MicroRNAs driving invasion and metastasis in ovarian cancer: Opportunities for translational medicine (Review)
- Authors:
- Carlos Palma Flores
- Raúl García-Vázquez
- Dolores Gallardo Rincón
- Erika Ruiz-García
- Horacio Astudillo de la Vega
- Laurence A. Marchat
- Yarely M. Salinas Vera
- César López-Camarillo
-
Affiliations: Catedratico CONACYT, Instituto Politécnico Nacional, Mexico City, Mexico, Molecular Biomedicine Program and Biotechnology Network, Instituto Politécnico Nacional, Mexico City, Mexico, Translational Medicine Laboratory, National Institute of Cancerology, Mexico City, Mexico, Laboratory of Translational Cancer Research and Cellular Therapy, National Medical Center ‘Siglo XXI’, Mexico City, Mexico, Autonomous University of Mexico City, Genomics Sciences Program, Mexico City, Mexico - Published online on: April 4, 2017 https://doi.org/10.3892/ijo.2017.3948
- Pages: 1461-1476
This article is mentioned in:
Abstract
![]() |
![]() |
![]() |
Vaughan S, Coward JI, Bast RC Jr, Berchuck A, Berek JS, Brenton JD, Coukos G, Crum CC, Drapkin R, Etemadmoghadam D, et al: Rethinking ovarian cancer: Recommendations for improving outcomes. Nat Rev Cancer. 11:719–725. 2011. View Article : Google Scholar : PubMed/NCBI | |
Ledermann JA, Marth C, Carey MS, Birrer M, Bowtell DD, Kaye S, McNeish I, Oza A, Scambia G, Rustin G, et al Gynecologic Cancer InterGroup: Role of molecular agents and targeted therapy in clinical trials for women with ovarian cancer. Int J Gynecol Cancer. 21:763–770. 2011. View Article : Google Scholar : PubMed/NCBI | |
Kim VN: MicroRNA biogenesis: Coordinated cropping and dicing. Nat Rev Mol Cell Biol. 6:376–385. 2005. View Article : Google Scholar : PubMed/NCBI | |
Nguyen DX, Bos PD and Massagué J: Metastasis: From dissemination to organ-specific colonization. Nat Rev Cancer. 9:274–284. 2009. View Article : Google Scholar : PubMed/NCBI | |
Lopez-Camarillo C, Marchat LA, Arechaga-Ocampo E, Perez-Plasencia C, Del Moral-Hernandez O, Castaneda-Ortiz EJ and Rodriguez-Cuevas S: MetastamiRs: Non-coding MicroRNAs driving cancer invasion and metastasis. Int J Mol Sci. 13:1347–1379. 2012. View Article : Google Scholar : PubMed/NCBI | |
White NM, Fatoohi E, Metias M, Jung K, Stephan C and Yousef GM: Metastamirs: A stepping stone towards improved cancer management. Nat Rev Clin Oncol. 8:75–84. 2011. View Article : Google Scholar | |
Cai X, Hagedorn CH and Cullen BR: Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA. 10:1957–1966. 2004. View Article : Google Scholar : PubMed/NCBI | |
Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Rådmark O, Kim S, et al: The nuclear RNase III Drosha initiates microRNA processing. Nature. 425:415–419. 2003. View Article : Google Scholar : PubMed/NCBI | |
Vasudevan S, Tong Y and Steitz JA: Switching from repression to activation: microRNAs can up-regulate translation. Science. 318:1931–1934. 2007. View Article : Google Scholar : PubMed/NCBI | |
Eulalio A, Behm-Ansmant I and Izaurralde E: P bodies: At the crossroads of post-transcriptional pathways. Nat Rev Mol Cell Biol. 8:9–22. 2007. View Article : Google Scholar | |
Sen GL and Blau HM: Argonaute 2/RISC resides in sites of mammalian mRNA decay known as cytoplasmic bodies. Nat Cell Biol. 7:633–636. 2005. View Article : Google Scholar : PubMed/NCBI | |
Esquela-Kerscher A and Slack FJ: Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer. 6:259–269. 2006. View Article : Google Scholar : PubMed/NCBI | |
Zhang B, Pan X, Cobb GP and Anderson TA: microRNAs as oncogenes and tumor suppressors. Dev Biol. 302:1–12. 2007. View Article : Google Scholar | |
Nishimura M, Jung E-J, Shah MY, Lu C, Spizzo R, Shimizu M, Han HD, Ivan C, Rossi S, Zhang X, et al: Therapeutic synergy between microRNA and siRNA in ovarian cancer treatment. Cancer Discov. 3:1302–1315. 2013. View Article : Google Scholar : PubMed/NCBI | |
Wang L, Mezencev R, Švajdler M, Benigno BB and McDonald JF: Ectopic over-expression of miR-429 induces mesenchymal-to-epithelial transition (MET) and increased drug sensitivity in meta- stasizing ovarian cancer cells. Gynecol Oncol. 134:96–103. 2014. View Article : Google Scholar : PubMed/NCBI | |
Micalizzi DS, Farabaugh SM and Ford HL: Epithelial-mesenchymal transition in cancer: Parallels between normal development and tumor progression. J Mammary Gland Biol Neoplasia. 15:117–134. 2010. View Article : Google Scholar : PubMed/NCBI | |
Corallino S, Malabarba MG, Zobel M, Di Fiore PP and Scita G: Epithelial-to-mesenchymal plasticity harnesses endocytic circuitries. Front Oncol. 5:452015. View Article : Google Scholar : PubMed/NCBI | |
Oskarsson T, Batlle E and Massagué J: Metastatic stem cells: Sources, niches, and vital pathways. Cell Stem Cell. 14:306–321. 2014. View Article : Google Scholar : PubMed/NCBI | |
Kalluri R and Weinberg RA: The basics of epithelial-mesenchymal transition. J Clin Invest. 119:1420–1428. 2009. View Article : Google Scholar : PubMed/NCBI | |
Garg M: Targeting microRNAs in epithelial-to-mesenchymal transition-induced cancer stem cells: Therapeutic approaches in cancer. Expert Opin Ther Targets. 19:285–297. 2015. View Article : Google Scholar : PubMed/NCBI | |
Abba ML, Patil N, Leupold JH and Allgayer H: MicroRNA regulation of epithelial to mesenchymal transition. J Clin Med. 5:82016. View Article : Google Scholar : | |
Huber MA, Kraut N and Beug H: Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol. 17:548–558. 2005. View Article : Google Scholar : PubMed/NCBI | |
Heuberger J and Birchmeier W: Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. Cold Spring Harb Perspect Biol. 2:a0029152010. View Article : Google Scholar : PubMed/NCBI | |
Arend RC, Londoño-Joshi AI, Straughn JM Jr and Buchsbaum DJ: The Wnt/β-catenin pathway in ovarian cancer: A review. Gynecol Oncol. 131:772–779. 2013. View Article : Google Scholar : PubMed/NCBI | |
Ke Z, Caiping S, Qing Z and Xiaojing W: Sonic hedgehog-Gli1 signals promote epithelial-mesenchymal transition in ovarian cancer by mediating PI3K/AKT pathway. Med Oncol. 32:3682015. View Article : Google Scholar | |
Fang D, Chen H, Zhu JY, Wang W, Teng Y, Ding HF, Jing Q, Su SB and Huang S: Epithelial-mesenchymal transition of ovarian cancer cells is sustained by Rac1 through simultaneous activation of MEK1/2 and Src signaling pathways. Oncogene Sep. 12:2016Epub ahead of print. View Article : Google Scholar | |
Talbot LJ, Bhattacharya SD and Kuo PC: Epithelial-mesenchymal transition, the tumor microenvironment, and metastatic behavior of epithelial malignancies. Int J Biochem Mol Biol. 3:117–136. 2012.PubMed/NCBI | |
Fuxe J, Vincent T and Garcia de Herreros A: Transcriptional crosstalk between TGF-β and stem cell pathways in tumor cell invasion: Role of EMT promoting Smad complexes. Cell Cycle. 9:2363–2374. 2010. View Article : Google Scholar : PubMed/NCBI | |
Moustakas A and Heldin CH: Signaling networks guiding epithelial-mesenchymal transitions during embryogenesis and cancer progression. Cancer Sci. 98:1512–1520. 2007. View Article : Google Scholar : PubMed/NCBI | |
Gibbons DL, Lin W, Creighton CJ, Rizvi ZH, Gregory PA, Goodall GJ, Thilaganathan N, Du L, Zhang Y, Pertsemlidis A, et al: Contextual extracellular cues promote tumor cell EMT and metastasis by regulating miR-200 family expression. Genes Dev. 23:2140–2151. 2009. View Article : Google Scholar : PubMed/NCBI | |
Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, Vadas MA, Khew-Goodall Y and Goodall GJ: The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol. 10:593–601. 2008. View Article : Google Scholar : PubMed/NCBI | |
Korpal M, Lee ES, Hu G and Kang Y: The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem. 283:14910–14914. 2008. View Article : Google Scholar : PubMed/NCBI | |
Park SM, Gaur AB, Lengyel E and Peter ME: The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 22:894–907. 2008. View Article : Google Scholar : PubMed/NCBI | |
Bendoraite A, Knouf EC, Garg KS, Parkin RK, Kroh EM, O'Briant KC, Ventura AP, Godwin AK, Karlan BY, Drescher CW, et al: Regulation of miR-200 family microRNAs and ZEB transcription factors in ovarian cancer: Evidence supporting a mesothelial-to-epithelial transition. Gynecol Oncol. 116:117–125. 2010. View Article : Google Scholar : | |
Chen J, Wang L, Matyunina LV, Hill CG and McDonald JF: Overexpression of miR-429 induces mesenchymal-to-epithelial transition (MET) in metastatic ovarian cancer cells. Gynecol Oncol. 121:200–205. 2011. View Article : Google Scholar : PubMed/NCBI | |
Jabbari N, Reavis AN and McDonald JF: Sequence variation among members of the miR-200 microRNA family is correlated with variation in the ability to induce hallmarks of mesenchymal-epithelial transition in ovarian cancer cells. J Ovarian Res. 7:122014. View Article : Google Scholar : PubMed/NCBI | |
Lu YM, Shang C, Ou YL, Yin D, Li YN, Li X, Wang N and Zhang SL: miR-200c modulates ovarian cancer cell metastasis potential by targeting zinc finger E-box-binding homeobox 2 (ZEB2) expression. Med Oncol. 31:1342014. View Article : Google Scholar : PubMed/NCBI | |
Chen D, Zhang Y, Wang J, Chen J, Yang C, Cai K, Wang X, Shi F and Dou J: MicroRNA-200c overexpression inhibits tumorige-nicity and metastasis of CD117+CD44+ ovarian cancer stem cells by regulating epithelial-mesenchymal transition. J Ovarian Res. 6:502013. View Article : Google Scholar | |
Wang Y, Yan S, Liu X, Zhang W, Li Y, Dong R, Zhang Q, Yang Q, Yuan C, Shen K, et al: miR-1236-3p represses the cell migration and invasion abilities by targeting ZEB1 in high-grade serous ovarian carcinoma. Oncol Rep. 31:1905–1910. 2014.PubMed/NCBI | |
Wu Q, Guo R, Lin M, Zhou B and Wang Y: MicroRNA-200a inhibits CD133/1+ ovarian cancer stem cells migration and invasion by targeting E-cadherin repressor ZEB2. Gynecol Oncol. 122:149–154. 2011. View Article : Google Scholar : PubMed/NCBI | |
Vang S, Wu HT, Fischer A, Miller DH, Maclaughlan S, Douglass E, Comisar L, Steinhoff M, Collins C, Smith PJ, et al: Identification of ovarian cancer metastatic miRNAs. PloS One. 8:e582262013. View Article : Google Scholar : PubMed/NCBI | |
Jin M, Yang Z, Ye W, Xu H and Hua X: MicroRNA-150 predicts a favorable prognosis in patients with epithelial ovarian cancer, and inhibits cell invasion and metastasis by suppressing transcriptional repressor ZEB1. PloS One. 9:e1039652014. View Article : Google Scholar : PubMed/NCBI | |
Chen Y, Luo J, Tian R, Sun H and Zou S: miR-373 negatively regulates methyl-CpG-binding domain protein 2 (MBD2) in hilar cholangiocarcinoma. Dig Dis Sci. 56:1693–1701. 2011. View Article : Google Scholar | |
Oppenheimer H, Kumar A, Meir H, Schwartz I, Zini A, Haze A, Kandel L, Mattan Y, Liebergall M and Dvir-Ginzberg M: Set7/9 impacts COL2A1 expression through binding and repression of SirT1 histone deacetylation. J Bone Miner Res. 29:348–360. 2014. View Article : Google Scholar | |
Zhou J, Xie M, Shi Y, Luo B, Gong G, Li J, Wang J, Zhao W, Zi Y, Wu X, et al: MicroRNA-153 functions as a tumor suppressor by targeting SET7 and ZEB2 in ovarian cancer cells. Oncol Rep. 34:111–120. 2015.PubMed/NCBI | |
Kim YS, Yi BR, Kim NH and Choi KC: Role of the epithelial-mesenchymal transition and its effects on embryonic stem cells. Exp Mol Med. 46:e1082014. View Article : Google Scholar : PubMed/NCBI | |
Yang D, Sun Y, Hu L, Zheng H, Ji P, Pecot CV, Zhao Y, Reynolds S, Cheng H, Rupaimoole R, et al: Integrated analyses identify a master microRNA regulatory network for the mesenchymal subtype in serous ovarian cancer. Cancer Cell. 23:186–199. 2013. View Article : Google Scholar : PubMed/NCBI | |
Sun Y, Mezzanzanica D and Zhang W: MiR-506: A Multitasker in suppression of the epithelial-to-mesenchymal transition. RNA Dis. 1:e4472014.PubMed/NCBI | |
Sun Y, Hu L, Zheng H, Bagnoli M, Guo Y, Rupaimoole R, Rodriguez-Aguayo C, Lopez-Berestein G, Ji P, Chen K, et al: MiR-506 inhibits multiple targets in the epithelial-to-mesenchymal transition network and is associated with good prognosis in epithelial ovarian cancer. J Pathol. 235:25–36. 2015. View Article : Google Scholar | |
Zhao G, Guo Y, Chen Z, Wang Y, Yang C, Dudas A, Du Z, Liu W, Zou Y, Szabo E, et al: miR-203 functions as a tumor suppressor by inhibiting epithelial to mesenchymal transition in ovarian cancer. J Cancer Sci Ther. 7:34–43. 2015. | |
Ye Z, Zhao L, Li J, Chen W and Li X: miR-30d blocked transforming growth factor β1-induced epithelial-mesenchymal transition by targeting Snail in ovarian cancer cells. Int J Gynecol Cancer. 25:1574–1581. 2015. View Article : Google Scholar : PubMed/NCBI | |
Siemens H, Jackstadt R, Hünten S, Kaller M, Menssen A, Götz U and Hermeking H: miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions. Cell Cycle. 10:4256–4271. 2011. View Article : Google Scholar : PubMed/NCBI | |
Su JL, Chen PB, Chen YH, Chen SC, Chang YW, Jan YH, Cheng X, Hsiao M and Hung MC: Downregulation of microRNA miR-520h by E1A contributes to anticancer activity. Cancer Res. 70:5096–5108. 2010. View Article : Google Scholar : PubMed/NCBI | |
Wu J and Wei JJ: HMGA2 and high-grade serous ovarian carcinoma. J Mol Med (Berl). 91:1155–1165. 2013. View Article : Google Scholar | |
Wu J, Liu Z, Shao C, Gong Y, Hernando E, Lee P, Narita M, Muller W, Liu J and Wei JJ: HMGA2 overexpression-induced ovarian surface epithelial transformation is mediated through regulation of EMT genes. Cancer Res. 71:349–359. 2011. View Article : Google Scholar : PubMed/NCBI | |
Tanaka T, Arai M, Wu S, Kanda T, Miyauchi H, Imazeki F, Matsubara H and Yokosuka O: Epigenetic silencing of microRNA-373 plays an important role in regulating cell proliferation in colon cancer. Oncol Rep. 26:1329–1335. 2011.PubMed/NCBI | |
Zhang Y, Zhao FJ, Chen LL, Wang LQ, Nephew KP, Wu YL and Zhang S: MiR-373 targeting of the Rab22a oncogene suppresses tumor invasion and metastasis in ovarian cancer. Oncotarget. 5:12291–12303. 2014. View Article : Google Scholar : PubMed/NCBI | |
Hsiao CP, Araneta M, Wang XM and Saligan LN: The association of IFI27 expression and fatigue intensification during localized radiation therapy: Implication of a para-inflammatory bystander response. Int J Mol Sci. 14:16943–16957. 2013. View Article : Google Scholar : PubMed/NCBI | |
Li S, Xie Y, Zhang W, Gao J, Wang M, Zheng G, Yin X, Xia H and Tao X: Interferon alpha-inducible protein 27 promotes epithelial-mesenchymal transition and induces ovarian tumorigenicity and stemness. J Surg Res. 193:255–264. 2015. View Article : Google Scholar | |
Baskar S, Wiestner A, Wilson WH, Pastan I and Rader C: Targeting malignant B cells with an immunotoxin against ROR1. MAbs. 4:349–361. 2012. View Article : Google Scholar : PubMed/NCBI | |
Tan H, He Q, Gong G, Wang Y, Li J, Wang J, Zhu D and Wu X: miR-382 inhibits migration and invasion by targeting ROR1 through regulating EMT in ovarian cancer. Int J Oncol. 48:181–190. 2016. | |
Yeh YM, Chuang CM, Chao KC and Wang LH: MicroRNA-138 suppresses ovarian cancer cell invasion and metastasis by targeting SOX4 and HIF-1α. Int J Cancer. 133:867–878. 2013. View Article : Google Scholar : PubMed/NCBI | |
Cowden Dahl KD, Dahl R, Kruichak JN and Hudson LG: The epidermal growth factor receptor responsive miR-125a represses mesenchymal morphology in ovarian cancer cells. Neoplasia. 11:1208–1215. 2009. View Article : Google Scholar : PubMed/NCBI | |
Bobbs A, Gellerman K, Hallas WM, Joseph S, Yang C, Kurkewich J and Cowden Dahl KD: ARID3B directly regulates ovarian cancer promoting genes. PloS One. 10:e01319612015. View Article : Google Scholar : PubMed/NCBI | |
Zhou X, Hu Y, Dai L, Wang Y, Zhou J, Wang W, Di W and Qiu L: MicroRNA-7 inhibits tumor metastasis and reverses epithelial-mesenchymal transition through AKT/ERK1/2 inactivation by targeting EGFR in epithelial ovarian cancer. PloS One. 9:e967182014. View Article : Google Scholar : PubMed/NCBI | |
Yuan ZQ, Sun M, Feldman RI, Wang G, Ma X, Jiang C, Coppola D, Nicosia SV and Cheng JQ: Frequent activation of AKT2 and induction of apoptosis by inhibition of phosphoinositide-3-OH kinase/Akt pathway in human ovarian cancer. Oncogene. 19:2324–2330. 2000. View Article : Google Scholar : PubMed/NCBI | |
Luo X, Dong Z, Chen Y, Yang L and Lai D: Enrichment of ovarian cancer stem-like cells is associated with epithelial to mesenchymal transition through an miRNA-activated AKT pathway. Cell Prolif. 46:436–446. 2013. View Article : Google Scholar : PubMed/NCBI | |
Parikh A, Lee C, Joseph P, Marchini S, Baccarini A, Kolev V, Romualdi C, Fruscio R, Shah H, Wang F, et al: microRNA-181a has a critical role in ovarian cancer progression through the regulation of the epithelial-mesenchymal transition. Nat Commun. 5:29772014. View Article : Google Scholar : PubMed/NCBI | |
Fang L, Li H, Wang L, Hu J, Jin T, Wang J and Yang BB: MicroRNA-17-5p promotes chemotherapeutic drug resistance and tumour metastasis of colorectal cancer by repressing PTEN expression. Oncotarget. 5:2974–2987. 2014. View Article : Google Scholar : PubMed/NCBI | |
Fang Y, Xu C and Fu Y: MicroRNA-17-5p induces drug resistance and invasion of ovarian carcinoma cells by targeting PTEN signaling. J Biol Res (Thessalon). 22:122015. View Article : Google Scholar | |
Qin W, Ren Q, Liu T, Huang Y and Wang J: MicroRNA-155 is a novel suppressor of ovarian cancer-initiating cells that targets CLDN1. FEBS Lett. 587:1434–1439. 2013. View Article : Google Scholar : PubMed/NCBI | |
Iorio MV, Visone R, Di Leva G, Donati V, Petrocca F, Casalini P, Taccioli C, Volinia S, Liu CG, Alder H, et al: MicroRNA signatures in human ovarian cancer. Cancer Res. 67:8699–8707. 2007. View Article : Google Scholar : PubMed/NCBI | |
Habata S, Iwasaki M, Sugio A, Suzuki M, Tamate M, Satohisa S, Tanaka R and Saito T: BAG3 increases the invasiveness of uterine corpus carcinoma cells by suppressing miR-29b and enhancing MMP2 expression. Oncol Rep. 33:2613–2621. 2015.PubMed/NCBI | |
Sun X, Cui M, Zhang A, Tong L, Wang K, Li K, Wang X, Sun Z and Zhang H: MiR-548c impairs migration and invasion of endo-metrial and ovarian cancer cells via downregulation of Twist. J Exp Clin Cancer Res. 35:102016. View Article : Google Scholar | |
Su N, Qiu H, Chen Y, Yang T, Yan Q and Wan X: miR-205 promotes tumor proliferation and invasion through targeting ESRRG in endometrial carcinoma. Oncol Rep. 29:2297–2302. 2013.PubMed/NCBI | |
Mozos A, Catasús L, D'Angelo E, Serrano E, Espinosa I, Ferrer I, Pons C and Prat J: The FOXO1-miR27 tandem regulates myometrial invasion in endometrioid endometrial adenocarcinoma. Hum Pathol. 45:942–951. 2014. View Article : Google Scholar : PubMed/NCBI | |
Dong M, Yang P and Hua F: MiR-191 modulates malignant transformation of endometriosis through regulating TIMP3. Med Sci Monit. 21:915–920. 2015. View Article : Google Scholar : PubMed/NCBI | |
Li S, Hu R, Wang C, Guo F, Li X and Wang S: miR-22 inhibits proliferation and invasion in estrogen receptor α-positive endometrial endometrioid carcinomas cells. Mol Med Rep. 9:2393–2399. 2014.PubMed/NCBI | |
Chen X, Yan Q, Li S, Zhou L, Yang H, Yang Y, Liu X and Wan X: Expression of the tumor suppressor miR-206 is associated with cellular proliferative inhibition and impairs invasion in ERα-positive endometrioid adenocarcinoma. Cancer Lett. 314:41–53. 2012. View Article : Google Scholar | |
Li S, Li Y, Wen Z, Kong F, Guan X and Liu W: microRNA-206 overexpression inhibits cellular proliferation and invasion of estrogen receptor α-positive ovarian cancer cells. Mol Med Rep. 9:1703–1708. 2014.PubMed/NCBI | |
Liang SH, Li J, Al-beit M, Zhang J, Ma D and Lu X: Screening and identification of potential miRNA involved in ovarian cancer invasion and metastasis. Zhonghua Zhong Liu Za Zhi. 32:650–654. 2010.In Chinese. PubMed/NCBI | |
Li J, Liang S, Yu H, Zhang J, Ma D and Lu X: An inhibitory effect of miR-22 on cell migration and invasion in ovarian cancer. Gynecol Oncol. 119:543–548. 2010. View Article : Google Scholar : PubMed/NCBI | |
Li J, Liang S, Jin H, Xu C, Ma D and Lu X: Tiam1, negatively regulated by miR-22, miR-183 and miR-31, is involved in migration, invasion and viability of ovarian cancer cells. Oncol Rep. 27:1835–1842. 2012.PubMed/NCBI | |
Wen C, Liu X, Ma H, Zhang W and Li H: miR-338-3p suppresses tumor growth of ovarian epithelial carcinoma by targeting Runx2. Int J Oncol. 46:2277–2285. 2015.PubMed/NCBI | |
Lin K-T, Yeh Y-M, Chuang C-M, Yang SY, Chang JW, Sun SP, Wang YS, Chao KC and Wang LH: Glucocorticoids mediate induction of microRNA-708 to suppress ovarian cancer metastasis through targeting Rap1B. Nat Commun. 6:59172015. View Article : Google Scholar : PubMed/NCBI | |
Zhang H, Wang Q, Zhao Q and Di W: MiR-124 inhibits the migration and invasion of ovarian cancer cells by targeting SphK1. J Ovarian Res. 6:842013. View Article : Google Scholar : PubMed/NCBI | |
Wen Z, Zhao S, Liu S, Liu Y, Li X and Li S: MicroRNA-148a inhibits migration and invasion of ovarian cancer cells via targeting sphingosine-1-phosphate receptor 1. Mol Med Rep. 12:3775–3780. 2015.PubMed/NCBI | |
Chen P, Zeng M, Zhao Y and Fang X: Upregulation of Limk1 caused by microRNA-138 loss aggravates the metastasis of ovarian cancer by activation of Limk1/cofilin signaling. Oncol Rep. 32:2070–2076. 2014.PubMed/NCBI | |
Wang W, Ren F, Wu Q, Jiang D, Li H, Peng Z, Wang J and Shi H: MicroRNA-497 inhibition of ovarian cancer cell migration and invasion through targeting of SMAD specific E3 ubiquitin protein ligase 1. Biochem Biophys Res Commun. 449:432–437. 2014. View Article : Google Scholar : PubMed/NCBI | |
Lee M, Kim EJ and Jeon MJ: MicroRNAs 125a and 125b inhibit ovarian cancer cells through post-transcriptional inactivation of EIF4EBP1. Oncotarget. 7:8726–8742. 2016. | |
Meng X, Joosse SA, Müller V, Trillsch F, Milde-Langosch K, Mahner S, Geffken M, Pantel K and Schwarzenbach H: Diagnostic and prognostic potential of serum miR-7, miR-16, miR-25, miR-93, miR-182, miR-376a and miR-429 in ovarian cancer patients. Br J Cancer. 113:1358–1366. 2015. View Article : Google Scholar : PubMed/NCBI | |
Cao J, Cai J, Huang D, Han Q, Yang Q, Li T, Ding H and Wang Z: miR-335 represents an invasion suppressor gene in ovarian cancer by targeting Bcl-w. Oncol Rep. 30:701–706. 2013.PubMed/NCBI | |
Imam JS, Plyler JR, Bansal H, Prajapati S, Bansal S, Rebeles J, Chen HI, Chang YF, Panneerdoss S, Zoghi B, et al: Genomic loss of tumor suppressor miRNA-204 promotes cancer cell migration and invasion by activating AKT/mTOR/Rac1 signaling and actin reorganization. PloS One. 7:e523972012. View Article : Google Scholar | |
Chung TK, Lau TS, Cheung TH, Yim SF, Lo KW, Siu NS, Chan LK, Yu MY, Kwong J, Doran G, et al: Dysregulation of microRNA-204 mediates migration and invasion of endometrial cancer by regulating FOXC1. Int J Cancer. 130:1036–1045. 2012. View Article : Google Scholar | |
Vimalraj S, Miranda PJ, Ramyakrishna B and Selvamurugan N: Regulation of breast cancer and bone metastasis by microRNAs. Dis Markers. 35:369–387. 2013. View Article : Google Scholar : PubMed/NCBI | |
Tang H, Yao L, Tao X, Yu Y, Chen M, Zhang R and Xu C: miR-9 functions as a tumor suppressor in ovarian serous carcinoma by targeting TLN1. Int J Mol Med. 32:381–388. 2013.PubMed/NCBI | |
Ohyagi-Hara C, Sawada K, Kamiura S, Tomita Y, Isobe A, Hashimoto K, Kinose Y, Mabuchi S, Hisamatsu T, Takahashi T, et al: miR-92a inhibits peritoneal dissemination of ovarian cancer cells by inhibiting integrin α5 expression. Am J Pathol. 182:1876–1889. 2013. View Article : Google Scholar : PubMed/NCBI | |
Doberstein K, Bretz NP, Schirmer U, Fiegl H, Blaheta R, Breunig C, Müller-Holzner E, Reimer D, Zeimet AG and Altevogt P: miR-21-3p is a positive regulator of L1CAM in several human carcinomas. Cancer Lett. 354:455–466. 2014. View Article : Google Scholar : PubMed/NCBI | |
Chen S, Chen X, Xiu YL, Sun KX and Zhao Y: MicroRNA-490-3P targets CDK1 and inhibits ovarian epithelial carcinoma tumorigenesis and progression. Cancer Lett. 362:122–130. 2015. View Article : Google Scholar : PubMed/NCBI | |
Chen X, Chen S, Xiu Y-L, Sun K-X, Zong Z-H and Zhao Y: RhoC is a major target of microRNA-93-5P in epithelial ovarian carcinoma tumorigenesis and progression. Mol Cancer. 14:312015. View Article : Google Scholar : PubMed/NCBI | |
Liu T, Qin W, Hou L and Huang Y: MicroRNA-17 promotes normal ovarian cancer cells to cancer stem cells development via suppression of the LKB1-p53-p21/WAF1 pathway. Tumour Biol. 36:1881–1893. 2015. View Article : Google Scholar | |
Corney DC, Hwang CI, Matoso A, Vogt M, Flesken-Nikitin A, Godwin AK, Kamat AA, Sood AK, Ellenson LH, Hermeking H, et al: Frequent downregulation of miR-34 family in human ovarian cancers. Clin Cancer Res. 16:1119–1128. 2010. View Article : Google Scholar : PubMed/NCBI | |
Hwang C-I, Choi J, Zhou Z, Flesken-Nikitin A, Tarakhovsky A and Nikitin AY: MET-dependent cancer invasion may be preprogrammed by early alterations of p53-regulated feedforward loop and triggered by stromal cell-derived HGF. Cell Cycle. 10:3834–3840. 2011. View Article : Google Scholar : PubMed/NCBI | |
Hwang C-I, Matoso A, Corney DC, Flesken-Nikitin A, Körner S, Wang W, Boccaccio C, Thorgeirsson SS, Comoglio PM, Hermeking H, et al: Wild-type p53 controls cell motility and invasion by dual regulation of MET expression. Proc Natl Acad Sci USA. 108:14240–14245. 2011. View Article : Google Scholar : PubMed/NCBI | |
Li R, Shi X, Ling F, Wang C, Liu J, Wang W and Li M: MiR-34a suppresses ovarian cancer proliferation and motility by targeting AXL. Tumour Biol. 36:7277–7283. 2015. View Article : Google Scholar : PubMed/NCBI | |
Wu H, Xiao Z, Wang K, Liu W and Hao Q: MiR-145 is downreg-ulated in human ovarian cancer and modulates cell growth and invasion by targeting p70S6K1 and MUC1. Biochem Biophys Res Commun. 441:693–700. 2013. View Article : Google Scholar : PubMed/NCBI | |
Ahmed AA, Etemadmoghadam D, Temple J, Lynch AG, Riad M, Sharma R, Stewart C, Fereday S, Caldas C, Defazio A, et al: Driver mutations in TP53 are ubiquitous in high grade serous carcinoma of the ovary. J Pathol. 221:49–56. 2010. View Article : Google Scholar : PubMed/NCBI | |
Dong R, Liu X, Zhang Q, Jiang Z, Li Y, Wei Y, Li Y, Yang Q, Liu J, Wei JJ, et al: miR-145 inhibits tumor growth and metastasis by targeting metadherin in high-grade serous ovarian carcinoma. Oncotarget. 5:10816–10829. 2014. View Article : Google Scholar : PubMed/NCBI | |
Chen X, Dong C, Law PT, Chan MT, Su Z, Wang S, Wu WK and Xu H: MicroRNA-145 targets TRIM2 and exerts tumor-suppressing functions in epithelial ovarian cancer. Gynecol Oncol. 139:513–519. 2015. View Article : Google Scholar : PubMed/NCBI | |
Kim TH, Song JY, Park H, Jeong JY, Kwon AY, Heo JH, Kang H, Kim G and An HJ: miR-145, targeting high-mobility group A2, is a powerful predictor of patient outcome in ovarian carcinoma. Cancer Lett. 356B:937–945. 2015. View Article : Google Scholar | |
Yan L, Zhou J, Gao Y, Ghazal S, Lu L, Bellone S, Yang Y, Liu N, Zhao X, Santin AD, et al: Regulation of tumor cell migration and invasion by the H19/let-7 axis is antagonized by metformin-induced DNA methylation. Oncogene. 34:3076–3084. 2015. View Article : Google Scholar | |
Gao Y, Meng H, Liu S, Hu J, Zhang Y, Jiao T, Liu Y, Ou J, Wang D, Yao L, et al: LncRNA-HOST2 regulates cell biological behaviors in epithelial ovarian cancer through a mechanism involving microRNA let-7b. Hum Mol Genet. 24:841–852. 2015. View Article : Google Scholar | |
Guo Y, Tian P, Yang C, Liang Z, Li M, Sims M, Lu L, Zhang Z, Li H, Pfeffer LM, et al: Silencing the double-stranded RNA binding protein DGCR8 inhibits ovarian cancer cell proliferation, migration, and invasion. Pharm Res. 32:769–778. 2015. View Article : Google Scholar : PubMed/NCBI | |
Rupaimoole R, Ivan C, Yang D, Gharpure KM, Wu SY, Pecot CV, Previs RA, Nagaraja AS, Armaiz-Pena GN, McGuire M, et al: Hypoxia-upregulated microRNA-630 targets Dicer, leading to increased tumor progression. Oncogene. 35:4312–4320. 2016. View Article : Google Scholar : PubMed/NCBI | |
Tang R, Cui ZM and Lou YH: MicroRNA-16 regulates the proliferation, invasion and apoptosis of ovarian epithelial carcinoma cells in vitro. Zhonghua Fu Chan Ke Za Zhi. 47:846–850. 2012.In Chinese. | |
Wei LQ, Liang HT, Qin DC, Jin HF, Zhao Y and She MC: MiR-212 exerts suppressive effect on SKOV3 ovarian cancer cells through targeting HBEGF. Tumour Biol. 35:12427–12434. 2014. View Article : Google Scholar : PubMed/NCBI | |
Li J, Li D and Zhang W: Tumor suppressor role of miR-217 in human epithelial ovarian cancer by targeting IGF1R. Oncol Rep. 35:1671–1679. 2016. | |
Li J, Li L, Li Z, Gong G, Chen P, Liu H, Wang J, Liu Y and Wu X: The role of miR-205 in the VEGF-mediated promotion of human ovarian cancer cell invasion. Gynecol Oncol. 137:125–133. 2015. View Article : Google Scholar : PubMed/NCBI | |
Zhou J, Liu H, Chen Y, Wen J, Li L and Wu X: Expression and significance of VEGF, miR-205 and target protein Ezrin and Lamin A/C in ovarian cancer. Zhong Nan Da Xue Xue Bao Yi Xue Ban. 39:142–150. 2014.0 (In Chinese). PubMed/NCBI | |
Fu X, Cui Y, Yang S, Xu Y and Zhang Z: MicroRNA-613 inhibited ovarian cancer cell proliferation and invasion by regulating KRAS. Tumour Biol. 37:6477–6483. 2016. View Article : Google Scholar | |
Zhang L, Li Z, Gai F and Wang Y: MicroRNA-137 suppresses tumor growth in epithelial ovarian cancer in vitro and in vivo. Mol Med Rep. 12:3107–3114. 2015.PubMed/NCBI | |
Shi C and Zhang Z: miR-761 inhibits tumor progression by targeting MSI1 in ovarian carcinoma. Tumour Biol. 37:5437–5443. 2016. View Article : Google Scholar | |
Yao L, Wang L, Li F, Gao X, Wei X and Liu Z: MiR181c inhibits ovarian cancer metastasis and progression by targeting PRKCD expression. Int J Clin Exp Med. 8:15198–15205. 2015.PubMed/NCBI | |
Feng S, Pan W, Jin Y and Zheng J: MiR-25 promotes ovarian cancer proliferation and motility by targeting LATS2. Tumour Biol. 35:12339–12344. 2014. View Article : Google Scholar : PubMed/NCBI | |
Xia Y and Gao Y: MicroRNA-181b promotes ovarian cancer cell growth and invasion by targeting LATS2. Biochem Biophys Res Commun. 447:446–451. 2014. View Article : Google Scholar : PubMed/NCBI | |
Lou Y, Yang X, Wang F, Cui Z and Huang Y: MicroRNA-21 promotes the cell proliferation, invasion and migration abilities in ovarian epithelial carcinomas through inhibiting the expression of PTEN protein. Int J Mol Med. 26:819–827. 2010. View Article : Google Scholar : PubMed/NCBI | |
Lou Y, Cui Z, Wang F, Yang X and Qian J: miR-21 down-regulation promotes apoptosis and inhibits invasion and migration abilities of OVCAR3 cells. Clin Invest Med. 34:E2812011.PubMed/NCBI | |
Wang YQ, Guo RD, Guo RM, Sheng W and Yin LR: MicroRNA-182 promotes cell growth, invasion, and chemoresis-tance by targeting programmed cell death 4 (PDCD4) in human ovarian carcinomas. J Cell Biochem. 114:1464–1473. 2013. View Article : Google Scholar : PubMed/NCBI | |
Xu X, Ayub B, Liu Z, Serna VA, Qiang W, Liu Y, Hernando E, Zabludoff S, Kurita T, Kong B, et al: Anti-miR182 reduces ovarian cancer burden, invasion, and metastasis: An in vivo study in orthotopic xenografts of nude mice. Mol Cancer Ther. 13:1729–1739. 2014. View Article : Google Scholar : PubMed/NCBI | |
Liu Z, Liu J, Segura MF, Shao C, Lee P, Gong Y, Hernando E and Wei JJ: MiR-182 overexpression in tumourigenesis of high-grade serous ovarian carcinoma. J Pathol. 228:204–215. 2012. View Article : Google Scholar : PubMed/NCBI | |
Nakayama I, Shibazaki M, Yashima-Abo A, Miura F, Sugiyama T, Masuda T and Maesawa C: Loss of HOXD10 expression induced by upregulation of miR-10b accelerates the migration and invasion activities of ovarian cancer cells. Int J Oncol. 43:63–71. 2013.PubMed/NCBI | |
Fan X, Liu Y, Jiang J, Ma Z, Wu H, Liu T, Liu M, Li X and Tang H: miR-20a promotes proliferation and invasion by targeting APP in human ovarian cancer cells. Acta Biochim Biophys Sin (Shanghai). 42:318–324. 2010. View Article : Google Scholar | |
Zou D, Wang D, Li R, Tang Y, Yuan L, Long X and Zhou Q: MiR-197 induces Taxol resistance in human ovarian cancer cells by regulating NLK. Tumour Biol. 36:6725–6732. 2015. View Article : Google Scholar : PubMed/NCBI | |
Taylor MA and Schiemann WP: Therapeutic opportunities for targeting microRNAs in cancer. Mol Cell Ther. 2:1–13. 2014. View Article : Google Scholar | |
Krützfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M and Stoffel M: Silencing of microRNAs in vivo with 'antagomirs'. Nature. 438:685–689. 2005. View Article : Google Scholar : PubMed/NCBI | |
Elmén J, Lindow M, Silahtaroglu A, Bak M, Christensen M, Lind-Thomsen A, Hedtjärn M, Hansen JB, Hansen HF, Straarup EM, et al: Antagonism of microRNA-122 in mice by systemically administered LNA-antimiR leads to up-regulation of a large set of predicted target mRNAs in the liver. Nucleic Acids Res. 36:1153–1162. 2008. View Article : Google Scholar : | |
Hutvágner G and Zamore PD: A microRNA in a multiple-turnover RNAi enzyme complex. Science. 297:2056–2060. 2002. View Article : Google Scholar : PubMed/NCBI | |
Kota J, Chivukula RR, O'Donnell KA, Wentzel EA, Montgomery CL, Hwang HW, Chang TC, Vivekanandan P, Torbenson M, Clark KR, et al: Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell. 137:1005–1017. 2009. View Article : Google Scholar : PubMed/NCBI | |
Garzon R, Marcucci G and Croce CM: Targeting microRNAs in cancer: Rationale, strategies and challenges. Nat Rev Drug Discov. 9:775–789. 2010. View Article : Google Scholar : PubMed/NCBI | |
Lu Y, Xiao J, Lin H, Bai Y, Luo X, Wang Z and Yang B: A single anti-microRNA antisense oligodeoxyribonucleotide (AMO) targeting multiple microRNAs offers an improved approach for microRNA interference. Nucleic Acids Res. 37:e242009. View Article : Google Scholar : PubMed/NCBI | |
Dai F, Zhang Y, Zhu X, Shan N and Chen Y: Anticancer role of MUC1 aptamer-miR-29b chimera in epithelial ovarian carcinoma cells through regulation of PTEN methylation. Target Oncol. 7:217–225. 2012. View Article : Google Scholar : PubMed/NCBI | |
Cittelly DM, Dimitrova I, Howe EN, Cochrane DR, Jean A, Spoelstra NS, Post MD, Lu X, Broaddus RR, Spillman MA, et al: Restoration of miR-200c to ovarian cancer reduces tumor burden and increases sensitivity to paclitaxel. Mol Cancer Ther. 11:2556–2565. 2012. View Article : Google Scholar : PubMed/NCBI | |
Gambari R, Brognara E, Spandidos DA and Fabbri E: Targeting oncomiRNAs and mimicking tumor suppressor miRNAs: New trends in the development of miRNA therapeutic strategies in oncology (Review). Int J Oncol. 49:5–32. 2016.PubMed/NCBI |