 141, 1195–1207.

    Article  CAS  PubMed  Google Scholar 

  • Mattiske S., Suetani R. J., Neilsen P. M. and Callen D. F. 2012 The oncogenic role of miR-155 in breast cancer. Cancer Epidemiol. Biomark. Prev. 21, 1236–1243.

    Article  CAS  Google Scholar 

  • McCormick F. 2001 Cancer gene therapy: fringe or cutting edge? Nat. Rev. Cancer 1, 130–141.

    Article  CAS  PubMed  Google Scholar 

  • McDermott A. M., Miller N., Wall D., Martyn L. M., Ball G., Sweeney K. J. et al. 2014 Identification and validation of oncologic miRNA biomarkers for luminal A-like breast cancer. PLoS One 9, e87032.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mehrgou A. and Akouchekian M. 2017 Therapeutic impacts of microRNAs in breast cancer by their roles in regulating processes involved in this disease. J. Res. Med. Sci. 22, 130.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mohammadi-Yeganeh S., Mansouri A. and Paryan M. 2015 Targeting of miR9/NOTCH1 interaction reduces metastatic behavior in triple-negative breast cancer. Chem. Biol. Drug Des. 86, 1185–1191.

    Article  CAS  PubMed  Google Scholar 

  • Mollaei H., Safaralizadeh R. and Rostami Z. 2019 MicroRNA replacement therapy in cancer. J. Cell. Physiol. 234, 12369–12384.

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee A., Di Bisceglie A. M. and Ray R. B. 2015 Hepatitis C virus-mediated enhancement of microRNA miR-373 impairs the JAK/STAT signaling pathway. J. Virol. 89, 3356–3365.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munagala R., Aqil F., Vadhanam M. V. and Gupta R. C. 2013 MicroRNA ‘signature’ during estrogen-mediated mammary carcinogenesis and its reversal by ellagic acid intervention. Cancer Lett. 339, 175–184.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nedaeinia R., Sharifi M., Avan A., Kazemi M., Rafiee L., Ghayour-Mobarhan M. et al. 2016 Locked nucleic acid anti-miR-21 inhibits cell growth and invasive behaviors of a colorectal adenocarcinoma cell line: LNA-anti-miR as a novel approach. Cancer Gene Ther. 23, 246–253.

    Article  CAS  PubMed  Google Scholar 

  • Neel J.-C. and Lebrun J.-J. 2013 Activin and TGFβ regulate expression of the microRNA-181 family to promote cell migration and invasion in breast cancer cells. Cell. Signal. 25, 1556–1566.

    Article  CAS  PubMed  Google Scholar 

  • Nieto M. A. 2011 The ins and outs of the epithelial to mesenchymal transition in health and disease. Ann. Rev. Cell Dev. Biol. 27, 347–376.

    Article  CAS  Google Scholar 

  • Niu J., Xue A., Chi Y., Xue J., Wang W., Zhao Z. et al. 2016 Induction of miRNA-181a by genotoxic treatments promotes chemotherapeutic resistance and metastasis in breast cancer. Oncogene 35, 1302–1313.

    Article  CAS  PubMed  Google Scholar 

  • Noh H., Hong S., Dong Z., Pan Z. K., Jing Q. and Huang S. 2011 Impaired microRNA processing facilitates breast cancer cell invasion by upregulating urokinase-type plasminogen activator expression. Genes Cancer 2, 140–150.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nygaard S., Jacobsen A., Lindow M., Eriksen J., Balslev E., Flyger H. et al. 2009 Identification and analysis of miRNAs in human breast cancer and teratoma samples using deep sequencing. BMC Med. Genomics 2, 35.

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Bryan S., Dong S., Mathis J. M. and Alahari S. K. 2017 The roles of oncogenic miRNAs and their therapeutic importance in breast cancer. Eur. J. Cancer 72, 1–11.

    Article  CAS  PubMed  Google Scholar 

  • Ouchida M., Kanzaki H., Ito S., Hanafusa H., Jitsumori Y., Tamaru S. et al. 2012 Novel direct targets of miR-19a identified in breast cancer cells by a quantitative proteomic approach. PLoS One 7, e44095.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pallante P., Federico A., Berlingieri M. T., Bianco M., Ferraro A., Forzati F. et al. 2008 Loss of the CBX7 gene expression correlates with a highly malignant phenotype in thyroid cancer. Cancer Res. 68, 6770–6778.

    Article  CAS  PubMed  Google Scholar 

  • Paul P., Chakraborty A., Sarkar D., Langthasa M., Rahman M., Bari M. et al. 2018 Interplay between miRNAs and human diseases. J. Cell. Physiol. 233, 2007–2018.

    Article  CAS  PubMed  Google Scholar 

  • Poliseno L., Salmena L., Zhang J., Carver B., Haveman W. J. and Pandolfi P. P. 2010 A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 465, 1033–1038.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prud’homme G. J., Glinka Y., Toulina A., Ace O., Subramaniam V. and Jothy S. 2010 Breast cancer stem-like cells are inhibited by a non-toxic aryl hydrocarbon receptor agonist. PLoS One 5, e13831.

    Article  PubMed  PubMed Central  Google Scholar 

  • Qiao Y., Jiang X., Lee S. T., Karuturi R. M., Hooi S. C. and Yu Q. 2011 FOXQ1 regulates epithelial-mesenchymal transition in human cancers. Cancer Res. 71, 3076–3086.

    Article  CAS  PubMed  Google Scholar 

  • Raemdonck K., Vandenbroucke R. E., Demeester J., Sanders N. N. and De Smedt S. C. 2008 Maintaining the silence: reflections on long-term RNAi. Drug Discov. Today 13, 917–931.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rao X., Di Leva G., Li M., Fang F., Devlin C., Hartman-Frey C. et al. 2011 MicroRNA-221/222 confers breast cancer fulvestrant resistance by regulating multiple signaling pathways. Oncogene 30, 1082–1097.

    Article  CAS  PubMed  Google Scholar 

  • Ren C.-X., Leng R.-X., Fan Y.-G., Pan H.-F., Wu C.-H. and Ye D.-Q. 2016 MicroRNA-210 and its theranostic potential. Expert Opin. Biol. Ther. 20, 1325–1338.

    Article  CAS  Google Scholar 

  • Rice L., Waters C. E., Eccles J., Garside H., Sommer P., Kay P. et al. 2008 Identification and functional analysis of SKA2 interaction with the glucocorticoid receptor. J. Endocrinol. 198, 499.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robertson N. M. and Yigit M. V. 2014 The role of microRNA in resistance to breast cancer therapy. Wiley Interdiscip. Rev. RNA 5, 823–833.

    Article  CAS  PubMed  Google Scholar 

  • Roese-Koerner B., Stappert L., Berger T., Braun N. C., Veltel M., Jungverdorben J. et al. 2016 Reciprocal regulation between bifunctional miR-9/9∗ and its transcriptional modulator notch in human neural stem cell self-renewal and differentiation. Stem Cell Rep. 7, 207–219.

    Article  CAS  Google Scholar 

  • Roth J. A. 2006 Adenovirus p53 gene therapy. Expert Opin. Biol. Ther. 6, 55–61.

    Article  CAS  PubMed  Google Scholar 

  • Rothe F., Ignatiadis M., Chaboteaux C., Haibe-Kains B., Kheddoumi N., Majjaj S. et al. 2011 Global microRNA expression profiling identifies MiR-210 associated with tumor proliferation, invasion and poor clinical outcome in breast cancer. PLoS One 6, e20980.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rupaimoole R. and Slack F. J. 2017 MicroRNA therapeutics: towards a new era for the management of cancer and other diseases. Nat. Rev. Drug Discov. 16, 203.

    Article  CAS  PubMed  Google Scholar 

  • Santolla M. F., Lappano R., Cirillo F., Rigiracciolo D. C., Sebastiani A., Abonante S. et al. 2018 miR-221 stimulates breast cancer cells and cancer-associated fibroblasts (CAFs) through selective interference with the A20/c-Rel/CTGF signaling. J. Exp. Clin. Cancer Res. 37, 94.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sherman B. T. and Lempicki R. A. 2009 Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44.

    Article  PubMed  Google Scholar 

  • Shi W., Gerster K., Alajez N. M., Tsang J., Waldron L., Pintilie M. et al. 2011 MicroRNA-301 mediates proliferation and invasion in human breast cancer. Cancer Res. 71, 2926–2937.

    Article  CAS  PubMed  Google Scholar 

  • Si H., Sun X., Chen Y., Cao Y., Chen S., Wang H. et al. 2013 Circulating microRNA-92a and microRNA-21 as novel minimally invasive biomarkers for primary breast cancer. J. Cancer Res. Clin. Oncol. 139, 223–229.

    Article  CAS  PubMed  Google Scholar 

  • Si M., Zhu S., Wu H., Lu Z., Wu F. and Mo Y. 2007 miR-21-mediated tumor growth. Oncogene 26, 2799–2803.

    Article  CAS  PubMed  Google Scholar 

  • Skurk C., Maatz H., Rocnik E., Bialik A., Force T. and Walsh K. 2005 Glycogen-synthase kinase3β/β-catenin axis promotes angiogenesis through activation of vascular endothelial growth factor signaling in endothelial cells. Circ. Res. 96, 308–318.

    Article  CAS  PubMed  Google Scholar 

  • Song B., Wang C., Liu J., Wang X., Lv L., Wei L. et al. 2010 MicroRNA-21 regulates breast cancer invasion partly by targeting tissue inhibitor of metalloproteinase 3 expression. J. Exp. Clin. Cancer Res. 29, 29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stinson S., Lackner M. R., Adai A. T., Yu N., Kim H.-J., O’Brien C. et al. 2011 TRPS1 targeting by miR-221/222 promotes the epithelial-to-mesenchymal transition in breast cancer. Sci. Signal. 4, 41.

    Article  Google Scholar 

  • Stückrath I., Rack B., Janni W., Jäger B., Pantel K. and Schwarzenbach H. 2015 Aberrant plasma levels of circulating miR-16, miR-107, miR-130a and miR-146a are associated with lymph node metastasis and receptor status of breast cancer patients. Oncotarget 6, 13387.

    Article  PubMed  PubMed Central  Google Scholar 

  • Stylianopoulos T. and Jain R. K. 2013 Combining two strategies to improve perfusion and drug delivery in solid tumors. Proc. Natl. Acad. Sci. USA 110, 18632–18637.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suárez Y., Fernández-Hernando C., Yu J., Gerber S. A., Harrison K. D., Pober J. S. et al. 2008 Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proc. Natl. Acad. Sci. USA 105, 14082–14087.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun X., Jiao X., Pestell T., Fan C., Qin S., Mirabelli E. et al. 2014 MicroRNAs and cancer stem cells: the sword and the shield. Oncogene 33, 4967–4977.

    Article  CAS  PubMed  Google Scholar 

  • Sun Y., Wu J., Wu S.-H., Thakur A., Bollig A., Huang Y. et al. 2009 Expression profile of microRNAs in c-Myc induced mouse mammary tumors. Breast Cancer Res. Treat. 118, 185.

    Article  CAS  PubMed  Google Scholar 

  • Tang C.-P., Zhou H.-J., Qin J., Luo Y. and Zhang T. 2017 MicroRNA-520c-3p negatively regulates EMT by targeting IL-8 to suppress the invasion and migration of breast cancer. Oncol. Rep. 38, 3144–3152.

    Article  CAS  PubMed  Google Scholar 

  • Taylor M. A., Sossey-Alaoui K., Thompson C. L., Danielpour D. and Schiemann W. P. 2013 TGF-β upregulates miR-181a expression to promote breast cancer metastasis. J. Clin. Invest. 123, 150–163.

    Article  CAS  PubMed  Google Scholar 

  • Terao M., Fratelli M., Kurosaki M., Zanetti A., Guarnaccia V., Paroni G. et al. 2011 Induction of miR-21 by retinoic acid in estrogen receptor-positive breast carcinoma cells Biological Correlates and Molecular Targets. J. Biol. Chem. 286, 4027–4042.

    Article  CAS  PubMed  Google Scholar 

  • Tian Y., Fu X., Li Q., Wang Y., Fan D., Zhou Q. et al. 2018 MicroRNA-181 serves an oncogenic role in breast cancer via the inhibition of SPRY4. Mol. Med. Rep. 18, 5603–5613.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tomasini R., Samir A. A., Carrier A., Isnardon D., Cecchinelli B., Soddu S. et al. 2003 TP53INP1s and homeodomain-interacting protein kinase-2 (HIPK2) are partners in regulating p53 activity. J. Biol. Chem. 278, 37722–37729.

    Article  CAS  PubMed  Google Scholar 

  • Trang P., Wiggins J. F., Daige C. L., Cho C., Omotola M., Brown D. et al. 2011 Systemic delivery of tumor suppressor microRNA mimics using a neutral lipid emulsion inhibits lung tumors in mice. Mol. Ther. 19, 1116–1122.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tseng C.-W., Huang H.-C., Shih A.C.-C., Chang Y.-Y., Hsu C.-C., Chang J.-Y. et al. 2012 Revealing the anti-tumor effect of artificial miRNA p-27-5p on human breast carcinoma cell line T-47D. Int. J. Mol. Sci. 13, 6352–6369.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Dongen S., Abreu-Goodger C. and Enright A. J. 2008 Detecting microRNA binding and siRNA off-target effects from expression data. Nat. Methods 5, 1023–1025.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vasudev N., Goh V., Juttla J., Thompson V., Larkin J., Gore M. et al. 2013 Changes in tumour vessel density upon treatment with anti-angiogenic agents: relationship with response and resistance to therapy. Br. J. Cancer 109, 1230.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Volinia S., Calin G. A., Liu C.-G., Ambs S., Cimmino A., Petrocca F. et al. 2006 A microRNA expression signature of human solid tumors defines cancer gene targets. Proc. Natl. Acad. Sci. USA 103, 2257–2261.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L., Liu J.-L., Yu L., Liu X.-X., Wu H.-M., Lei F.-Y. et al. 2015a Downregulated miR-45 inhibits the G1-S phase transition by targeting Bmi-1 in breast cancer. Medicine 94, 1.

    Google Scholar 

  • Wang N., Wei L., Huang Y., Wu Y., Su M., Pang X. et al. 2017 miR520c blocks EMT progression of human breast cancer cells by repressing STAT3. Oncol. Rep. 37, 1537–1544.

    Article  CAS  PubMed  Google Scholar 

  • Wang Q.-S., Kong P.-Z., Li X.-Q., Yang F. and Feng Y.-M. 2015b FOXF2 deficiency promotes epithelial-mesenchymal transition and metastasis of basal-like breast cancer. Breast Cancer Res. 17, 30.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y., Yu Y., Tsuyada A., Ren X., Wu X., Stubblefield K. et al. 2011 Transforming growth factor-β regulates the sphere-initiating stem cell-like feature in breast cancer through miRNA-181 and ATM. Oncogene 30, 1470–1480.

    Article  CAS  PubMed  Google Scholar 

  • Wang Z. 2011 The guideline of the design and validation of MiRNA mimics. Methods Mol. Biol. 676, 211–223.

    Article  CAS  PubMed  Google Scholar 

  • Wei F., Cao C., Xu X. and Wang J. 2015 Diverse functions of miR-373 in cancer. J. Transl. Med. 13, 162.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wen D., Danquah M., Chaudhary A. K. and Mahato R. I. 2015 Small molecules targeting microRNA for cancer therapy: Promises and obstacles. J. Control. Release 219, 237–247.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiang D., Shigdar S., Qiao G., Zhou S.-F., Li Y., Wei M. et al. 2015 Aptamer-mediated cancer gene therapy. Curr. Gene Ther. 15, 109–119.

    Article  CAS  PubMed  Google Scholar 

  • Xiao F., Qiu H., Zhou L., Shen X., Yang L. and Ding K. 2013 WSS25 inhibits Dicer, downregulating microRNA-210, which targets Ephrin-A3, to suppress human microvascular endothelial cell (HMEC-1) tube formation. Glycobiology 23, 524–535.

    Article  CAS  PubMed  Google Scholar 

  • Xu S., Witmer P. D., Lumayag S., Kovacs B. and Valle D. 2007 MicroRNA (miRNA) transcriptome of mouse retina and identification of a sensory organ-specific miRNA cluster. J. Biol. Chem. 282, 25053–25066.

    Article  CAS  PubMed  Google Scholar 

  • Yahya S. M. and Elsayed G. H. 2015 A summary for molecular regulations of miRNAs in breast cancer. Clin. Biochem. 48, 388–396.

    Article  CAS  PubMed  Google Scholar 

  • Yan G. R., Xu S. H., Tan Z. L., Liu L. and He Q. Y. 2011a Global identification of miR-373-regulated genes in breast cancer by quantitative proteomics. Proteomics 11, 912–920.

    Article  CAS  PubMed  Google Scholar 

  • Yan L.-X., Huang X.-F., Shao Q., Huang M.-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, 2348–2360.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan L. X., Wu Q. N., Zhang Y., Li Y. Y., Liao D. Z., Hou J. H. et al. 2011b Knockdown of miR-21 in human breast cancer cell lines inhibits proliferation, in vitro migration and in vivo tumor growth. Breast Cancer Res. 13, R2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang C., Tabatabaei S. N., Ruan X. and Hardy P. 2017 The dual regulatory role of MiR-181a in breast cancer. Cell. Physiol. Biochem. 44, 843–856.

    Article  CAS  PubMed  Google Scholar 

  • Yang H.-S., Knies J. L., Stark C. and Colburn N. H. 2003 Pdcd4 suppresses tumor phenotype in JB6 cells by inhibiting AP-1 transactivation. Oncogene 22, 3712–3720.

    Article  CAS  PubMed  Google Scholar 

  • Yang J. and Weinberg R. A. 2008 Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 14, 818–829.

    Article  CAS  PubMed  Google Scholar 

  • Yoo J.-O., Kwak S.-Y., An H.-J., Bae I.-H., Park M.-J. and Han Y.-H. 2016 miR-181b-3p promotes epithelial–mesenchymal transition in breast cancer cells through Snail stabilization by directly targeting YWHAG. Mol. Cell Res. 1863, 1601–1611.

    CAS  Google Scholar 

  • Yu B., Zhao X., Lee L. J. and Lee R. J. 2009 Targeted delivery systems for oligonucleotide therapeutics. AAPS J. 11, 195–203.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu F., Yao H., Zhu P., Zhang X., Pan Q., Gong C. et al. 2007 let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 131, 1109–1123.

    Article  CAS  PubMed  Google Scholar 

  • Yu Z., Wang C., Wang M., Li Z., Casimiro M. C., Liu M. et al. 2008 A cyclin D1/microRNA 17/20 regulatory feedback loop in control of breast cancer cell proliferation. J. Cell Biol. 182, 509–517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang C.-M., Zhao J. and Deng H.-Y. 2013 MiR-155 promotes proliferation of human breast cancer MCF-7 cells through targeting tumor protein 53-induced nuclear protein 1. J. Sci. 20, 79.

    CAS  Google Scholar 

  • Zhang C.-Z., Zhang J.-X., Zhang A.-L., Shi Z.-D., Han L., Jia Z.-F. et al. 2010 MiR-221 and miR-222 target PUMA to induce cell survival in glioblastoma. Mol. Cancer 9, 229.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang J., Yang J., Zhang X., Xu J., Sun Y. and Zhang P. 2018 MicroRNA-10b expression in breast cancer and its clinical association. PLoS One 13, e0192509.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang X., Ma G., Liu J. and Zhang Y. 2017 MicroRNA-182 promotes proliferation and metastasis by targeting FOXF2 in triple-negative breast cancer. Oncol. Lett. 14, 4805–4811.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao Y.-S., Yang W.-C., Xin H.-W., Han J.-X. and Ma S.-G. 2019 MiR-182-5p knockdown targeting PTEN inhibits cell proliferation and invasion of breast cancer cells. Yonsei Med. J. 60, 148–157.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng S.-R., Guo G.-L., Zhai Q., Zou Z.-Y. and Zhang W. 2013 Effects of miR-155 antisense oligonucleotide on breast carcinoma cell line MDA-MB-157 and implanted tumors. Asian Pacific J. Cancer Prev. 14, 2361–2366.

    Article  Google Scholar 

  • Zheng Y., Lv X., Wang X., Wang B., Shao X., Huang Y. et al. 2016 MiR-181b promotes chemoresistance in breast cancer by regulating Bim expression. Oncol. Rep. 35, 683–690.

    Article  CAS  PubMed  Google Scholar 

  • Zhong Z., Yeow W.-S., Zou C., Wassell R., Wang C., Pestell R. G. et al. 2010 Cyclin D1/cyclin-dependent kinase 4 interacts with filamin A and affects the migration and invasion potential of breast cancer cells. Cancer Res. 70, 2105–2114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou A., Diao L., Xu H., Xiao Z.-D., Li J., Zhou H. et al. 2012 β-Catenin/LEF1 transactivates the microRNA-371-373 cluster that modulates the Wnt/β-catenin-signaling pathway. Oncogene 31, 2968–2978.

    Article  CAS  PubMed  Google Scholar 

  • Zhou W., Shi G., Zhang Q., Wu Q., Li B. and Zhang Z. 2014 MicroRNA-20b promotes cell growth of breast cancer cells partly via targeting phosphatase and tensin homologue (PTEN). Cell Biosci. 4, 62.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou X., Zhang J., Jia Q., Ren Y., Wang Y., Shi L. et al. 2010 Reduction of miR-21 induces glioma cell apoptosis via activating caspase 9 and 3. Oncol. Rep. 24, 195–201.

    CAS  PubMed  Google Scholar 

  • Zhu S., Si M.-L., Wu H. and Mo Y.-Y. 2007 MicroRNA-21 targets the tumor suppressor gene tropomyosin 1 (TPM1). J. Biol. Chem. 282, 14328–14336.

    Article  CAS  PubMed  Google Scholar 

  • Zhu Y., Wu J., Li S., Ma R., Cao H., Ji M. et al. 2013 The function role of miR-181a in chemosensitivity to adriamycin by targeting Bcl-2 in low-invasive breast cancer cells. Cell. Physiol. Biochem. 32, 1225–1237.

    Article  CAS  PubMed  Google Scholar 

  • Zong Y., Zhang Y., Sun X., Xu T., Cheng X. and Qin Y. 2019 miR-221/222 promote tumor growth and suppress apoptosis by targeting lncRNA GAS5 in breast cancer. Biosci. Rep. 39 BSR20181859.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zou L., Ding Z. and Roy P. 2010 Profilin-1 overexpression inhibits proliferation of MDA-MB-231 breast cancer cells partly through p27kip1 upregulation. J. Cell. Physiol. 223, 623–629.

    CAS  PubMed  PubMed Central  Google Scholar 

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Corresponding editor: H. A. Ranganath

SSH and MNa contributed to the idea design and literature search. MNu helped in data interpretation. SSH wrote parts of the manuscript. MNa contributed to designing the figures.

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Nurzadeh, M., Naemi, M. & Sheikh Hasani, S. A comprehensive review on oncogenic miRNAs in breast cancer. J Genet 100, 15 (2021). https://doi.org/10.1007/s12041-021-01265-7

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