MicroRNAs as novel targets and tools in cancer therapy

Cancer Letters

Volumn 387, Issue , 2017, Pages 84-94

  Abba, Mohammed L ^a   Patil, Nitin ^a   Leupold, Jörg H ^a   Moniuszko, Marcin ^b   Utikal, Jochen ^a,c   Niklinski, Jacek ^b   Allgayer, Heike ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b MEDICAL UNIVERSITY OF BIALYSTOK   (Poland)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Cancer; Metastasis; microRNAs; Stem cells; Therapy

Indexed keywords

ANTAGOMIR; ANTI MIR; ANTINEOPLASTIC AGENT; ANTISENSE MICRORNA ANTAGONIST; ANTISENSE OLIGONUCLEOTIDE; COMPETITIVE ENDOGENOUS RNA; DOUBLE STRANDED RNA; LIPOSOME; LOCKED NUCLEIC ACID; MICRORNA; MICRORNA 107; MICRORNA 124; MICRORNA 145; MICRORNA 155; MICRORNA 16; MICRORNA 21; MICRORNA 221; MICRORNA 34A; MIR 124 3P ANTAGOMIR; MIRAVIRSEN; MIRNA SPONGE; MRX 34; NANOPARTICLE; RIBONUCLEOTIDE; RNA; SMALL MOLECULE INHIBITOR OF MIRNA; SUNITINIB; TARGOMIR; TEMOZOLOMIDE; UNCLASSIFIED DRUG; UNINDEXED DRUG;

CANCER GROWTH; CANCER STEM CELL; CANCER THERAPY; CARCINOGENICITY; CELLULAR DISTRIBUTION; DRUG TARGETING; GENE CONTROL; GENE LOCATION; HEPATITIS C; HUMAN; LIVER CELL CARCINOMA; METASTASIS; NON SMALL CELL LUNG CANCER; NONHUMAN; PLEURA MESOTHELIOMA; PRIORITY JOURNAL; PSEUDOGENE; SHORT SURVEY; TUMOR MICROENVIRONMENT; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; NEOPLASMS; ONCOGENE; TUMOR SUPPRESSOR GENE;

ANIMALS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; HUMANS; MICRORNAS; NEOPLASMS; ONCOGENES;

EID: 84964375025     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2016.03.043     Document Type: Review

References (115)

1. [1] Calin, G.A., Croce, C.M., MicroRNA–cancer connection: the beginning of a new tale. Cancer Res 66 (2006), 7390–7394.
2. [2] Wach, S., Nolte, E., Szczyrba, J., Stohr, R., Hartmann, A., Orntoft, T., et al. MicroRNA profiles of prostate carcinoma detected by multiplatform microRNA screening. Int. J. Cancer 130 (2012), 611–621.
3. [3] Saito, Y., Suzuki, H., Imaeda, H., Matsuzaki, J., Hirata, K., Tsugawa, H., et al. The tumor suppressor microRNA-29c is downregulated and restored by celecoxib in human gastric cancer cells. Int. J. Cancer 132 (2013), 1751–1760.
4. [4] Munding, J.B., Adai, A.T., Maghnouj, A., Urbanik, A., Zollner, H., Liffers, S.T., et al. Global microRNA expression profiling of microdissected tissues identifies miR-135b as a novel biomarker for pancreatic ductal adenocarcinoma. Int. J. Cancer 131 (2012), E86–E95.
5. [5] Li, W., Xie, L., He, X., Li, J., Tu, K., Wei, L., et al. Diagnostic and prognostic implications of microRNAs in human hepatocellular carcinoma. Int. J. Cancer 123 (2008), 1616–1622.
6. [6] Gits, C.M., van Kuijk, P.F., Jonkers, M.B., Boersma, A.W., Smid, M., van Ijcken, W.F., et al. MicroRNA expression profiles distinguish liposarcoma subtypes and implicate miR-145 and miR-451 as tumor suppressors. Int. J. Cancer 135 (2014), 348–361.
7. [7] Ferretti, E., De Smaele, E., Po, A., Di Marcotullio, L., Tosi, E., Espinola, M.S., et al. MicroRNA profiling in human medulloblastoma. Int. J. Cancer 124 (2009), 568–577.
8. [8] Bjaanaes, M.M., Halvorsen, A.R., Solberg, S., Jorgensen, L., Dragani, T.A., Galvan, A., et al. Unique microRNA-profiles in EGFR-mutated lung adenocarcinomas. Int. J. Cancer 135 (2014), 1812–1821.
9. [9] Lu, J., Getz, G., Miska, E.A., Alvarez-Saavedra, E., Lamb, J., Peck, D., et al. MicroRNA expression profiles classify human cancers. Nature 435 (2005), 834–838.
10. [10] Mudduluru, G., Abba, M., Batliner, J., Patil, N., Scharp, M., Lunavat, T.R., et al. A systematic approach to defining the microRNA landscape in metastasis. Cancer Res 75 (2015), 3010–3019.
11. [11] Filipowicz, W., Bhattacharyya, S.N., Sonenberg, N., Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight?. Nat. Rev. Genet 9 (2008), 102–114.
12. [12] Reinhart, B.J., Slack, F.J., Basson, M., Pasquinelli, A.E., Bettinger, J.C., Rougvie, A.E., et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403 (2000), 901–906.
13. [13] Lee, R.C., Feinbaum, R.L., Ambros, V., The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75 (1993), 843–854.
14. [14] Nielsen, C.B., Shomron, N., Sandberg, R., Hornstein, E., Kitzman, J., Burge, C.B., Determinants of targeting by endogenous and exogenous microRNAs and siRNAs. RNA 13 (2007), 1894–1910.
15. [15] Lewis, B.P., Burge, C.B., Bartel, D.P., Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120 (2005), 15–20.
16. [16] Wightman, B., Ha, I., Ruvkun, G., Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75 (1993), 855–862.
17. [17] Krutzfeldt, J., Kuwajima, S., Braich, R., Rajeev, K.G., Pena, J., Tuschl, T., et al. Specificity, duplex degradation and subcellular localization of antagomirs. Nucleic Acids Res 35 (2007), 2885–2892.
18. [18] Krutzfeldt, J., Rajewsky, N., Braich, R., Rajeev, K.G., Tuschl, T., Manoharan, M., et al. Silencing of microRNAs in vivo with ‘antagomirs’. Nature 438 (2005), 685–689.
19. [19] Ebert, M.S., Neilson, J.R., Sharp, P.A., MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat. Methods 4 (2007), 721–726.
20. [20] Velagapudi, S.P., Gallo, S.M., Disney, M.D., Sequence-based design of bioactive small molecules that target precursor microRNAs. Nat. Chem. Biol 10 (2014), 291–297.
21. [21] Sayed, D., Rane, S., Lypowy, J., He, M., Chen, I.Y., Vashistha, H., et al. MicroRNA-21 targets Sprouty2 and promotes cellular outgrowths. Mol. Biol. Cell 19 (2008), 3272–3282.
22. [22] Thomas, J.R., Hergenrother, P.J., Targeting RNA with small molecules. Chem. Rev 108 (2008), 1171–1224.
23. [23] Zhang, S., Chen, L., Jung, E.J., Calin, G.A., Targeting microRNAs with small molecules: from dream to reality. Clin. Pharmacol. Ther 87 (2010), 754–758.
24. [24] Melo, S., Villanueva, A., Moutinho, C., Davalos, V., Spizzo, R., Ivan, C., et al. Small molecule enoxacin is a cancer-specific growth inhibitor that acts by enhancing TAR RNA-binding protein 2-mediated microRNA processing. Proc. Natl. Acad. Sci. U.S.A. 108 (2011), 4394–4399.
25. [25] Wang, B., Li, S., Qi, H.H., Chowdhury, D., Shi, Y., Novina, C.D., Distinct passenger strand and mRNA cleavage activities of human Argonaute proteins. Nat. Struct. Mol. Biol 16 (2009), 1259–1266.
26. [26] Wang, H.W., Noland, C., Siridechadilok, B., Taylor, D.W., Ma, E., Felderer, K., et al. Structural insights into RNA processing by the human RISC-loading complex. Nat. Struct. Mol. Biol 16 (2009), 1148–1153.
27. [27] Deiters, A., Small molecule modifiers of the microRNA and RNA interference pathway. AAPS J. 12 (2010), 51–60.
28. [28] Ebert, M.S., Sharp, P.A., MicroRNA sponges: progress and possibilities. RNA 16 (2010), 2043–2050.
29. [29] Du, C., Liu, C., Kang, J., Zhao, G., Ye, Z., Huang, S., et al. MicroRNA miR-326 regulates TH-17 differentiation and is associated with the pathogenesis of multiple sclerosis. Nat. Immunol 10 (2009), 1252–1259.
30. [30] Care, A., Catalucci, D., Felicetti, F., Bonci, D., Addario, A., Gallo, P., et al. MicroRNA-133 controls cardiac hypertrophy. Nat. Med 13 (2007), 613–618.
31. [31] Taulli, R., Loretelli, C., Pandolfi, P.P., From pseudo-ceRNAs to circ-ceRNAs: a tale of cross-talk and competition. Nat. Struct. Mol. Biol 20 (2013), 541–543.
32. [32] Xia, T., Chen, S., Jiang, Z., Shao, Y., Jiang, X., Li, P., et al. Long noncoding RNA FER1L4 suppresses cancer cell growth by acting as a competing endogenous RNA and regulating PTEN expression. Sci. Rep, 5, 2015, 13445.
33. [33] Welch, J.D., Baran-Gale, J., Perou, C.M., Sethupathy, P., Prins, J.F., Pseudogenes transcribed in breast invasive carcinoma show subtype-specific expression and ceRNA potential. BMC Genomics, 16, 2015, 113.
34. [34] Poliseno, L., Marranci, A., Pandolfi, P.P., Pseudogenes in human cancer. Front. Med, 2, 2015, 68.
35. [35] Karreth, F.A., Reschke, M., Ruocco, A., Ng, C., Chapuy, B., Leopold, V., et al. The BRAF pseudogene functions as a competitive endogenous RNA and induces lymphoma in vivo. Cell 161 (2015), 319–332.
36. [36] Karreth, F.A., Ala, U., Provero, P., Pandolfi, P.P., Pseudogenes as competitive endogenous RNAs: target prediction and validation. Methods Mol. Biol 1167 (2014), 199–212.
37. [37] Walther, W., Stein, U., Viral vectors for gene transfer: a review of their use in the treatment of human diseases. Drugs 60 (2000), 249–271.
38. [38] Kasiappan, R., Sun, Y., Lungchukiet, P., Quarni, W., Zhang, X., Bai, W., Vitamin D suppresses leptin stimulation of cancer growth through microRNA. Cancer Res 74 (2014), 6194–6204.
39. [39] Ben-Shushan, D., Markovsky, E., Gibori, H., Tiram, G., Scomparin, A., Satchi-Fainaro, R., Overcoming obstacles in microRNA delivery towards improved cancer therapy. Drug Deliv. Transl. Res 4 (2014), 38–49.
40. [40] Cheng, C.J., Bahal, R., Babar, I.A., Pincus, Z., Barrera, F., Liu, C., et al. MicroRNA silencing for cancer therapy targeted to the tumour microenvironment. Nature 518 (2015), 107–110.
41. [41] Ofran, Y., Rowe, J.M., Genetic profiling in acute myeloid leukaemia – where are we and what is its role in patient management. Br. J. Haematol 160 (2013), 303–320.
42. [42] Gao, X.N., Lin, J., Li, Y.H., Gao, L., Wang, X.R., Wang, W., et al. MicroRNA-193a represses c-kit expression and functions as a methylation-silenced tumor suppressor in acute myeloid leukemia. Oncogene 30 (2011), 3416–3428.
43. [43] Lin, Y., Li, D., Liang, Q., Liu, S., Zuo, X., Li, L., et al. miR-638 regulates differentiation and proliferation in leukemic cells by targeting cyclin-dependent kinase 2. J. Biol. Chem 290 (2015), 1818–1828.
44. [44] Emmrich, S., Engeland, F., El-Khatib, M., Henke, K., Obulkasim, A., Schoning, J., et al. miR-139-5p controls translation in myeloid leukemia through EIF4G2. Oncogene, 2015, 10.1038/onc.2015.247.
45. [45] Gong, J.N., Yu, J., Lin, H.S., Zhang, X.H., Yin, X.L., Xiao, Z., et al. The role, mechanism and potentially therapeutic application of microRNA-29 family in acute myeloid leukemia. Cell Death Differ 21 (2014), 100–112.
46. [46] Huang, X., Schwind, S., Yu, B., Santhanam, R., Wang, H., Hoellerbauer, P., et al. Targeted delivery of microRNA-29b by transferrin-conjugated anionic lipopolyplex nanoparticles: a novel therapeutic strategy in acute myeloid leukemia. Clin. Cancer Res 19 (2013), 2355–2367.
47. [47] Su, R., Lin, H.S., Zhang, X.H., Yin, X.L., Ning, H.M., Liu, B., et al. MiR-181 family: regulators of myeloid differentiation and acute myeloid leukemia as well as potential therapeutic targets. Oncogene 34 (2015), 3226–3239.
48. [48] Utikal, J., Abba, M., Novak, D., Moniuszko, M., Allgayer, H., Function and significance of MicroRNAs in benign and malignant human stem cells. Semin. Cancer Biol 35 (2015), 200–211.
49. [49] Dorrance, A.M., Neviani, P., Ferenchak, G.J., Huang, X., Nicolet, D., Maharry, K.S., et al. Targeting leukemia stem cells in vivo with antagomiR-126 nanoparticles in acute myeloid leukemia. Leukemia 29 (2015), 2143–2153.
50. [50] Li, Z., Chen, P., Su, R., Li, Y., Hu, C., Wang, Y., et al. Overexpression and knockout of miR-126 both promote leukemogenesis. Blood 126 (2015), 2005–2015.
51. [51] Yu, Y., Yang, L., Zhao, M., Zhu, S., Kang, R., Vernon, P., et al. Targeting microRNA-30a-mediated autophagy enhances imatinib activity against human chronic myeloid leukemia cells. Leukemia 26 (2012), 1752–1760.
52. [52] Wang, W.Z., Pu, Q.H., Lin, X.H., Liu, M.Y., Wu, L.R., Wu, Q.Q., et al. Silencing of miR-21 sensitizes CML CD34(+) stem/progenitor cells to imatinib-induced apoptosis by blocking PI3K/AKT pathway. Leuk. Res 39 (2015), 1117–1124.
53. [53] Kumarswamy, R., Mudduluru, G., Ceppi, P., Muppala, S., Kozlowski, M., Niklinski, J., et al. MicroRNA-30a inhibits epithelial-to-mesenchymal transition by targeting Snai1 and is downregulated in non-small cell lung cancer. Int. J. Cancer 130 (2012), 2044–2053.
54. [54] Sampath, D., Liu, C., Vasan, K., Sulda, M., Puduvalli, V.K., Wierda, W.G., et al. Histone deacetylases mediate the silencing of miR-15a, miR-16, and miR-29b in chronic lymphocytic leukemia. Blood 119 (2012), 1162–1172.
55. [55] Wang, L.Q., Wong, K.Y., Rosen, A., Chim, C.S., Epigenetic silencing of tumor suppressor miR-3151 contributes to Chinese chronic lymphocytic leukemia by constitutive activation of MADD/ERK and PIK3R2/AKT signaling pathways. Oncotarget 6 (2015), 44422–44436.
56. [56] Al-Harbi, S., Choudhary, G.S., Ebron, J.S., Hill, B.T., Vivekanathan, N., Ting, A.H., et al. miR-377-dependent BCL-xL regulation drives chemotherapeutic resistance in B-cell lymphoid malignancies. Mol. Cancer, 14, 2015, 185.
57. [57] Babar, I.A., Cheng, C.J., Booth, C.J., Liang, X., Weidhaas, J.B., Saltzman, W.M., et al. Nanoparticle-based therapy in an in vivo microRNA-155 (miR-155)-dependent mouse model of lymphoma. Proc. Natl. Acad. Sci. U.S.A. 109 (2012), E1695–E1704.
58. [58] Nguyen, L.V., Vanner, R., Dirks, P., Eaves, C.J., Cancer stem cells: an evolving concept. Nat. Rev. Cancer 12 (2012), 133–143.
59. [59] Valent, P., Bonnet, D., De Maria, R., Lapidot, T., Copland, M., Melo, J.V., et al. Cancer stem cell definitions and terminology: the devil is in the details. Nat. Rev. Cancer 12 (2012), 767–775.
60. [60] Bernhardt, M., Galach, M., Novak, D., Utikal, J., Mediators of induced pluripotency and their role in cancer cells – current scientific knowledge and future perspectives. Biotechnol. J. 7 (2012), 810–821.
61. [61] Liu, C., Tang, D.G., MicroRNA regulation of cancer stem cells. Cancer Res 71 (2011), 5950–5954.
62. [62] Fang, L., Cai, J., Chen, B., Wu, S., Li, R., Xu, X., et al. Aberrantly expressed miR-582-3p maintains lung cancer stem cell-like traits by activating Wnt/beta-catenin signalling. Nat. Commun, 6, 2015, 8640.
63. [63] Zhou, W., Li, Y., Gou, S., Xiong, J., Wu, H., Wang, C., et al. MiR-744 increases tumorigenicity of pancreatic cancer by activating Wnt/beta-catenin pathway. Oncotarget 6 (2015), 37557–37569.
64. [64] Wen, S.Y., Lin, Y., Yu, Y.Q., Cao, S.J., Zhang, R., Yang, X.M., et al. miR-506 acts as a tumor suppressor by directly targeting the hedgehog pathway transcription factor Gli3 in human cervical cancer. Oncogene 34 (2015), 717–725.
65. [65] Gao, Y., Liu, T., Huang, Y., MicroRNA-134 suppresses endometrial cancer stem cells by targeting POGLUT1 and Notch pathway proteins. FEBS Lett 589 (2015), 207–214.
66. [66] Wezel, F., Pearson, J., Kirkwood, L.A., Southgate, J., Differential expression of Oct4 variants and pseudogenes in normal urothelium and urothelial cancer. Am. J. Pathol 183 (2013), 1128–1136.
67. [67] Johnsson, P., Morris, K.V., Grander, D., Pseudogenes: a novel source of trans-acting antisense RNAs. Methods Mol. Biol 1167 (2014), 213–226.
68. [68] Hayashi, H., Arao, T., Togashi, Y., Kato, H., Fujita, Y., De Velasco, M.A., et al. The OCT4 pseudogene POU5F1B is amplified and promotes an aggressive phenotype in gastric cancer. Oncogene 34 (2015), 199–208.
69. [69] Wang, L., Guo, Z.Y., Zhang, R., Xin, B., Chen, R., Zhao, J., et al. Pseudogene OCT4-pg4 functions as a natural micro RNA sponge to regulate OCT4 expression by competing for miR-145 in hepatocellular carcinoma. Carcinogenesis 34 (2013), 1773–1781.
70. [70] Kawamura, N., Nimura, K., Nagano, H., Yamaguchi, S., Nonomura, N., Kaneda, Y., CRISPR/Cas9-mediated gene knockout of NANOG and NANOGP8 decreases the malignant potential of prostate cancer cells. Oncotarget 6 (2015), 22361–22374.
71. [71] Hanahan, D., Weinberg, R.A., Hallmarks of cancer: the next generation. Cell 144 (2011), 646–674.
72. [72] Lamouille, S., Xu, J., Derynck, R., Molecular mechanisms of epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol 15 (2014), 178–196.
73. [73] Ye, X., Weinberg, R.A., Epithelial-mesenchymal plasticity: a central regulator of cancer progression. Trends Cell Biol 25 (2015), 675–686.
74. [74] Abba, M.L., Patil, N., Leupold, J.H., Allgayer, H., MicroRNA regulation of epithelial to mesenchymal transition. J. Clin. Med, 5, 2016, 8.
75. [75] Suzhi, Z., Liang, T., Yuexia, P., Lucy, L., Xiaoting, H., Yuan, Z., et al. Gap junctions enhance the antiproliferative effect of MicroRNA-124-3p in glioblastoma cells. J. Cell. Physiol 230 (2015), 2476–2488.
76. [76] Ananta, J.S., Paulmurugan, R., Massoud, T.F., Nanoparticle-delivered antisense MicroRNA-21 enhances the effects of temozolomide on glioblastoma cells. Mol. Pharm 12 (2015), 4509–4517.
77. [77] Passadouro, M., Pedroso de Lima, M.C., Faneca, H., MicroRNA modulation combined with sunitinib as a novel therapeutic strategy for pancreatic cancer. Int. J. Nanomedicine 9 (2014), 3203–3217.
78. [78] Gao, S., Tian, H., Guo, Y., Li, Y., Guo, Z., Zhu, X., et al. miRNA oligonucleotide and sponge for miRNA-21 inhibition mediated by PEI-PLL in breast cancer therapy. Acta Biomater 25 (2015), 184–193.
79. [79] Salah, Z., Arafeh, R., Maximov, V., Galasso, M., Khawaled, S., Abou-Sharieha, S., et al. miR-27a and miR-27a* contribute to metastatic properties of osteosarcoma cells. Oncotarget 6 (2015), 4920–4935.
80. [80] de Melo Maia, B., Ling, H., Monroig, P., Ciccone, M., Soares, F.A., Calin, G.A., et al. Design of a miRNA sponge for the miR-17 miRNA family as a therapeutic strategy against vulvar carcinoma. Mol. Cell. Probes 29 (2015), 420–426.
81. [81] Li, P., Sheng, C., Huang, L., Zhang, H., Huang, L., Cheng, Z., et al. MiR-183/-96/-182 cluster is up-regulated in most breast cancers and increases cell proliferation and migration. Breast Cancer Res, 16, 2014, 473.
82. [82] Moshiri, F., Callegari, E., Abundo, L.D., Corra, F., Lupini, L., Sabbioni, S., et al. Inhibiting the oncogenic mir-221 by microRNA sponge: toward microRNA-based therapeutics for hepatocellular carcinoma. Gastroenterol. Hepatol. Bed Bench 7 (2014), 43–54.
83. [83] Lin, C.W., Chang, Y.L., Chang, Y.C., Lin, J.C., Chen, C.C., Pan, S.H., et al. MicroRNA-135b promotes lung cancer metastasis by regulating multiple targets in the Hippo pathway and LZTS1. Nat. Commun, 4, 2013, 1877.
84. [84] Wang, Y.D., Cai, N., Wu, X.L., Cao, H.Z., Xie, L.L., Zheng, P.S., OCT4 promotes tumorigenesis and inhibits apoptosis of cervical cancer cells by miR-125b/BAK1 pathway. Cell Death Dis, 4, 2013, e760.
85. [85] Li, Q., Li, X., Guo, Z., Xu, F., Xia, J., Liu, Z., et al. MicroRNA-574-5p was pivotal for TLR9 signaling enhanced tumor progression via down-regulating checkpoint suppressor 1 in human lung cancer. PLoS ONE, 7, 2012, e48278.
86. [86] Liu, S., Sun, X., Wang, M., Hou, Y., Zhan, Y., Jiang, Y., et al. A microRNA 221- and 222-mediated feedback loop maintains constitutive activation of NFkappaB and STAT3 in colorectal cancer cells. Gastroenterology 147 (2014), 847–859 e811.
87. [87] Ma, L., Young, J., Prabhala, H., Pan, E., Mestdagh, P., Muth, D., et al. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat. Cell Biol 12 (2010), 247–256.
88. [88] Poliseno, L., Salmena, L., Zhang, J., Carver, B., Haveman, W.J., Pandolfi, P.P., A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 465 (2010), 1033–1038.
89. [89] Asangani, I.A., Rasheed, S.A., Nikolova, D.A., Leupold, J.H., Colburn, N.H., Post, S., et al. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27 (2008), 2128–2136.
90. [90] Poria, D.K., Guha, A., Nandi, I., Ray, P.S., RNA-binding protein HuR sequesters microRNA-21 to prevent translation repression of proinflammatory tumor suppressor gene programmed cell death 4. Oncogene 35 (2015), 1703–1715.
91. [91] Eades, G., Wolfson, B., Zhang, Y., Li, Q., Yao, Y., Zhou, Q., lincRNA-RoR and miR-145 regulate invasion in triple-negative breast cancer via targeting ARF6. Mol. Cancer Res 13 (2015), 330–338.
92. [92] Kallen, A.N., Zhou, X.B., Xu, J., Qiao, C., Ma, J., Yan, L., et al. The imprinted H19 lncRNA antagonizes let-7 microRNAs. Mol. Cell 52 (2013), 101–112.
93. [93] Ando, H., Asai, T., Koide, H., Okamoto, A., Maeda, N., Tomita, K., et al. Advanced cancer therapy by integrative antitumor actions via systemic administration of miR-499. J. Control. Release 181 (2014), 32–39.
94. [94] Zheng, F., Liao, Y.J., Cai, M.Y., Liu, T.H., Chen, S.P., Wu, P.H., et al. Systemic delivery of microRNA-101 potently inhibits hepatocellular carcinoma in vivo by repressing multiple targets. PLoS Genet, 11, 2015, e1004873.
95. [95] Cortez, M.A., Valdecanas, D., Zhang, X., Zhan, Y., Bhardwaj, V., Calin, G.A., et al. Therapeutic delivery of miR-200c enhances radiosensitivity in lung cancer. Mol. Ther 22 (2014), 1494–1503.
96. [96] Mudduluru, G., Ceppi, P., Kumarswamy, R., Scagliotti, G.V., Papotti, M., Allgayer, H., Regulation of Axl receptor tyrosine kinase expression by miR-34a and miR-199a/b in solid cancer. Oncogene 30 (2011), 2888–2899.
97. [97] Li, Y., Guessous, F., Zhang, Y., Dipierro, C., Kefas, B., Johnson, E., et al. MicroRNA-34a inhibits glioblastoma growth by targeting multiple oncogenes. Cancer Res 69 (2009), 7569–7576.
98. [98] He, X., He, L., Hannon, G.J., The guardian's little helper: microRNAs in the p53 tumor suppressor network. Cancer Res 67 (2007), 11099–11101.
99. [99] Misso, G., Di Martino, M.T., De Rosa, G., Farooqi, A.A., Lombardi, A., Campani, V., et al. Mir-34: a new weapon against cancer? Molecular therapy. Nucleic Acids, 3, 2014, e194.
100. [100] Di Martino, M.T., Campani, V., Misso, G., Gallo Cantafio, M.E., Gulla, A., Foresta, U., et al. In vivo activity of miR-34a mimics delivered by stable nucleic acid lipid particles (SNALPs) against multiple myeloma. PLoS ONE, 9, 2014, e90005.
101. [101] Lou, W., Chen, Q., Ma, L., Liu, J., Yang, Z., Shen, J., et al. Oncolytic adenovirus co-expressing miRNA-34a and IL-24 induces superior antitumor activity in experimental tumor model. J. Mol. Med. (Berl) 91 (2013), 715–725.
102. [102] Reid, G., Pel, M.E., Kirschner, M.B., Cheng, Y.Y., Mugridge, N., Weiss, J., et al. Restoring expression of miR-16: a novel approach to therapy for malignant pleural mesothelioma. Ann. Oncol 24 (2013), 3128–3135.
103. [103] Garofalo, M., Croce, C.M., Role of microRNAs in maintaining cancer stem cells. Adv. Drug Deliv. Rev 81 (2015), 53–61.
104. [104] Oleksiuk, O., Abba, M., Tezcan, K.C., Schaufler, W., Bestvater, F., Patil, N., et al. Single-molecule localization microscopy allows for the analysis of cancer metastasis-specific miRNA distribution on the nanoscale. Oncotarget 6 (2015), 44745–44757.
105. [105] Mitra, A.K., Zillhardt, M., Hua, Y., Tiwari, P., Murmann, A.E., Peter, M.E., et al. MicroRNAs reprogram normal fibroblasts into cancer-associated fibroblasts in ovarian cancer. Cancer Discov 2 (2012), 1100–1108.
106. [106] Zhao, X., Zhao, Z., Xu, W., Hou, J., Du, X., Down-regulation of miR-497 is associated with poor prognosis in renal cancer. Int. J. Clin. Exp. Pathol 8 (2015), 758–764.
107. [107] Zhang, S., Zhang, C., Liu, W., Zheng, W., Zhang, Y., Wang, S., et al. MicroRNA-24 upregulation inhibits proliferation, metastasis and induces apoptosis in bladder cancer cells by targeting CARMA3. Int. J. Oncol 47 (2015), 1351–1360.
108. [108] Wang, Z., Ma, B., Ji, X., Deng, Y., Zhang, T., Zhang, X., et al. MicroRNA-378-5p suppresses cell proliferation and induces apoptosis in colorectal cancer cells by targeting BRAF. Cancer Cell Int, 15, 2015, 40.
109. [109] Wang, X., Chen, Z., MicroRNA-19a functions as an oncogenic microRNA in non-small cell lung cancer by targeting the suppressor of cytokine signaling 1 and mediating STAT3 activation. Int. J. Mol. Med 35 (2015), 839–846.
110. [110] Wang, J., Song, Y.X., Ma, B., Wang, J.J., Sun, J.X., Chen, X.W., et al. Regulatory roles of non-coding RNAs in colorectal cancer. Int. J. Mol. Sci 16 (2015), 19886–19919.
111. [111] D'Ippolito, E., Iorio, M.V., MicroRNAs and triple negative breast cancer. Int. J. Mol. Sci 14 (2013), 22202–22220.
112. [112] Chandrasekaran, K., Karolina, D.S., Sepramaniam, S., Armugam, A., Wintour, E.M., Bertram, J.F., et al. Role of microRNAs in kidney homeostasis and disease. Kidney Int 81 (2012), 617–627.
113. [113] Catania, A., Maira, F., Skarmoutsou, E., Amico, F.D., Abounader, R., Mazzarino, M.C., Insight into the role of microRNAs in brain tumors (review). Int. J. Oncol 40 (2012), 605–624.
114. [114] Cannistraci, A., Di Pace, A.L., De Maria, R., Bonci, D., MicroRNA as new tools for prostate cancer risk assessment and therapeutic intervention: results from clinical data set and patients’ samples. Biomed Res. Int, 2014, 2014, 146170.
115. [115] Barbarotto, E., Schmittgen, T.D., Calin, G.A., MicroRNAs and cancer: profile, profile, profile. Int. J. Cancer 122 (2008), 969–977.