Review Article

MicroRNAs Determining Carcinogenesis by Regulating Oncogenes and Tumor Suppressor Genes During Cell Cycle

Author(s): Zacharias Fasoulakis*, George Daskalakis, Michail Diakosavvas, Ioannis Papapanagiotou, Marianna Theodora, Arzou Bourazan, Dimitra Alatzidou, Athanasios Pagkalos and Emmanuel N. Kontomanolis

Volume 9, Issue 2, 2020

Page: [82 - 92] Pages: 11

DOI: 10.2174/2211536608666190919161849

Abstract

Aim: To provide a review considering microRNAs regulating oncogenes and tumor suppressor genes during the different stages of cell cycle, controlling carcinogenesis.

Methods: The role of microRNAs involved as oncogenes’ and tumor suppressor genes’ regulators in cancer was searched in the relevant available literature in MEDLINE, including terms such as “microRNA”, “oncogenes”, “tumor suppressor genes”, “metastasis”, “cancer” and others.

Results: MicroRNAs determine the expression levels of multiple cell cycle regulators, such as cyclins, cyclin dependent kinases and other major cell cycle activators including retinoblastoma 1 (RB- 1) and p53, resulting in alteration and promotion/inhibition of the cell cycle.

Conclusion: MicroRNAs are proven to have a key role in cancer pathophysiology by altering the expression profile of different regulator proteins during cell division cycle and DNA replication. Thus, by acting as oncogenes and tumor suppressor genes, they can either promote or inhibit cancer development and formation, revealing their innovative role as biomarkers and therapeutic tools.

Keywords: Cancer, metastasis, microRNA, oncogene, tumor suppressor gene, segregation.

« Previous
Graphical Abstract

[1]
Society AC. Cancer facts and figures. American Cancer Society 2018.
[2]
Belmont JW, Boudreau A, Leal SM, et al. A haplotype map of the human genome. Nature 2005; 437(7063): 1299-320.
[http://dx.doi.org/10.1038/nature04226]
[3]
Lin S, Gregory RI. MicroRNA biogenesis pathways in cancer. Nat Rev Cancer 2015; 15(6): 321-33.
[http://dx.doi.org/10.1038/nrc3932] [PMID: 25998712]
[4]
Cell Signaling. Cell cycle control: G1 / S checkpoint. Cell Signal Tech 2019.https://www.cellsignal.com/contents/science-cst-pathways-cell-cycle-regulation/g1-s-checkpoint/pathways-cc-g1s
[5]
Yang N, Sheridan AM. Cell cycle Encyclopedia of toxicology. 3rd ed. Ref Module Biomed Sci 2014; pp. 753-8.
[http://dx.doi.org/10.1016/B978-0-12-386454-3.00273-6]
[6]
Lambert SA, Jolma A, Campitelli LF, et al. The human transcription factors. Cell 2018; 172(4): 650-65.
[http://dx.doi.org/10.1016/j.cell.2018.01.029] [PMID: 29425488]
[7]
Salazar-Roa M, Malumbres M. Fueling the cell division cycle. Trends Cell Biol 2017; 27(1): 69-81.
[http://dx.doi.org/10.1016/j.tcb.2016.08.009] [PMID: 27746095]
[8]
Lim S, Kaldis P. CDKs, cyclins and CKIs: roles beyond cell cycle regulation. Development 2013; 140(15): 3079-93.
[http://dx.doi.org/10.1242/dev.091744] [PMID: 23861057]
[9]
Hochegger H, Takeda S, Hunt T. Cyclin-dependent kinases and cell-cycle transitions: does one fit all? Nat Rev Mol Cell Biol 2008; 9(11): 910-6.
[http://dx.doi.org/10.1038/nrm2510] [PMID: 18813291]
[10]
Sánchez I, Dynlacht BD. New insights into cyclins, CDKs, and cell cycle control. Semin Cell Dev Biol 2005; 16(3): 311-21.
[http://dx.doi.org/10.1016/j.semcdb.2005.02.007] [PMID: 15840440]
[11]
Boutros R, Lobjois V, Ducommun B. CDC25 phosphatases in cancer cells: key players? Good targets? Nat Rev Cancer 2007; 7(7): 495-507.
[http://dx.doi.org/10.1038/nrc2169] [PMID: 17568790]
[12]
Hoffmann I, Clarke PR, Marcote MJ, Karsenti E, Draetta G. Phosphorylation and activation of human cdc25-C by cdc2--cyclin B and its involvement in the self-amplification of MPF at mitosis. EMBO J 1993; 12(1): 53-63.
[http://dx.doi.org/10.1002/j.1460-2075.1993.tb05631.x] [PMID: 8428594]
[13]
Zhang Z, Roe SM, Diogon M, Kong E, El Alaoui H, Barford D. Molecular structure of the N-terminal domain of the APC/C subunit CDC27 reveals a homo-dimeric tetratricopeptide repeat architecture. J Mol Biol 2010; 397(5): 1316-28.
[http://dx.doi.org/10.1016/j.jmb.2010.02.045] [PMID: 20206185]
[14]
Giacinti C, Giordano A. RB and cell cycle progression. Oncogene 2006; 25(38): 5220-7.
[http://dx.doi.org/10.1038/sj.onc.1209615] [PMID: 16936740]
[15]
Lujambio A, Akkari L, Simon J, et al. Non-cell-autonomous tumor suppression by p53. Cell 2013; 153(2): 449-60.
[http://dx.doi.org/10.1016/j.cell.2013.03.020] [PMID: 23562644]
[16]
Nevins JR. The Rb/E2F pathway and cancer. Hum Mol Genet 2001; 10(7): 699-703.
[http://dx.doi.org/10.1093/hmg/10.7.699] [PMID: 11257102]
[17]
Malumbres M, Barbacid M. To cycle or not to cycle: a critical decision in cancer. Nat Rev Cancer 2001; 1(3): 222-31.
[http://dx.doi.org/10.1038/35106065] [PMID: 11902577]
[18]
Esquela-Kerscher A, Slack FJ. Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer 2006; 6(4): 259-69.
[http://dx.doi.org/10.1038/nrc1840] [PMID: 16557279]
[19]
Fabian MR, Sonenberg N, Filipowicz W. Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 2010; 79: 351-79.
[http://dx.doi.org/10.1146/annurev-biochem-060308-103103] [PMID: 20533884]
[20]
Kontomanolis EN, Kalagasidou S, Fasoulakis Z. MicroRNAs as potential serum biomarkers for early detection of ectopic pregnancy. Cureus 2018; 10(3) e2344
[http://dx.doi.org/10.7759/cureus.2344] [PMID: 29796356]
[21]
Kontomanolis EN, Fasoulakis Z, Papamanolis V, et al. The impact of microRNAs in breast cancer angiogenesis and progression. MicroRNA 2019; 8(2): 101-9.
[http://dx.doi.org/10.2174/2211536607666181017122921]
[22]
Weber JA, Baxter DH, Zhang S, et al. The microRNA spectrum in 12 body fluids. Clin Chem 2010; 56(11): 1733-41.
[http://dx.doi.org/10.1373/clinchem.2010.147405] [PMID: 20847327]
[23]
Croce CM. Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet 2009; 10(10): 704-14.
[http://dx.doi.org/10.1038/nrg2634] [PMID: 19763153]
[24]
Takeshita F, Patrawala L, Osaki M, et al. Systemic delivery of synthetic microRNA-16 inhibits the growth of metastatic prostate tumors via downregulation of multiple cell-cycle genes. Mol Ther 2010; 18(1): 181-7.
[http://dx.doi.org/10.1038/mt.2009.207] [PMID: 19738602]
[25]
Shi T, Jiang R, Yu J, et al. SGOG-OV/AICE investigators. Addition of intraperitoneal cisplatin and etoposide to first-line chemotherapy for advanced ovarian cancer: a randomised, phase 2 trial. Br J Cancer 2018; 119(1): 12-8.
[http://dx.doi.org/10.1038/s41416-018-0036-7] [PMID: 29899395]
[26]
Pierson J, Hostager B, Fan R, Vibhakar R. Regulation of cyclin dependent kinase 6 by microRNA 124 in medulloblastoma. J Neurooncol 2008; 90(1): 1-7.
[http://dx.doi.org/10.1007/s11060-008-9624-3] [PMID: 18607543]
[27]
Kozaki K, Imoto I, Mogi S, Omura K, Inazawa J. Exploration of tumor-suppressive microRNAs silenced by DNA hypermethylation in oral cancer. Cancer Res 2008; 68(7): 2094-105.
[http://dx.doi.org/10.1158/0008-5472.CAN-07-5194] [PMID: 18381414]
[28]
Lal A, Kim HH, Abdelmohsen K, et al. p16(INK4a) translation suppressed by miR-24. PLoS One 2008; 3(3) e1864
[http://dx.doi.org/10.1371/journal.pone.0001864] [PMID: 18365017]
[29]
Sun F, Fu H, Liu Q, et al. Downregulation of CCND1 and CDK6 by miR-34a induces cell cycle arrest. FEBS Lett 2008; 582(10): 1564-8.
[http://dx.doi.org/10.1016/j.febslet.2008.03.057] [PMID: 18406353]
[30]
Shi L, Zhang J, Pan T, et al. MiR-125b is critical for the suppression of human U251 glioma stem cell proliferation. Brain Res 2010; 1312: 120-6.
[http://dx.doi.org/10.1016/j.brainres.2009.11.056] [PMID: 19948152]
[31]
Wu J, Qian J, Li C, et al. miR-129 regulates cell proliferation by downregulating CDK6 expression. Cell Cycle 2010; 9(9): 1809-18.
[http://dx.doi.org/10.4161/cc.9.9.11535] [PMID: 20404570]
[32]
Xu T, Zhu Y, Xiong Y, Ge YY, Yun JP, Zhuang SM. MicroRNA-195 suppresses tumorigenicity and regulates G1/S transition of human hepatocellular carcinoma cells. Hepatology 2009; 50(1): 113-21.
[http://dx.doi.org/10.1002/hep.22919] [PMID: 19441017]
[33]
Feng M, Yu Q. miR-449 regulates CDK-Rb-E2F1 through an auto-regulatory feedback circuit. Cell Cycle 2010; 9(2): 213-4.
[http://dx.doi.org/10.4161/cc.9.2.10502] [PMID: 20046097]
[34]
Bottoni A, Piccin D, Tagliati F, Luchin A, Zatelli MC. degli Uberti EC. miR-15a and miR-16-1 down-regulation in pituitary adenomas. J Cell Physiol 2005; 204(1): 280-5.
[http://dx.doi.org/10.1002/jcp.20282] [PMID: 15648093]
[35]
Bonci D, Coppola V, Musumeci M, et al. The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nat Med 2008; 14(11): 1271-7.
[http://dx.doi.org/10.1038/nm.1880] [PMID: 18931683]
[36]
Xia L, Zhang D, Du R, et al. miR-15b and miR-16 modulate multidrug resistance by targeting BCL2 in human gastric cancer cells. Int J Cancer 2008; 123(2): 372-9.
[http://dx.doi.org/10.1002/ijc.23501] [PMID: 18449891]
[37]
Liu Q, Fu H, Sun F, et al. miR-16 family induces cell cycle arrest by regulating multiple cell cycle genes. Nucleic Acids Res 2008; 36(16): 5391-404.
[http://dx.doi.org/10.1093/nar/gkn522] [PMID: 18701644]
[38]
Yu Z, Wang C, Wang M, et al. A cyclin D1/microRNA 17/20 regulatory feedback loop in control of breast cancer cell proliferation. J Cell Biol 2008; 182(3): 509-17.
[http://dx.doi.org/10.1083/jcb.200801079] [PMID: 18695042]
[39]
Kota J, Chivukula RR, O’Donnell KA, et al. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 2009; 137(6): 1005-17.
[http://dx.doi.org/10.1016/j.cell.2009.04.021] [PMID: 19524505]
[40]
Schultz J, Lorenz P, Gross G, Ibrahim S, Kunz M. MicroRNA let-7b targets important cell cycle molecules in malignant melanoma cells and interferes with anchorage-independent growth. Cell Res 2008; 18(5): 549-57.
[http://dx.doi.org/10.1038/cr.2008.45] [PMID: 18379589]
[41]
Wang F, Fu XD, Zhou Y, Zhang Y. Down-regulation of the cyclin E1 oncogene expression by microRNA-16-1 induces cell cycle arrest in human cancer cells. BMB Rep 2009; 42(11): 725-30.
[http://dx.doi.org/10.5483/BMBRep.2009.42.11.725] [PMID: 19944013]
[42]
Lujambio A, Ropero S, Ballestar E, et al. Genetic unmasking of an epigenetically silenced microRNA in human cancer cells. Cancer Res 2007; 67(4): 1424-9.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-4218] [PMID: 17308079]
[43]
O’Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 2005; 435(7043): 839-43.
[http://dx.doi.org/10.1038/nature03677] [PMID: 15944709]
[44]
Pickering MT, Stadler BM, Kowalik TF. miR-17 and miR-20a temper an E2F1-induced G1 checkpoint to regulate cell cycle progression. Oncogene 2009; 28(1): 140-5.
[http://dx.doi.org/10.1038/onc.2008.372] [PMID: 18836483]
[45]
Díaz R, Silva J, García JM, et al. Deregulated expression of miR-106a predicts survival in human colon cancer patients. Genes Chromosomes Cancer 2008; 47(9): 794-802.
[http://dx.doi.org/10.1002/gcc.20580]
[46]
Lin RJ, Lin YC, Yu AL. miR-149* induces apoptosis by inhibiting Akt1 and E2F1 in human cancer cells. Mol Carcinog 2010; 49(8): 719-27.
[http://dx.doi.org/10.1002/mc.20647] [PMID: 20623644]
[47]
Lee KH, Chen YL, Yeh SD, et al. MicroRNA-330 acts as tumor suppressor and induces apoptosis of prostate cancer cells through E2F1-mediated suppression of Akt phosphorylation. Oncogene 2009; 28(38): 3360-70.
[http://dx.doi.org/10.1038/onc.2009.192] [PMID: 19597470]
[48]
Guo X, Guo L, Ji J, et al. miRNA-331-3p directly targets E2F1 and induces growth arrest in human gastric cancer. Biochem Biophys Res Commun 2010; 398(1): 1-6.
[http://dx.doi.org/10.1016/j.bbrc.2010.05.082] [PMID: 20510161]
[49]
Giannakakis A, Sandaltzopoulos R, Greshock J, et al. miR-210 links hypoxia with cell cycle regulation and is deleted in human epithelial ovarian cancer. Cancer Biol Ther 2008; 7(2): 255-64.
[http://dx.doi.org/10.4161/cbt.7.2.5297] [PMID: 18059191]
[50]
Huang L, Luo J, Cai Q, et al. MicroRNA-125b suppresses the development of bladder cancer by targeting E2F3. Int J Cancer 2011; 128(8): 1758-69.
[http://dx.doi.org/10.1002/ijc.25509] [PMID: 20549700]
[51]
Volinia S, Calin GA, Liu CG, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 2006; 103(7): 2257-61.
[http://dx.doi.org/10.1073/pnas.0510565103] [PMID: 16461460]
[52]
Benetti R, Gonzalo S, Jaco I, et al. A mammalian microRNA cluster controls DNA methylation and telomere recombination via Rbl2-dependent regulation of DNA methyltransferases. Nat Struct Mol Biol 2008; 15(3): 268-79.
[http://dx.doi.org/10.1038/nsmb.1399] [PMID: 18311151]
[53]
Wang Q, Li YC, Wang J, et al. miR-17-92 cluster accelerates adipocyte differentiation by negatively regulating tumor-suppressor Rb2/p130. Proc Natl Acad Sci USA 2008; 105(8): 2889-94.
[http://dx.doi.org/10.1073/pnas.0800178105] [PMID: 18287052]
[54]
Cloonan N, Brown MK, Steptoe AL, et al. The miR-17-5p microRNA is a key regulator of the G1/S phase cell cycle transition. Genome Biol 2008; 9(8): R127.
[http://dx.doi.org/10.1186/gb-2008-9-8-r127] [PMID: 18700987]
[55]
Malhas A, Saunders NJ, Vaux DJ. The nuclear envelope can control gene expression and cell cycle progression via miRNA regulation. Cell Cycle 2010; 9(3): 531-9.
[http://dx.doi.org/10.4161/cc.9.3.10511] [PMID: 20081371]
[56]
Ivanovska I, Ball AS, Diaz RL, et al. MicroRNAs in the miR-106b family regulate p21/CDKN1A and promote cell cycle progression. Mol Cell Biol 2008; 28(7): 2167-74.
[http://dx.doi.org/10.1128/MCB.01977-07] [PMID: 18212054]
[57]
Kim YK, Yu J, Han TS, et al. Functional links between clustered microRNAs: suppression of cell-cycle inhibitors by microRNA clusters in gastric cancer. Nucleic Acids Res 2009; 37(5): 1672-81.
[http://dx.doi.org/10.1093/nar/gkp002] [PMID: 19153141]
[58]
Visone R, Russo L, Pallante P, et al. MicroRNAs (miR)-221 and miR-222, both overexpressed in human thyroid papillary carcinomas, regulate p27Kip1 protein levels and cell cycle. Endocr Relat Cancer 2007; 14(3): 791-8.
[http://dx.doi.org/10.1677/ERC-07-0129] [PMID: 17914108]
[59]
Wang X, Gocek E, Liu CG, Studzinski GP. MicroRNAs181 regulate the expression of p27Kip1 in human myeloid leukemia cells induced to differentiate by 1,25-dihydroxyvitamin D3. Cell Cycle 2009; 8(5): 736-41.
[http://dx.doi.org/10.4161/cc.8.5.7870] [PMID: 19221487]
[60]
Miller TE, Ghoshal K, Ramaswamy B, et al. MicroRNA-221/222 confers tamoxifen resistance in breast cancer by targeting p27Kip1. J Biol Chem 2008; 283(44): 29897-903.
[http://dx.doi.org/10.1074/jbc.M804612200] [PMID: 18708351]
[61]
Qi J, Yu JY, Shcherbata HR, et al. microRNAs regulate human embryonic stem cell division. Cell Cycle 2009; 8(22): 3729-41.
[http://dx.doi.org/10.4161/cc.8.22.10033] [PMID: 19823043]
[62]
Butz H, Likó I, Czirják S, et al. Down-regulation of Wee1 kinase by a specific subset of microRNA in human sporadic pituitary adenomas. J Clin Endocrinol Metab 2010; 95(10): E181-91.
[http://dx.doi.org/10.1210/jc.2010-0581] [PMID: 20668041]
[63]
Glover DM, Hagan IM, Tavares ÁAM. Polo-like kinases: a team that plays throughout mitosis. Genes Dev 1998; 12(24): 3777-87.
[http://dx.doi.org/10.1101/gad.12.24.3777] [PMID: 9869630]
[64]
Shi W, Alajez NM, Bastianutto C, et al. Significance of Plk1 regulation by miR-100 in human nasopharyngeal cancer. Int J Cancer 2010; 126(9): 2036-48.
[http://dx.doi.org/10.1002/ijc.24880] [PMID: 19739117]
[65]
Bader AG. miR-34 - a microRNA replacement therapy is headed to the clinic. Front Genet 2012; 3: 120.
[http://dx.doi.org/10.3389/fgene.2012.00120] [PMID: 22783274]
[66]
Ji Q, Hao X, Zhang M, et al. MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS One 2009; 4(8) e6816
[http://dx.doi.org/10.1371/journal.pone.0006816] [PMID: 19714243]
[67]
Li N, Fu H, Tie Y, et al. miR-34a inhibits migration and invasion by down-regulation of c-Met expression in human hepatocellular carcinoma cells. Cancer Lett 2009; 275(1): 44-53.
[http://dx.doi.org/10.1016/j.canlet.2008.09.035] [PMID: 19006648]
[68]
Tryndyak VP, Ross SA, Beland FA, Pogribny IP. Down-regulation of the microRNAs miR-34a, miR-127, and miR-200b in rat liver during hepatocarcinogenesis induced by a methyl-deficient diet. Mol Carcinog 2009; 48(6): 479-87.
[http://dx.doi.org/10.1002/mc.20484] [PMID: 18942116]
[69]
Tian YW, Shen Q, Jiang QF, Wang YX, Li K, Xue HZ. Decreased levels of miR-34a and miR-217 act as predictor biomarkers of aggressive progression and poor prognosis in hepatocellular carcinoma. Minerva Med 2017; 108(2): 108-13.
[http://dx.doi.org/10.23736/S0026-4806.16.04616-4] [PMID: 27879964]
[70]
Wang X-P, Zhou J, Han M, et al. MicroRNA-34a regulates liver regeneration and the development of liver cancer in rats by targeting Notch signaling pathway. Oncotarget 2017; 8(8): 13264-76.
[http://dx.doi.org/10.18632/oncotarget.14807] [PMID: 28129650]
[71]
Misso G, Di Martino MT, De Rosa G, et al. Mir-34: a new weapon against cancer? Mol Ther Nucleic Acids 2014; 3 e194
[http://dx.doi.org/10.1038/mtna.2014.47] [PMID: 25247240]
[72]
Wei W, Tang H, Tang L. MicroRNA-34a inhibits metastasis in liver cancer cells. Oncol Lett 2018; 16(6): 6960-5.
[http://dx.doi.org/10.3892/ol.2018.9555] [PMID: 30546428]
[73]
Pok S, Wen V, Shackel N, et al. Cyclin E facilitates dysplastic hepatocytes to bypass G1/S checkpoint in hepatocarcinogenesis. J Gastroenterol Hepatol 2013; 28(9): 1545-54.
[http://dx.doi.org/10.1111/jgh.12216] [PMID: 23574010]
[74]
Han R, Chen X, Li Y, Zhang S, Li R, Lu L. MicroRNA-34a suppresses aggressiveness of hepatocellular carcinoma by modulating E2F1, E2F3, and Caspase-3. Cancer Manag Res 2019; 11: 2963-76.
[http://dx.doi.org/10.2147/CMAR.S202664] [PMID: 31114344]
[75]
Brock M, Samillan VJ, Trenkmann M, et al. AntagomiR directed against miR-20a restores functional BMPR2 signalling and prevents vascular remodelling in hypoxia-induced pulmonary hypertension. Eur Heart J 2014; 35(45): 3203-11.
[http://dx.doi.org/10.1093/eurheartj/ehs060] [PMID: 22450430]
[76]
Wahlquist C, Jeong D, Rojas-Muñoz A, et al. Inhibition of miR-25 improves cardiac contractility in the failing heart. Nature 2014; 508(7497): 531-5.
[http://dx.doi.org/10.1038/nature13073] [PMID: 24670661]
[77]
Xu LJ, Ouyang YB, Xiong X, Stary CM, Giffard RG. Post-stroke treatment with miR-181 antagomir reduces injury and improves long-term behavioral recovery in mice after focal cerebral ischemia. Exp Neurol 2015; 264: 1-7.
[http://dx.doi.org/10.1016/j.expneurol.2014.11.007] [PMID: 25433215]
[78]
Kwekkeboom RFJ, Sluijter JPG, van Middelaar BJ, et al. Increased local delivery of antagomir therapeutics to the rodent myocardium using ultrasound and microbubbles. J Control Release 2016; 222: 18-31.
[http://dx.doi.org/10.1016/j.jconrel.2015.11.020] [PMID: 26616760]
[79]
Briones C, Moreno M. Applications of Peptide Nucleic Acids (PNAs) and Locked Nucleic Acids (LNAs) in biosensor development. Anal Bioanal Chem 2012; 402(10): 3071-89.
[http://dx.doi.org/10.1007/s00216-012-5742-z] [PMID: 22297860]
[80]
Fabani MM, Abreu-Goodger C, Williams D, et al. Efficient inhibition of miR-155 function in vivo by peptide nucleic acids. Nucleic Acids Res 2010; 38(13): 4466-75.
[http://dx.doi.org/10.1093/nar/gkq160] [PMID: 20223773]
[81]
Ebert MS, Sharp PA. MicroRNA sponges: progress and possibilities. RNA 2010; 16(11): 2043-50.
[http://dx.doi.org/10.1261/rna.2414110] [PMID: 20855538]
[82]
Merhautová J, Vychytilová-Faltejsková P, Demlová R, et al. Systemic administration of miRNA mimics by liposomal delivery system in animal model of colorectal carcinoma. Physiol Res 2016; 65(Suppl. 4): S481-8.https://www.ncbi.nlm.nih.gov/pubmed/28006930
[PMID: 28006930]
[83]
Rupaimoole R, Slack FJ. MicroRNA therapeutics: towards a new era for the management of cancer and other diseases. Nat Rev Drug Discov 2017; 16(3): 203-22.
[http://dx.doi.org/10.1038/nrd.2016.246] [PMID: 28209991]
[84]
Yu F, Yao H, Zhu P, et al. Let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 2007; 131(6): 1109-23.
[http://dx.doi.org/10.1016/j.cell.2007.10.054] [PMID: 18083101]
[85]
Li Z, Shi K, Guan L, et al. ROS leads to MnSOD upregulation through ERK2 translocation and p53 activation in selenite-induced apoptosis of NB4 cells. FEBS Lett 2010; 584(11): 2291-7.
[http://dx.doi.org/10.1016/j.febslet.2010.03.040] [PMID: 20353787]
[86]
Zhao Y, Deng C, Wang J, et al. Let-7 family miRNAs regulate estrogen receptor alpha signaling in estrogen receptor positive breast cancer. Breast Cancer Res Treat 2011; 127(1): 69-80.
[http://dx.doi.org/10.1007/s10549-010-0972-2] [PMID: 20535543]
[87]
Yong SL, Dutta A. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev 2007; 21: 1025-30.
[http://dx.doi.org/10.1101/gad.1540407]
[88]
Ohno S, Takanashi M, Sudo K, et al. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther 2013; 21(1): 185-91.
[http://dx.doi.org/10.1038/mt.2012.180] [PMID: 23032975]
[89]
Cortez MA, Valdecanas D, Zhang X, et al. Therapeutic delivery of miR-200c enhances radiosensitivity in lung cancer. Mol Ther 2014; 22(8): 1494-503.
[http://dx.doi.org/10.1038/mt.2014.79] [PMID: 24791940]
[90]
Coussens LM, Werb Z. Inflammation and cancer. Nature 2002; 420(6917): 860-7.
[http://dx.doi.org/10.1038/nature01322] [PMID: 12490959]
[91]
Ji J, Shi J, Budhu A, et al. MicroRNA expression, survival, and response to interferon in liver cancer. N Engl J Med 2009; 361(15): 1437-47.
[http://dx.doi.org/10.1056/NEJMoa0901282] [PMID: 19812400]
[92]
Yang D, Sun Y, Hu L, et al. Integrated analyses identify a master microRNA regulatory network for the mesenchymal subtype in serous ovarian cancer. Cancer Cell 2013; 23(2): 186-99.
[http://dx.doi.org/10.1016/j.ccr.2012.12.020] [PMID: 23410973]
[93]
Nishimura M, Jung EJ, Shah MY, et al. Therapeutic synergy between microRNA and siRNA in ovarian cancer treatment. Cancer Discov 2013; 3(11): 1302-15.
[http://dx.doi.org/10.1158/2159-8290.CD-13-0159] [PMID: 24002999]
[94]
Rupaimoole R, Ivan C, Yang D, et al. Hypoxia-upregulated microRNA-630 targets Dicer, leading to increased tumor progression. Oncogene 2016; 35(33): 4312-20.
[http://dx.doi.org/10.1038/onc.2015.492] [PMID: 26725326]
[95]
Calin GA, Cimmino A, Fabbri M, et al. MiR-15a and miR-16-1 cluster functions in human leukemia. Proc Natl Acad Sci USA 2008; 105(13): 5166-71.
[http://dx.doi.org/10.1073/pnas.0800121105] [PMID: 18362358]
[96]
Stahlhut C, Slack FJ. Combinatorial action of microRNAs let-7 and miR-34 effectively synergizes with erlotinib to suppress non-small cell lung cancer cell proliferation. Cell Cycle 2015; 14(13): 2171-80.
[http://dx.doi.org/10.1080/15384101.2014.1003008] [PMID: 25714397]
[97]
Gabriely G, Yi M, Narayan RS, et al. Human glioma growth is controlled by microRNA-10b. Cancer Res 2011; 71(10): 3563-72.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-3568] [PMID: 21471404]
[98]
Yoo B, Kavishwar A, Ross A, et al. Combining miR-10b-targeted nanotherapy with low-dose doxorubicin elicits durable regressions of metastatic breast cancer. Cancer Res 2015; 75(20): 4407-15.
[http://dx.doi.org/10.1158/0008-5472.CAN-15-0888] [PMID: 26359455]
[99]
Garofalo M, Di Leva G, Romano G, et al. miR-221&222 regulate TRAIL resistance and enhance tumorigenicity through PTEN and TIMP3 downregulation. Cancer Cell 2009; 16(6): 498-509.
[http://dx.doi.org/10.1016/j.ccr.2009.10.014] [PMID: 19962668]
[100]
le Sage C, Nagel R, Egan DA, et al. Regulation of the p27(Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO J 2007; 26(15): 3699-708.
[http://dx.doi.org/10.1038/sj.emboj.7601790] [PMID: 17627278]
[101]
Babar IA, Cheng CJ, Booth CJ, et al. Nanoparticle-based therapy in an in vivo microRNA-155 (miR-155)-dependent mouse model of lymphoma. Proc Natl Acad Sci USA 2012; 109(26): E1695-704.
[http://dx.doi.org/10.1073/pnas.1201516109] [PMID: 22685206]
[102]
Cheng CJ, Bahal R, Babar IA, et al. MicroRNA silencing for cancer therapy targeted to the tumour microenvironment. Nature 2015; 518(7537): 107-10.
[http://dx.doi.org/10.1038/nature13905] [PMID: 25409146]
[103]
Wang Y, Blelloch R. Cell cycle regulation by microRNAs in stem cells. Results Probl Cell Differ 2011; 53: 459-72.
[http://dx.doi.org/10.1007/978-3-642-19065-0_19] [PMID: 21630156]
[104]
Houbaviy HB, Murray MF, Sharp PA. Embryonic stem cell-specific microRNAs. Dev Cell 2003; 5(2): 351-8.
[http://dx.doi.org/10.1016/S1534-5807(03)00227-2] [PMID: 12919684]
[105]
Melton C, Judson RL, Blelloch R. Opposing microRNA families regulate self-renewal in mouse embryonic stem cells. Nature 2010; 463(7281): 621-6.
[http://dx.doi.org/10.1038/nature08725] [PMID: 20054295]
[106]
Lichner Z, Páll E, Kerekes A, et al. The miR-290-295 cluster promotes pluripotency maintenance by regulating cell cycle phase distribution in mouse embryonic stem cells. Differentiation 2011; 81(1): 11-24.
[http://dx.doi.org/10.1016/j.diff.2010.08.002] [PMID: 20864249]
[107]
Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126(4): 663-76.
[http://dx.doi.org/10.1016/j.cell.2006.07.024] [PMID: 16904174]
[108]
Zheng GXY, Ravi A, Calabrese JM, et al. A latent pro-survival function for the mir-290-295 cluster in mouse embryonic stem cells. PLoS Genet 2011; 7(5) e1002054
[http://dx.doi.org/10.1371/journal.pgen.1002054] [PMID: 21573140]
[109]
Hao J, Duan FF, Wang Y. MicroRNAs and RNA binding protein regulators of microRNAs in the control of pluripotency and reprogramming. Curr Opin Genet Dev 2017; 46: 95-103.
[http://dx.doi.org/10.1016/j.gde.2017.07.001] [PMID: 28753462]
[110]
Yuan K, Ai WB, Wan LY, Tan X, Wu JF. The miR-290-295 cluster as multi-faceted players in mouse embryonic stem cells. Cell Biosci 2017; 7: 38.
[http://dx.doi.org/10.1186/s13578-017-0166-2] [PMID: 28794853]
[111]
Wang Y, Baskerville S, Shenoy A, Babiarz JE, Baehner L, Blelloch R. Embryonic stem cell-specific microRNAs regulate the G1-S transition and promote rapid proliferation. Nat Genet 2008; 40(12): 1478-83.
[http://dx.doi.org/10.1038/ng.250] [PMID: 18978791]
[112]
Kanellopoulou C, Gilpatrick T, Kilaru G, et al. Reprogramming of polycomb-mediated gene silencing in embryonic stem cells by the miR-290 family and the methyltransferase Ash1l. Stem Cell Reports 2015; 5(6): 971-8.
[http://dx.doi.org/10.1016/j.stemcr.2015.10.001] [PMID: 26549848]
[113]
Richly H, Aloia L, Di Croce L. Roles of the Polycomb group proteins in stem cells and cancer. Cell Death Dis 2011; 2 e204
[http://dx.doi.org/10.1038/cddis.2011.84] [PMID: 21881606]
[114]
Li Y, Choi PS, Casey SC, Dill DL, Felsher DW. MYC through miR-17-92 suppresses specific target genes to maintain survival, autonomous proliferation, and a neoplastic state. Cancer Cell 2014; 26(2): 262-72.
[http://dx.doi.org/10.1016/j.ccr.2014.06.014] [PMID: 25117713]
[115]
Aguda BD, Kim Y, Piper-Hunter MG, Friedman A, Marsh CB. microRNA regulation of a cancer network: consequences of the feedback loops involving miR-17-92, E2F, and Myc. Proc Natl Acad Sci USA 2008; 105(50): 19678-83.
[http://dx.doi.org/10.1073/pnas.0811166106] [PMID: 19066217]
[116]
Kuo CH, Deng JH, Deng Q, Ying SY. A novel role of miR-302/367 in reprogramming. Biochem Biophys Res Commun 2012; 417(1): 11-6.
[http://dx.doi.org/10.1016/j.bbrc.2011.11.058] [PMID: 22138244]
[117]
Greer Card DA, Hebbar PB, Li L, et al. Oct4/Sox2-regulated miR-302 targets cyclin D1 in human embryonic stem cells. Mol Cell Biol 2008; 28(20): 6426-38.
[http://dx.doi.org/10.1128/MCB.00359-08]
[118]
Anokye-Danso F, Trivedi CM, Juhr D, et al. Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 2011; 8(4): 376-88.
[http://dx.doi.org/10.1016/j.stem.2011.03.001] [PMID: 21474102]
[119]
Lipchina I, Studer L, Betel D. The expanding role of miR-302-367 in pluripotency and reprogramming. Cell Cycle 2012; 11(8): 1517-23.
[http://dx.doi.org/10.4161/cc.19846] [PMID: 22436490]
[120]
Dolezalova D, Mraz M, Barta T, et al. MicroRNAs regulate p21(Waf1/Cip1) protein expression and the DNA damage response in human embryonic stem cells. Stem Cells 2012; 30(7): 1362-72.
[http://dx.doi.org/10.1002/stem.1108] [PMID: 22511267]
[121]
Liang Y, Li Y, Li Z, et al. Mechanism of folate deficiency-induced apoptosis in mouse embryonic stem cells: cell cycle arrest/apoptosis in G1/G0 mediated by microRNA-302a and tumor suppressor gene Lats2. Int J Biochem Cell Biol 2012; 44(11): 1750-60.
[http://dx.doi.org/10.1016/j.biocel.2012.07.014] [PMID: 22828209]

© 2024 Bentham Science Publishers | Privacy Policy