Targeting noncoding RNAs in disease

Journal of Clinical Investigation

Volumn 127, Issue 3, 2017, Pages 761-771

  Adams, Brian D ^a,b   Parsons, Christine ^c   Walker, Lisa ^d   Zhang, Wen Cai ^d   Slack, Frank J ^d  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BOWDOIN COLLEGE   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; FOMIVIRSEN; GLUCOSE; INSULIN; LONG UNTRANSLATED RNA; MICRORNA; MIPOMERSEN; MOLECULAR SCAFFOLD; NANOPARTICLE; POLYGLACTIN; UNTRANSLATED RNA; ANTISENSE OLIGODEOXYNUCLEOTIDE; RNA;

ALZHEIMER DISEASE; ANGIOGENESIS; CARCINOGENESIS; CHEMICAL MODIFICATION; CHRONIC DISEASE; CYTOMEGALOVIRUS RETINITIS; DIABETES MELLITUS; DRUG DELIVERY SYSTEM; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HYDROPHOBICITY; MALIGNANT NEOPLASM; MOLECULARLY TARGETED THERAPY; NERVE CELL NETWORK; NERVOUS SYSTEM DEVELOPMENT; OLIGONUCLEOTIDE THERAPY; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); REVIEW; RNA INTERFERENCE; RNA PROCESSING; SIGNAL TRANSDUCTION; TUMOR GROWTH; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEOPLASMS; NEURODEGENERATIVE DISEASES;

CLINICAL TRIALS, PHASE I AS TOPIC; CLINICAL TRIALS, PHASE II AS TOPIC; CYTOMEGALOVIRUS RETINITIS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; NEOPLASMS; NEURODEGENERATIVE DISEASES; OLIGODEOXYRIBONUCLEOTIDES, ANTISENSE; RNA, LONG NONCODING; RNA, NEOPLASM;

EID: 85015882308     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI84424     Document Type: Review

References (143)

1. Mattick JS. Non-coding RNAs: the architects of eukaryotic complexity. EMBO Rep. 2001;2(11):986-991.
2. Djebali S, et al. Landscape of transcription in human cells. Nature. 2012;489(7414):101-108.
3. Mattick JS, Makunin IV. Non-coding RNA. Hum Mol Genet. 2006;15(suppl 1):R17-R29.
4. Esquela-Kerscher A, Slack FJ. Oncomirs-microRNAs with a role in cancer. Nat Rev. 2006;6(4):259-269.
5. Memczak S, et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature. 2013;495(7441):333-338.
6. Volinia S, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A. 2006;103(7):2257-2261.
7. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 1993;75(5):843-854.
8. Rinn JL, Chang HY. Genome regulation by long noncoding RNAs. Annu Rev Biochem. 2012;81:145-166.
9. Kiss T. Small nucleolar RNA-guided post-transcriptional modification of cellular RNAs. EMBO J. 2001;20(14):3617-3622.
10. Kiss T. Small nucleolar RNAs: an abundant group of noncoding RNAs with diverse cellular functions. Cell. 2002;109(2):145-148.
11. Napoli C, Lemieux C, Jorgensen R. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell. 1990;2(4):279-289.
12. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 1998;391(6669):806-811.
13. Kato M, Slack FJ. microRNAs: small molecules with big roles-C. elegans to human cancer. Biol Cell. 2008;100(2):71-81.
14. Zhou J, Ng SB, Chng WJ. LIN28/LIN28B: an emerging oncogenic driver in cancer stem cells. Int J Biochem Cell Biol. 2013;45(5):973-978.
15. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136(2):215-233.
16. Mendell JT, Olson EN. MicroRNAs in stress signaling and human disease. Cell. 2012;148(6):1172-1187.
17. Finnerty JR, Wang WX, Hébert SS, Wilfred BR, Mao G, Nelson PT. The miR-15/107 group of microRNA genes: evolutionary biology, cellular functions, and roles in human diseases. J Mol Biol. 2010;402(3):491-509.
18. Adams BD, Kasinski AL, Slack FJ. Aberrant regulation and function of microRNAs in cancer. Curr Biol. 2014;24(16):R762-R776.
19. Macfarlane LA, Murphy PR. MicroRNA: biogenesis, function and role in cancer. Curr Genomics. 2010;11(7):537-561.
20. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116(2):281-297.
21. Lee Y, et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 2004;23(20):4051-4060.
22. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol. 2009;11(3):228-234.
23. Fabian MR, Sonenberg N, Filipowicz W. Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem. 2010;79:351-379.
24. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009;19(1):92-105.
25. Lee JT. Epigenetic regulation by long noncoding RNAs. Science. 2012;338(6113):1435-1439.
26. Ponting CP, Oliver PL, Reik W. Evolution and functions of long noncoding RNAs. Cell. 2009;136(4):629-641.
27. McHugh CA, et al. The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature. 2015;521(7551):232-236.
28. Cheetham SW, Gruhl F, Mattick JS, Dinger ME. Long noncoding RNAs and the genetics of cancer. Br J Cancer. 2013;108(12):2419-2425.
29. Pasmant E, Sabbagh A, Vidaud M, Bièche I. ANRIL, a long, noncoding RNA, is an unexpected major hotspot in GWAS. FASEB J. 2011;25(2):444-448.
30. Jendrzejewski J, et al. The polymorphism rs944289 predisposes to papillary thyroid carcinoma through a large intergenic noncoding RNA gene of tumor suppressor type. Proc Natl Acad Sci U S A. 2012;109(22):8646-8651.
31. Zeliadt N. Big pharma shows signs of renewed interest in RNAi drugs. Nat Med. 2014;20(2):109.
32. Van Rooij E, Purcell AL, Levin AA. Developing MicroRNA therapeutics. Circ Res. 2012;110(3):496-507.
33. Stenvang J, Petri A, Lindow M, Obad S, Kauppinen S. Inhibition of microRNA function by antimiR oligonucleotides. Silence. 2012;3(1):1.
34. Hutvágner G, Simard MJ, Mello CC, Zamore PD. Sequence-specific inhibition of small RNA function. PLoS Biol. 2004;2(4):E98.
35. Meister G, Landthaler M, Dorsett Y, Tuschl T. Sequence-specific inhibition of microRNAand siRNA-induced RNA silencing. RNA. 2004;10(3):544-550.
36. Elmén J, et al. LNA-mediated microRNA silencing in non-human primates. Nature. 2008;452(7189):896-899.
37. Ørom UA, Kauppinen S, Lund AH. LNA-modified oligonucleotides mediate specific inhibition of microRNA function. Gene. 2006;372:137-141.
38. Davis S, Lollo B, Freier S, Esau C. Improved targeting of miRNA with antisense oligonucleotides. Nucleic Acids Res. 2006;34(8):2294-2304.
39. Esau C, et al. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab. 2006;3(2):87-98.
40. Obad S, et al. Silencing of microRNA families by seed-targeting tiny LNAs. Nat Genet. 2011;43(4):371-378.
41. Henry JC, Azevedo-Pouly ACP, Schmittgen TD. MicroRNA replacement therapy for cancer. Pharm Res. 2011;28(12):3030-3042.
42. Henry JC, et al. miR-199a-3p targets CD44 and reduces proliferation of CD44 positive hepatocellular carcinoma cell lines. Biochem Biophys Res Commun. 2010;403(1):120-125.
43. Fabani MM, Gait MJ. miR-122 targeting with LNA/2O-methyl oligonucleotide mixmers, peptide nucleic acids (PNA), and PNA-peptide conjugates. RNA. 2008;14(2):336-346.
44. Nielsen PE, Egholm M, Buchardt O. Peptide nucleic acid (PNA). A DNA mimic with a peptide backbone. Bioconjug Chem. 1994;5(1):3-7.
45. Misso G, et al. Mir-34: a new weapon against cancer? Mol Ther Nucleic Acids. 2014;3:e194.
46. Pirollo KF, et al. Tumor-targeting nanocomplex delivery of novel tumor suppressor RB94 chemosensitizes bladder carcinoma cells in vitro and in vivo. Clin Cancer Res. 2008;14(7):2190-2198.
47. Trang P, et al. Systemic delivery of tumor suppressor microRNA mimics using a neutral lipid emulsion inhibits lung tumors in mice. Mol Ther. 2011;19(6):1116-1122.
48. Kasinski AL, Slack FJ. miRNA-34 prevents cancer initiation and progression in a therapeutically resistant K-ras and p53-induced mouse model of lung adenocarcinoma. Cancer Res. 2012;72(21):5576-5587.
49. Kasinski AL, et al. A combinatorial microRNA therapeutics approach to suppressing non-small cell lung cancer. Oncogene. 2015;34(27):3547-3555.
50. Babar IA, 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. 2012;109(26):E1695-E1704.
51. Woodrow KA, Cu Y, Booth CJ, Saucier-Sawyer JK, Wood MJ, Saltzman WM. Intravaginal gene silencing using biodegradable polymer nanoparticles densely loaded with small-interfering RNA. Nat Mater. 2009;8(6):526-533.
52. Zhou J, et al. Biodegradable poly(amine-co-ester) terpolymers for targeted gene delivery. Nat Mater. 2011;11(1):82-90.
53. Adams BD, et al. miR-34a silences c-SRC to attenuate tumor growth in triple-negative breast cancer. Cancer Res. 2016;76(4):927-939.
54. Cheng CJ, et al. MicroRNA silencing for cancer therapy targeted to the tumour microenvironment. Nature. 2015;518(7537):107-110.
55. Yao L, et al. pHLIP peptide targets nanogold particles to tumors. Proc Natl Acad Sci U S A. 2013;110(2):465-470.
56. Catuogno S, Rienzo A, Di Vito A, Esposito CL, de Franciscis V. Selective delivery of therapeutic single strand antimiRs by aptamer-based conjugates. J Control Release. 2015;210:147-159.
57. Pofahl M, Wengel J, Mayer G. Multifunctional nucleic acids for tumor cell treatment. Nucleic Acid Ther. 2014;24(2):171-177.
58. Gupta RA, et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature. 2010;464(7291):1071-1076.
59. Roberts TC, Wood MJ. Therapeutic targeting of non-coding RNAs. Essays Biochem. 2013;54(1):127-145.
60. Tano K, et al. MALAT-1 enhances cell motility of lung adenocarcinoma cells by influencing the expression of motility-related genes. FEBS Lett. 2010;584(22):4575-4580.
61. Ji P, et al. MALAT-1, a novel noncoding RNA, and thymosin beta4 predict metastasis and survival in early-stage non-small cell lung cancer. Oncogene. 2003;22(39):8031-8041.
62. Smaldone MC, Davies BJ. BC-819, a plasmid comprising the H19 gene regulatory sequences and diphtheria toxin A, for the potential targeted therapy of cancers. Curr Opin Mol Ther. 2010;12(5):607-616.
63. Fatemi RP, Velmeshev D, Faghihi MA. Derepressing LncRNA-targeted genes to upregulate gene expression: focus on small molecule therapeutics. Mol Ther Nucleic Acids. 2014;3:e196.
64. Rettig GR, Behlke MA. Progress toward in vivo use of siRNAs-II. Mol Ther. 2012;20(3):483-512.
65. Kurreck J, Wyszko E, Gillen C, Erdmann VA. Design of antisense oligonucleotides stabilized by locked nucleic acids. Nucleic Acids Res. 2002;30(9):1911-1918.
66. Bonasio R, Shiekhattar R. Regulation of transcription by long noncoding RNAs. Annu Rev Genet. 2014;48:433-455.
67. Villegas VE, Zaphiropoulos PG. Neighboring gene regulation by antisense long non-coding RNAs. Int J Mol Sci. 2015;16(2):3251-3266.
68. Kaneko S, et al. Interactions between JARID2 and noncoding RNAs regulate PRC2 recruitment to chromatin. Mol Cell. 2014;53(2):290-300.
69. Paris O, et al. Direct regulation of microRNA biogenesis and expression by estrogen receptor beta in hormone-responsive breast cancer. Oncogene. 2012;31(38):4196-4206.
70. Davis BN, Hata A. Regulation of MicroRNA Biogenesis: A miRiad of mechanisms. Cell Commun Signal. 2009;7:18.
71. Xiao Z, Chen Y. Small molecule targeting miR-34a for cancer therapy. Mol Cell Oncol. 2015;2(1):e977160.
72. Ferrarelli LK. Targeting the undruggable MYCN. Sci Signal. 2014;7(344):ec260.
73. Melkman-Zehavi T, et al. miRNAs control insulin content in pancreatic cells via downregulation of transcriptional repressors. EMBO J. 2011;30(5):835-845.
74. Poy MN, et al. A pancreatic islet-specific microRNA regulates insulin secretion. Nature. 2004;432(7014):226-230.
75. Poy MN, et al. miR-375 maintains normal pancreatic alpha-and beta-cell mass. Proc Natl Acad Sci U S A. 2009;106(14):5813-5818.
76. Higuchi C, et al. Identification of circulating miR-101, miR-375 and miR-802 as biomarkers for type 2 diabetes. Metab Clin Exp. 2015;64(4):489-497.
77. Erener S, Mojibian M, Fox JK, Denroche HC, Kieffer TJ. Circulating miR-375 as a biomarker of cell death and diabetes in mice. Endocrinology. 2013;154(2):603-608.
78. Zhao E, et al. Obesity and genetics regulate microRNAs in islets, liver, and adipose of diabetic mice. Mamm Genome. 2009;20(8):476-485.
79. Lovis P, et al. Alterations in microRNA expression contribute to fatty acid-induced pancreatic cell dysfunction. Diabetes. 2008;57(10):2728-2736.
80. Ohno M, et al. The flavonoid apigenin improves glucose tolerance through inhibition of microRNA maturation in miRNA103 transgenic mice. Sci Rep. 2013;3:2553.
81. Trajkovski M, et al. MicroRNAs 103 and 107 regulate insulin sensitivity. Nature. 2011;474(7353):649-653.
82. Christoph. A microRNA therapeutic targeting microRNA-103/107 for the treatment of NASH in patients with type 2 diabetes/pre-diabetes, selected as clinical candidate by AstraZeneca. miRNA Blog, miRNA Res Ind News. April 7, 2015. http://mirnablog. com/a-microrna-therapeutic-targetingmicrorna-103107-for-the-treatment-of-nashin-patients-with-type-2-diabetespre-diabetesselected-as-clinical-candidate-by-astrazeneca/. Accessed February 10, 2017.
83. Chen JF, et al. Targeted deletion of Dicer in the heart leads to dilated cardiomyopathy and heart failure. Proc Natl Acad Sci U S A. 2008;105(6):2111-2116.
84. van Rooij E, Sutherland LB, Qi X, Richardson JA, Hill J, Olson EN. Control of stress-dependent cardiac growth and gene expression by a microRNA. Science. 2007;316(5824):575-579.
85. Zhao Y, Samal E, Srivastava D. Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature. 2005;436(7048):214-220.
86. Montgomery RL, et al. Therapeutic inhibition of miR-208a improves cardiac function and survival during heart failure. Circulation. 2011;124(14):1537-1547.
87. Callis TE, et al. MicroRNA-208a is a regulator of cardiac hypertrophy and conduction in mice. J Clin Invest. 2009;119(9):2772-2786.
88. Hydbring P, Badalian-Very G. Clinical applications of microRNAs. F1000Res. 2013;2:136.
89. Hullinger TG, et al. Inhibition of miR-15 protects against cardiac ischemic injury. Circ Res. 2012;110(1):71-81.
90. Yap KL, et al. Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol Cell. 2010;38(5):662-674.
91. Mercer TR, Dinger ME, Sunkin SM, Mehler MF, Mattick JS. Specific expression of long noncoding RNAs in the mouse brain. Proc Natl Acad Sci U S A. 2008;105(2):716-721.
92. Bak M, et al. MicroRNA expression in the adult mouse central nervous system. RNA. 2008;14(3):432-444.
93. Daughters RS, et al. RNA gain-of-function in spinocerebellar ataxia type 8. PLoS Genet. 2009;5(8):e1000600.
94. Smith P, Al Hashimi A, Girard J, Delay C, Hébert SS. In vivo regulation of amyloid precursor protein neuronal splicing by microRNAs. J Neurochem. 2011;116(2):240-247.
95. Chang F, Zhang LH, Xu WP, Jing P, Zhan PY. microRNA-9 attenuates amyloidinduced synaptotoxicity by targeting calcium/calmodulindependent protein kinase kinase 2. Mol Med Rep. 2014;9(5):1917-1922.
96. Krützfeldt J, et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature. 2005;438(7068):685-689.
97. Ali SS, et al. Pathological microRNAs in acute cardiovascular diseases and microRNA therapeutics. J Acute Dis. 2015;5(1):9-15.
98. Banzhaf-Strathmann J, et al. MicroRNA-125b induces tau hyperphosphorylation and cognitive deficits in Alzheimer's disease. EMBO J. 2014;33(15):1667-1680.
99. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100(1):57-70.
100. Herranz H, Cohen SM. MicroRNAs and gene regulatory networks: managing the impact of noise in biological systems. Genes Dev. 2010;24(13):1339-1344.
101. Tsang J, Zhu J, van Oudenaarden A. MicroRNAmediated feedback and feedforward loops are recurrent network motifs in mammals. Mol Cell. 2007;26(5):753-767.
102. Martinez NJ, Walhout AJ. The interplay between transcription factors and microRNAs in genome-scale regulatory networks. Bioessays. 2009;31(4):435-445.
103. Dong Q, et al. MicroRNA let-7a inhibits proliferation of human prostate cancer cells in vitro and in vivo by targeting E2F2 and CCND2. PLoS One. 2010;5(4):e10147.
104. Trang P, et al. Regression of murine lung tumors by the let-7 microRNA. Oncogene. 2010;29(11):1580-1587.
105. Bandi N, Vassella E. miR-34a and miR-15a/16 are co-regulated in non-small cell lung cancer and control cell cycle progression in a synergistic and Rb-dependent manner. Mol Cancer. 2011;10:55.
106. Redon S, Reichenbach P, Lingner J. The noncoding RNA TERRA is a natural ligand and direct inhibitor of human telomerase. Nucleic Acids Res. 2010;38(17):5797-5806.
107. Liu Z, et al. Downregulation of GAS5 promotes bladder cancer cell proliferation, partly by regulating CDK6. PLoS One. 2013;8(9):e73991.
108. Guo X, et al. GAS5 inhibits gastric cancer cell proliferation partly by modulating CDK6. Oncol Res Treat. 2015;38(7-8):362-366.
109. Yin D, He X, Zhang E, Kong R, De W, Zhang Z. Long noncoding RNA GAS5 affects cell proliferation and predicts a poor prognosis in patients with colorectal cancer. Med Oncol. 2014;31(11):253.
110. Jovanovic M, Hengartner MO. miRNAs and apoptosis: RNAs to die for. Oncogene. 2006;25(46):6176-6187.
111. Wang L, et al. Effects of microRNA-221/222 on cell proliferation and apoptosis in prostate cancer cells. Gene. 2015;572(2):252-258.
112. Yang X, et al. Down-regulation of mir-221 and mir-222 restrain prostate cancer cell proliferation and migration that is partly mediated by activation of SIRT1. PLoS One. 2014;9(6):e98833.
113. Naemura M, Murasaki C, Inoue Y, Okamoto H, Kotake Y. Long noncoding RNA ANRIL regulates proliferation of non-small cell lung cancer and cervical cancer cells. Anticancer Res. 2015;35(10):5377-5382.
114. Nie FQ, et al. Long noncoding RNA ANRIL promotes non-small cell lung cancer cell proliferation and inhibits apoptosis by silencing KLF2 and P21 expression. Mol Cancer Ther. 2015;14(1):268-277.
115. Zhu H, Li X, Song Y, Zhang P, Xiao Y, Xing Y. Long non-coding RNA ANRIL is up-regulated in bladder cancer and regulates bladder cancer cell proliferation and apoptosis through the intrinsic pathway. Biochem Biophys Res Commun. 2015;467(2):223-228.
116. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med. 1971;285(21):1182-1186.
117. Klagsbrun M, Soker S. VEGF/VPF: the angiogenesis factor found? Curr Biol. 1993;3(10):699-702.
118. Folkman J, Klagsbrun M. Angiogenic factors. Science. 1987;235(4787):442-447.
119. Chen S, et al. Global microRNA depletion suppresses tumor angiogenesis. Genes Dev. 2014;28(10):1054-1067.
120. Cimmino A, et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci U S A. 2005;102(39):13944-13949.
121. Kuehbacher A, Urbich C, Zeiher AM, Dimmeler S. Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circ Res. 2007;101(1):59-68.
122. Stahlhut C, Suárez Y, Lu J, Mishima Y, Giraldez AJ. miR-1 and miR-206 regulate angiogenesis by modulating VegfA expression in zebrafish. Development. 2012;139(23):4356-4364.
123. Babae N, et al. Systemic miRNA-7 delivery inhibits tumor angiogenesis and growth in murine xenograft glioblastoma. Oncotarget. 2014;5(16):6687-6700.
124. Mercer TR, Dinger ME, Mattick JS. Long noncoding RNAs: insights into functions. Nat Rev Genet. 2009;10(3):155-159.
125. Zhou Y, Zhang X, Klibanski A. MEG3 noncoding RNA: a tumor suppressor. J Mol Endocrinol. 2012;48(3):R45-R53.
126. Li X, et al. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor PDCD4 and promotes cell transformation, proliferation, and metastasis in renal cell carcinoma. Cell Physiol Biochem. 2014;33(6):1631-1642.
127. Meng F, Henson R, Wehbe-Janek H, Ghoshal K, Jacob ST, Patel T. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology. 2007;133(2):647-658.
128. De Mattos-Arruda L, et al. MicroRNA-21 links epithelial-to-mesenchymal transition and inflammatory signals to confer resistance to neoadjuvant trastuzumab and chemotherapy in HER2-positive breast cancer patients. Oncotarget. 2015;6(35):37269-37280.
129. Yigit MV, et al. Context-dependent differences in miR-10b breast oncogenesis can be targeted for the prevention and arrest of lymph node metastasis. Oncogene. 2013;32(12):1530-1538.
130. Ma L, et al. Therapeutic silencing of miR-10b inhibits metastasis in a mouse mammary tumor model. Nat Biotechnol. 2010;28(4):341-347.
131. Liu Z, Zhu J, Cao H, Ren H, Fang X. miR-10b promotes cell invasion through RhoC-AKT signaling pathway by targeting HOXD10 in gastric cancer. Int J Oncol. 2012;40(5):1553-1560.
132. Le MT, et al. miR-200-containing extracellular vesicles promote breast cancer cell metastasis. J Clin Invest. 2014;124(12):5109-5128.
133. Perdigão-Henriques R, et al. miR-200 promotes the mesenchymal to epithelial transition by suppressing multiple members of the Zeb2 and Snail1 transcriptional repressor complexes. Oncogene. 2016;35(2):158-172.
134. Burk U, et al. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 2008;9(6):582-589.
135. Sundararajan V, Gengenbacher N, Stemmler MP, Kleemann JA, Brabletz T, Brabletz S. The ZEB1/miR-200c feedback loop regulates invasion via actin interacting proteins MYLK and TKS5. Oncotarget. 2015;6(29):27083-27096.
136. Banyard J, et al. Regulation of epithelial plasticity by miR-424 and miR-200 in a new prostate cancer metastasis model. Sci Rep. 2013;3:3151.
137. Edmonds MD, et al. MicroRNA-31 initiates lung tumorigenesis and promotes mutant KRAS-driven lung cancer. J Clin Invest. 2016;126(1):349-364.
138. Zhang WC, et al. Tumour-initiating cell-specific miR-1246 and miR-1290 expression converge to promote non-small cell lung cancer progression. Nat Commun. 2016;7:11702.
139. Ge Y, Zhang L, Nikolova M, Reva B, Fuchs E. Strand-specific in vivo screen of cancer-associated miRNAs unveils a role for miR-21() in SCC progression. Nat Cell Biol. 2016;18(1):111-121.
140. Mitra RN, et al. Nanoparticle-mediated miR200-b delivery for the treatment of diabetic retinopathy. J Control Release. 2016;236:31-37.
141. Arun G, et al. Differentiation of mammary tumors and reduction in metastasis upon Malat1 lncRNA loss. Genes Dev. 2016;30(1):34-51.
142. Fu WM, et al. Long noncoding RNA Hotair mediated angiogenesis in nasopharyngeal carcinoma by direct and indirect signaling pathways. Oncotarget. 2016;7(4):4712-4723.
143. Yin DD, Liu ZJ, Zhang E, Kong R, Zhang ZH, Guo RH. Decreased expression of long noncoding RNA MEG3 affects cell proliferation and predicts a poor prognosis in patients with colorectal cancer. Tumour Biol. 2015;36(6):4851-4859.