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The Roles of MicroRNAs in Breast Cancer

Takahashi, Ryou-u, Miyazaki, Hiroaki, Ochiya, Takahiro·2015·Cancers

Abstract

MicroRNAs (miRNAs) constitute a large family of small, approximately 20–22 nucleotide, non-coding RNAs that regulate the expression of target genes, mainly at the post-transcriptional level. Accumulating lines of evidence have indicated that miRNAs play important roles in the maintenance of biological homeostasis and that aberrant expression levels of miRNAs are associated with the onset of many diseases, including cancer. In various cancers, miRNAs play important roles in tumor initiation, drug resistance and metastasis. Recent studies reported that miRNAs could also be secreted via small endosome-derived vesicles called exosomes, which are derived from multiple cell types, including dendritic cells, lymphocytes, and tumor cells. Exosomal miRNAs play an important role in cell-to-cell communication and have been investigated as prognostic and diagnostic biomarkers. In this review, we summarize the major findings related to the functions of miRNAs in breast cancer, which is the most frequent cancer in women, and discuss the potential clinical uses of miRNAs, including their roles as therapeutic targets and diagnostic markers.

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Research works printed but not linked: 96

  1. Yi, 2014, Quantitative phosphoproteomic analysis reveals system-wide signaling pathways downstream of SDF-1/CXCR4 in breast cancer stem cells, Proc. Natl. Acad. Sci. USA, 111, E2182, 10.1073/pnas.1404943111 · DOI
  2. Perou, 2000, Molecular portraits of human breast tumours, Nature, 406, 747, 10.1038/35021093 · DOI
  3. Taylor, 2008, MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer, Gynecol. Oncol., 110, 13, 10.1016/j.ygyno.2008.04.033 · DOI
  4. Shiohama, 2003, Molecular cloning and expression analysis of a novel gene DGCR8 located in the digeorge syndrome chromosomal region, Biochem. Biophys. Res. Commun., 304, 184, 10.1016/S0006-291X(03)00554-0 · DOI
  5. Yamagishi, 2003, Unraveling the genetic and developmental mysteries of 22q11 deletion syndrome, Trends Mol. Med., 9, 383, 10.1016/S1471-4914(03)00141-2 · DOI
  6. Ruby, 2007, Intronic microRNA precursors that bypass drosha processing, Nature, 448, 83, 10.1038/nature05983 · DOI · Paper page
  7. Sibley, 2012, The biogenesis and characterization of mammalian microRNAs of mirtron origin, Nucleic Acids Res., 40, 438, 10.1093/nar/gkr722 · DOI
  8. Lund, 2004, Nuclear export of microRNA precursors, Science, 303, 95, 10.1126/science.1090599 · DOI
  9. Ota, 2013, Adar1 forms a complex with dicer to promote microRNA processing and rna-induced gene silencing, Cell, 153, 575, 10.1016/j.cell.2013.03.024 · DOI
  10. Iorio, 2012, MicroRNA dysregulation in cancer: Diagnostics, monitoring and therapeutics. A comprehensive review, EMBO Mol. Med., 4, 143, 10.1002/emmm.201100209 · DOI
  11. Uchino, 2013, Therapeutic effects of microRNA-582-5p and -3p on the inhibition of bladder cancer progression, Mol. Ther. J. Am. Soc. Gene Ther., 21, 610, 10.1038/mt.2012.269 · DOI
  12. Liu, 2013, The IGF2 intronic MIR-483 selectively enhances transcription from IGF2 fetal promoters and enhances tumorigenesis, Genes Dev., 27, 2543, 10.1101/gad.224170.113 · DOI
  13. Mandke, 2012, MicroRNA-34a modulates MDM4 expression via a target site in the open reading frame, PLoS ONE, 7, e42034, 10.1371/journal.pone.0042034 · DOI
  14. Blenkiron, 2007, MicroRNA expression profiling of human breast cancer identifies new markers of tumor subtype, Genome Biol., 8, R214, 10.1186/gb-2007-8-10-r214 · DOI
  15. Iorio, 2005, MicroRNA gene expression deregulation in human breast cancer, Cancer Res., 65, 7065, 10.1158/0008-5472.CAN-05-1783 · DOI · Paper page
  16. He, 2005, A microRNA polycistron as a potential human oncogene, Nature, 435, 828, 10.1038/nature03552 · DOI
  17. Yamamoto, Y., Yoshioka, Y., Minoura, K., Takahashi, R.U., Takeshita, F., Taya, T., Horii, R., Fukuoka, Y., Kato, T., and Kosaka, N. (2011). An integrative genomic analysis revealed the relevance of microRNA and gene expression for drug-resistance in human breast cancer cells. Mol. Cancer, 10. · DOI
  18. Ruan, 2014, MicroRNA-21 regulates T-cell apoptosis by directly targeting the tumor suppressor gene tipe2, Cell Death Dis., 5, e1095, 10.1038/cddis.2014.47 · DOI
  19. Wang, 2014, MicroRNA-497 inhibition of ovarian cancer cell migration and invasion through targeting of SMAD specific E3 ubiquitin protein ligase 1, Biochem. Biophys. Res. Commun., 449, 432, 10.1016/j.bbrc.2014.05.053 · DOI
  20. Bu, 2013, A microRNA miR-34a-regulated bimodal switch targets Notch in colon cancer stem cells, Cell Stem Cell, 12, 602, 10.1016/j.stem.2013.03.002 · DOI
  21. Shimono, 2009, Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells, Cell, 138, 592, 10.1016/j.cell.2009.07.011 · DOI
  22. Hwang, 2014, MicroRNA-146a directs the symmetric division of Snail-dominant colorectal cancer stem cells, Nature Cell Biol., 16, 268, 10.1038/ncb2910 · DOI
  23. Yu, 2007, let-7 regulates self renewal and tumorigenicity of breast cancer cells, Cell, 131, 1109, 10.1016/j.cell.2007.10.054 · DOI
  24. Gregory, 2008, The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1, Nat. Cell Biol., 10, 593, 10.1038/ncb1722 · DOI
  25. Martello, 2010, A microRNA targeting dicer for metastasis control, Cell, 141, 1195, 10.1016/j.cell.2010.05.017 · DOI
  26. Song, 2013, MicroRNA-Antagonism regulates breast cancer stemness and metastasis via TET-family-dependent chromatin remodeling, Cell, 154, 311, 10.1016/j.cell.2013.06.026 · DOI
  27. Kovalchuk, 2008, Involvement of microRNA-451 in resistance of the MCF-7 breast cancer cells to chemotherapeutic drug doxorubicin, Mol. Cancer Therapeutics, 7, 2152, 10.1158/1535-7163.MCT-08-0021 · DOI
  28. Liang, 2010, Involvement of miR-326 in chemotherapy resistance of breast cancer through modulating expression of multidrug resistance-associated protein 1, Biochem. Pharmacol., 79, 817, 10.1016/j.bcp.2009.10.017 · DOI
  29. Ma, 2013, MiR-487a resensitizes mitoxantrone (mx)-resistant breast cancer cells (MCF-7/MX) to MX by targeting breast cancer resistance protein (BCRP/ABCG2), Cancer Lett., 339, 107, 10.1016/j.canlet.2013.07.016 · DOI
  30. Miller, 2008, MicroRNA-221/222 confers tamoxifen resistance in breast cancer by targeting p27Kip1, J. Biol. Chem., 283, 29897, 10.1074/jbc.M804612200 · DOI
  31. Bockhorn, J., Dalton, R., Nwachukwu, C., Huang, S., Prat, A., Yee, K., Chang, Y.F., Huo, D., Wen, Y., and Swanson, K.E. (2013). MicroRNA-30c inhibits human breast tumour chemotherapy resistance by regulating TWF1 and IL-11. Nat. Commun., 4. · DOI
  32. Korner, 2013, MicroRNA-31 sensitizes human breast cells to apoptosis by direct targeting of protein kinase C epsilon (PKCepsilon), J. Biol. Chem., 288, 8750, 10.1074/jbc.M112.414128 · DOI
  33. Tavazoie, 2008, Endogenous human microRNAs that suppress breast cancer metastasis, Nature, 451, 147, 10.1038/nature06487 · DOI
  34. Valastyan, 2009, A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis, Cell, 137, 1032, 10.1016/j.cell.2009.03.047 · DOI
  35. Kim, 2011, A p53/miRNA-34 axis regulates Snail1-dependent cancer cell epithelial-mesenchymal transition, J. Cell Biol., 195, 417, 10.1083/jcb.201103097 · DOI
  36. Chou, 2013, Gata3 suppresses metastasis and modulates the tumour microenvironment by regulating microRNA-29b expression, Nat. Cell Biol., 15, 201, 10.1038/ncb2672 · DOI
  37. Ryu, 2013, Suppression of miRNA-708 by polycomb group promotes metastases by calcium-induced cell migration, Cancer Cell, 23, 63, 10.1016/j.ccr.2012.11.019 · DOI
  38. Takahashi, 2014, The role of microRNAs in the regulation of cancer stem cells, Front. Genet., 4, e295, 10.3389/fgene.2013.00295 · DOI · Paper page
  39. Chaffer, 2011, Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state, Proc. Natl. Acad. Sci. USA, 108, 7950, 10.1073/pnas.1102454108 · DOI
  40. Wicha, 2003, Prospective identification of tumorigenic breast cancer cells, Proc. Natl. Acad. Sci. USA, 100, 3983, 10.1073/pnas.0530291100 · DOI
  41. Mani, 2008, The epithelial-mesenchymal transition generates cells with properties of stem cells, Cell, 133, 704, 10.1016/j.cell.2008.03.027 · DOI
  42. Burk, 2008, A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells, EMBO Rep., 9, 582, 10.1038/embor.2008.74 · DOI
  43. Honma, 2008, Rpn2 gene confers docetaxel resistance in breast cancer, Nat. Med., 14, 939, 10.1038/nm.1858 · DOI
  44. Takahashi, R.U., Takeshita, F., Honma, K., Ono, M., Kato, K., and Ochiya, T. (2013). Ribophorin II regulates breast tumor initiation and metastasis through the functional suppression of GSK3beta. Sci. Rep., 3. · DOI
  45. Vecchione, 2013, A microRNA signature defines chemoresistance in ovarian cancer through modulation of angiogenesis, Proc. Natl. Acad. Sci. USA, 110, 9845, 10.1073/pnas.1305472110 · DOI
  46. Kartner, 1983, Cell surface p-glycoprotein associated with multidrug resistance in mammalian cell lines, Science, 221, 1285, 10.1126/science.6137059 · DOI
  47. Kartner, 1983, Daunorubicin-resistant chinese hamster ovary cells expressing multidrug resistance and a cell-surface p-glycoprotein, Cancer Res., 43, 4413
  48. Doyle, 1998, A multidrug resistance transporter from human MCF-7 breast cancer cells, Proc. Natl. Acad. Sci. USA, 95, 15665, 10.1073/pnas.95.26.15665 · DOI
  49. Fletcher, 2010, Abc transporters in cancer: More than just drug efflux pumps, Nat. Rev. Cancer, 10, 147, 10.1038/nrc2789 · DOI
  50. Juliano, 1976, A surface glycoprotein modulating drug permeability in chinese hamster ovary cell mutants, Biochim. Biophys. Acta, 455, 152, 10.1016/0005-2736(76)90160-7 · DOI
  51. Pirker, 1993, MDR1 gene expression in primary colorectal carcinomas, Br. J. Cancer, 68, 691, 10.1038/bjc.1993.411 · DOI
  52. Reeve, 1989, Amplification and expression of MDR1 gene in a multidrug resistant variant of small cell lung cancer cell line NCI-H69, Br. J. Cancer, 60, 339, 10.1038/bjc.1989.282 · DOI
  53. Sullivan, 2000, Regulation of expression of the multidrug resistance protein MRP1 by p53 in human prostate cancer cells, J. Clin. Investig., 105, 1261, 10.1172/JCI9290 · DOI
  54. Kim, 2001, An analysis of relapsed breast cancer in patients previously treated with breast conserving surgery, Breast Cancer, 8, 146, 10.1007/BF02967494 · DOI
  55. Scheffer, 2002, Multidrug resistance related molecules in human and murine lung, J. Clin. Pathol., 55, 332, 10.1136/jcp.55.5.332 · DOI
  56. Ross, 2000, Novel mechanisms of drug resistance in leukemia, Leukemia, 14, 467, 10.1038/sj.leu.2401694 · DOI
  57. Haraguchi, 2010, Cd13 is a therapeutic target in human liver cancer stem cells, J. Clin. Investig., 120, 3326, 10.1172/JCI42550 · DOI
  58. Nagel, 2007, Regulation of the p27(Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation, EMBO J., 26, 3699, 10.1038/sj.emboj.7601790 · DOI
  59. Pichiorri, 2013, In vivo NCL targeting affects breast cancer aggressiveness through miRNA regulation, J. Exp. Med., 210, 951, 10.1084/jem.20120950 · DOI
  60. Gupta, 2006, Cancer metastasis: Building a framework, Cell, 127, 679, 10.1016/j.cell.2006.11.001 · DOI
  61. Chou, 2010, Gata3 in development and cancer differentiation: Cells gata have it!, J. Cell. Physiol., 222, 42, 10.1002/jcp.21943 · DOI
  62. Sutherland, 2007, Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation, Nat. Cell Biol., 9, 201, 10.1038/ncb1530 · DOI · Paper page
  63. Bechis, 2008, Gata-3 links tumor differentiation and dissemination in a luminal breast cancer model, Cancer Cell, 13, 141, 10.1016/j.ccr.2008.01.011 · DOI
  64. Canel, 2013, E-cadherin-integrin crosstalk in cancer invasion and metastasis, J. Cell Sci., 126, 393, 10.1242/jcs.100115 · DOI
  65. Shen, 2013, EGFR modulates microRNA maturation in response to hypoxia through phosphorylation of AGO2, Nature, 497, 383, 10.1038/nature12080 · DOI
  66. Taylor, 1979, Quantitation of peroxidase-antibody binding to membrane fragments using column chromatography, Anal. Biochem., 98, 53, 10.1016/0003-2697(79)90704-8 · DOI
  67. Mittelbrunn, M., Gutierrez-Vazquez, C., Villarroya-Beltri, C., Gonzalez, S., Sanchez-Cabo, F., Gonzalez, M.A., Bernad, A., and Sanchez-Madrid, F. (2011). Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat. Commun., 2. · DOI
  68. McDonald, 2014, Functional significance of macrophage-derived exosomes in inflammation and pain, Pain, 155, 1527, 10.1016/j.pain.2014.04.029 · DOI
  69. Putz, U., Howitt, J., Doan, A., Goh, C.P., Low, L.H., Silke, J., and Tan, S.S. (2012). The tumor suppressor PTEN is exported in exosomes and has phosphatase activity in recipient cells. Sci. Signal., 5. · DOI
  70. Taylor, D.D., and Gercel-Taylor, C. (2013). The origin, function, and diagnostic potential of RNA within extracellular vesicles present in human biological fluids. Front. Genet., 4. · DOI
  71. Valadi, 2007, Exosome-mediated transfer of mrnas and microRNAs is a novel mechanism of genetic exchange between cells, Nat. Cell Biol., 9, 654, 10.1038/ncb1596 · DOI · Paper page
  72. Peinado, 2012, Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET, Nat. Med., 18, 883, 10.1038/nm.2753 · DOI · Paper page
  73. Marleau, A.M., Chen, C.S., Joyce, J.A., and Tullis, R.H. (2012). Exosome removal as a therapeutic adjuvant in cancer. J. Transl. Med., 10. · DOI
  74. Lim, 2011, Gap junction-mediated import of microRNA from bone marrow stromal cells can elicit cell cycle quiescence in breast cancer cells, Cancer Res., 71, 1550, 10.1158/0008-5472.CAN-10-2372 · DOI
  75. Chen, 2014, Exosomes from drug-resistant breast cancer cells transmit chemoresistance by a horizontal transfer of microRNAs, PLoS ONE, 9, e95240, 10.1371/journal.pone.0095240 · DOI
  76. Zhong, 2013, MiR-222 and miR-29a contribute to the drug-resistance of breast cancer cells, Gene, 531, 8, 10.1016/j.gene.2013.08.062 · DOI
  77. Takeshita, 2010, Systemic delivery of synthetic microRNA-16 inhibits the growth of metastatic prostate tumors via downregulation of multiple cell-cycle genes, Mol. Ther. J. Am. Soc. Gene Ther., 18, 181, 10.1038/mt.2009.207 · DOI
  78. Fujiwara, 2014, Clinical relevance and therapeutic significance of microRNA-133a expression profiles and functions in malignant osteosarcoma-initiating cells, Stem Cells, 32, 959, 10.1002/stem.1618 · DOI
  79. Noguchi, 2013, Chemically modified synthetic microRNA-205 inhibits the growth of melanoma cells in vitro and in vivo, Mol. Ther. J. Am. Soc. Gene Ther., 21, 1204, 10.1038/mt.2013.70 · DOI
  80. Takahashi, 2013, In vitro optimization of 2'-ome-4'-thioribonucleoside-modified anti-microRNA oligonucleotides and its targeting delivery to mouse liver using a liposomal nanoparticle, Nucleic Acids Res., 41, 10659, 10.1093/nar/gkt823 · DOI
  81. Chao, 2014, MicroRNA-205 signaling regulates mammary stem cell fate and tumorigenesis, J. Clin. Investig., 124, 3093, 10.1172/JCI73351 · DOI
  82. Huang, 2013, Targeted delivery of microRNA-29b by transferrin-conjugated anionic lipopolyplex nanoparticles: A novel therapeutic strategy in acute myeloid leukemia, Clin. Cancer Res., 19, 2355, 10.1158/1078-0432.CCR-12-3191 · DOI
  83. Garzon, 2009, MicroRNA 29b functions in acute myeloid leukemia, Blood, 114, 5331, 10.1182/blood-2009-03-211938 · DOI
  84. Esposito, 2014, Multifunctional aptamer-miRNA conjugates for targeted cancer therapy, Mol. Ther. J. Am. Soc. Gene Ther., 22, 1151, 10.1038/mt.2014.5 · DOI
  85. Li, 2009, Axl as a potential therapeutic target in cancer: Role of Axl in tumor growth, metastasis and angiogenesis, Oncogene, 28, 3442, 10.1038/onc.2009.212 · DOI
  86. Volinia, 2013, Prognostic microRNA/mrna signature from the integrated analysis of patients with invasive breast cancer, Proc. Natl. Acad. Sci. USA, 110, 7413, 10.1073/pnas.1304977110 · DOI · Paper page
  87. Trevino, 2013, Differential expression of miR-21, miR-125b and miR-191 in breast cancer tissue, Asia-Pacific J. Clin. Oncol., 9, 53, 10.1111/j.1743-7563.2012.01548.x · DOI
  88. Hoppe, 2013, Increased expression of miR-126 and miR-10a predict prolonged relapse-free time of primary oestrogen receptor-positive breast cancer following tamoxifen treatment, Eur. J. Cancer, 49, 3598, 10.1016/j.ejca.2013.07.145 · DOI
  89. Zhu, 2009, Circulating microRNAs in breast cancer and healthy subjects, BMC Res. Notes, 2, e89, 10.1186/1756-0500-2-89 · DOI
  90. Wang, 2014, Increased circulating microRNA-155 as a potential biomarker for breast cancer screening: A meta-analysis, Molecules, 19, 6282, 10.3390/molecules19056282 · DOI
  91. Dinami, 2014, MiR-155 drives telomere fragility in human breast cancer by targeting TRF1, Cancer Res., 74, 4145, 10.1158/0008-5472.CAN-13-2038 · DOI
  92. Wouters, 2012, Expression profiling of cancerous and normal breast tissues identifies microRNAs that are differentially expressed in serum from patients with (metastatic) breast cancer and healthy volunteers, Breast Cancer Res., 14, PMID
  93. Godfrey, A.C., Xu, Z., Weinberg, C.R., Getts, R.C., Wade, P.A., Deroo, L.A., Sandler, D.P., and Taylor, J.A. (2013). Serum microRNA expression as an early marker for breast cancer risk in prospectively collected samples from the sister study cohort. Breast Cancer Res., 15. · DOI
  94. Sochor, 2014, Oncogenic microRNAs: MiR-155, miR-19a, miR-181b, and miR-24 enable monitoring of early breast cancer in serum, BMC Cancer, 14, e448, 10.1186/1471-2407-14-448 · DOI
  95. Im, 2014, Label-free detection and molecular profiling of exosomes with a nano-plasmonic sensor, Nat. Biotechnol., 32, 490, 10.1038/nbt.2886 · DOI
  96. Yoshioka, Y., Kosaka, N., Konishi, Y., Ohta, H., Okamoto, H., Sonoda, H., Nonaka, R., Yamamoto, H., Ishii, H., and Mori, M. (2014). Ultra-Sensitive liquid biopsy of circulating extracellular vesicles using exoscreen. Nat. Commun., 5. · DOI

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Metadata

Authors
Takahashi, R.-U., Miyazaki, H., & Ochiya, T.
Affiliations
Division of Molecular and Cellular Medicine, National Cancer Center Research Institute 1-1, Tsukiji 5-chome, Chuo-ku, Tokyo 104-0045, Japan
Venue
Cancers
Publisher
MDPI AG
Published
2015-04-09
Volume
7
Issue
2
Pages
598-616
ISSN
2072-6694
Cited by
116
References
7
Language
en

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