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Review

Circular RNAs: A Promising Biomarker for Endometrial Cancer

, &
Pages 1651-1665 | Published online: 17 Feb 2021

References

  • Amant F, Moerman P, Neven P, et al. Endometrial cancer. Lancet. 2005;366(9484):491–505. doi:10.1016/s0140-6736(05)67063-816084259
  • Jemal A, Murray T, Ward E, et al. Cancer statistics, 2005. CA Cancer J Clin. 2005;55:10–30. doi:10.3322/canjclin.55.1.1015661684
  • Braun MM, Overbeek-Wager EA, Grumbo RJ. Diagnosis and Management of Endometrial Cancer. Am Fam Physician. 2016;93:468–474.26977831
  • Bokhman JV. Two pathogenetic types of endometrial carcinoma. Gynecol Oncol. 1983;15:10–17. doi:10.1016/0090-8258(83)90111-76822361
  • Tornesello ML, Faraonio R, Buonaguro L, et al. The Role of microRNAs, Long Non-coding RNAs, and Circular RNAs in Cervical Cancer. Front Oncol. 2020;10:150. doi:10.3389/fonc.2020.0015032154165
  • Huang J, Zhou Q, Li Y. Circular RNAs in gynecological disease: promising biomarkers and diagnostic targets. Biosci Rep. 2019;39. doi:10.1042/bsr20181641
  • Yang X, Mei J, Wang H, et al. The emerging roles of circular RNAs in ovarian cancer. Cancer Cell Int. 2020;20:265. doi:10.1186/s12935-020-01367-932587475
  • Dong P, Xu D, Xiong Y, et al. The Expression, Functions and Mechanisms of Circular RNAs in Gynecological Cancers. Cancers. 2020;12. doi:10.3390/cancers12061472
  • Liu KS, Pan F, Mao XD, Liu C, Chen YJ. Biological functions of circular RNAs and their roles in occurrence of reproduction and gynecological diseases. Am J Transl Res. 2019;11:1–15.30787966
  • Chen BJ, Byrne FL, Takenaka K, et al. Analysis of the circular RNA transcriptome in endometrial cancer. Oncotarget. 2018;9(5):5786–5796. doi:10.18632/oncotarget.2353429464034
  • Ye F, Tang QL, Ma F, et al. Analysis of the circular RNA transcriptome in the grade 3 endometrial cancer. Cancer Manag Res. 2019;11:6215–6227. doi:10.2147/cmar.S19734331308756
  • Jeck WR, Sharpless NE. Detecting and characterizing circular RNAs. Nat Biotechnol. 2014;32:453–461. doi:10.1038/nbt.289024811520
  • Ashwal-Fluss R, et al. circRNA Biogenesis Competes with Pre-mRNA Splicing. Mol Cell. 2014;56:55–66. doi:10.1016/j.molcel.2014.08.01925242144
  • Vo JN, et al. The Landscape of Circular RNA in Cancer. Cell. 2019;176:869–881.e813. doi:10.1016/j.cell.2018.12.02130735636
  • Zhao ZJ, Shen J. Circular RNA participates in the carcinogenesis and the malignant behavior of cancer. RNA Biol. 2017;14:514–521. doi:10.1080/15476286.2015.112216226649774
  • Tran AM, et al. A New World of Biomarkers and Therapeutics for Female Reproductive System and Breast Cancers: circular RNAs. Front Cell Dev Biol. 2020;8:50. doi:10.3389/fcell.2020.0005032211400
  • Vicens Q, Westhof E. Biogenesis of Circular RNAs. Cell. 2014;159:13–14. doi:10.1016/j.cell.2014.09.00525259915
  • Starke S, et al. Exon Circularization Requires Canonical Splice Signals. Cell Rep. 2015;10:103–111. doi:10.1016/j.celrep.2014.12.00225543144
  • Wang Y, Wang Z. Efficient backsplicing produces translatable circular mRNAs. Rna. 2015;21:172–179. doi:10.1261/rna.048272.11425449546
  • Zhang XO, et al. Diverse alternative back-splicing and alternative splicing landscape of circular RNAs. Genome Res. 2016;26:1277–1287. doi:10.1101/gr.202895.11527365365
  • Chen -L-L. The expanding regulatory mechanisms and cellular functions of circular RNAs. Nat Rev Mol Cell Biol. 2020;21:475–490. doi:10.1038/s41580-020-0243-y32366901
  • Rong D, et al. An emerging function of circRNA-miRNAs-mRNA axis in human diseases. Oncotarget. 2017;8:73271–73281. doi:10.18632/oncotarget.1915429069868
  • Wilusz JE. A 360° view of circular RNAs: from biogenesis to functions. Wiley Interdiscip Rev RNA. 2018;9:e1478. doi:10.1002/wrna.147829655315
  • Danan M, Schwartz S, Edelheit S, Sorek R. Transcriptome-wide discovery of circular RNAs in Archaea. Nucleic Acids Res. 2012;40:3131–3142. doi:10.1093/nar/gkr100922140119
  • Noto JJ, Schmidt CA, Matera AG. Engineering and expressing circular RNAs via tRNA splicing. RNA Biol. 2017;14:978–984. doi:10.1080/15476286.2017.131791128402213
  • Lasda E, Parker R. Circular RNAs: diversity of form and function. Rna. 2014;20:1829–1842. doi:10.1261/rna.047126.11425404635
  • Zhang Y, et al. Circular intronic long noncoding RNAs. Mol Cell. 2013;51:792–806. doi:10.1016/j.molcel.2013.08.01724035497
  • Jeck WR, et al. Circular RNAs are abundant, conserved, and associated with ALU repeats. Rna. 2013;19:141–157. doi:10.1261/rna.035667.11223249747
  • Czubak K, Sedehizadeh S, Kozlowski P, Wojciechowska M. An Overview of Circular RNAs and Their Implications in Myotonic Dystrophy. Int J Mol Sci. 2019;20. doi:10.3390/ijms20184385
  • Chen I, Chen CY, Chuang TJ. Biogenesis, identification, and function of exonic circular RNAs. Wiley Interdiscip Rev RNA. 2015;6:563–579. doi:10.1002/wrna.129426230526
  • Kristensen LS, et al. The biogenesis, biology and characterization of circular RNAs. Nat Rev Genet. 2019;20:675–691. doi:10.1038/s41576-019-0158-731395983
  • Ivanov A, et al. Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals. Cell Rep. 2015;10:170–177. doi:10.1016/j.celrep.2014.12.01925558066
  • Du WW, et al. Identifying and Characterizing circRNA-Protein Interaction. Theranostics. 2017;7:4183–4191. doi:10.7150/thno.2129929158818
  • Chen LL, Yang L. Regulation of circRNA biogenesis. RNA Biol. 2015;12:381–388. doi:10.1080/15476286.2015.102027125746834
  • Taylor K, et al. MBNL splicing activity depends on RNA binding site structural context. Nucleic Acids Res. 2018;46:9119–9133. doi:10.1093/nar/gky56529955876
  • Athanasiadis A, Rich A, Maas S. Widespread A-to-I RNA editing of Alu-containing mRNAs in the human transcriptome. PLoS Biol. 2004;2:e391. doi:10.1371/journal.pbio.002039115534692
  • Kim DD, et al. Widespread RNA editing of embedded alu elements in the human transcriptome. Genome Res. 2004;14:1719–1725. doi:10.1101/gr.285550415342557
  • Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. Identification of novel genes coding for small expressed RNAs. Science. 2001;294:853–858. doi:10.1126/science.106492111679670
  • Poliseno L, et al. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature. 2010;465:1033–1038. doi:10.1038/nature0914420577206
  • Hansen TB, et al. Natural RNA circles function as efficient microRNA sponges. Nature. 2013;495:384–388. doi:10.1038/nature1199323446346
  • Cesana M, et al. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell. 2011;147:358–369. doi:10.1016/j.cell.2011.09.02822000014
  • Salzman J, Gawad C, Wang PL, Lacayo N, Brown PO. Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS One. 2012;7:e30733. doi:10.1371/journal.pone.003073322319583
  • Hansen TB, et al. miRNA-dependent gene silencing involving Ago2-mediated cleavage of a circular antisense RNA. EMBO J. 2011;30:4414–4422. doi:10.1038/emboj.2011.35921964070
  • Capel B, et al. Circular transcripts of the testis-determining gene Sry in adult mouse testis. Cell. 1993;73:1019–1030. doi:10.1016/0092-8674(93)90279-y7684656
  • Kefas B, et al. microRNA-7 inhibits the epidermal growth factor receptor and the Akt pathway and is down-regulated in glioblastoma. Cancer Res. 2008;68:3566–3572. doi:10.1158/0008-5472.Can-07-663918483236
  • Reddy SD, Ohshiro K, Rayala SK, Kumar R. MicroRNA-7, a homeobox D10 target, inhibits p21-activated kinase 1 and regulates its functions. Cancer Res. 2008;68:8195–8200. doi:10.1158/0008-5472.Can-08-210318922890
  • Bolisetty MT, Graveley BR. Circuitous route to transcription regulation. Mol Cell. 2013;51:705–706. doi:10.1016/j.molcel.2013.09.01224074951
  • Li Z, et al. Exon-intron circular RNAs regulate transcription in the nucleus. Nat Struct Mol Biol. 2015;22:256–264. doi:10.1038/nsmb.295925664725
  • Memczak S, et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature. 2013;495:333–338. doi:10.1038/nature1192823446348
  • Du WW, et al. Foxo3 circular RNA promotes cardiac senescence by modulating multiple factors associated with stress and senescence responses. Eur Heart J. 2017;38:1402–1412. doi:10.1093/eurheartj/ehw00126873092
  • Du WW, et al. Foxo3 circular RNA retards cell cycle progression via forming ternary complexes with p21 and CDK2. Nucleic Acids Res. 2016;44:2846–2858. doi:10.1093/nar/gkw02726861625
  • Chen CY, Sarnow P. Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs. Science. 1995;268:415–417. doi:10.1126/science.75363447536344
  • Pamudurti NR, et al. Translation of CircRNAs. Mol Cell. 2017;66:9–21. doi:10.1016/j.molcel.2017.02.02128344080
  • Legnini I, et al. Circ-ZNF609 Is a Circular RNA that Can Be Translated and Functions in Myogenesis. Mol Cell. 2017;66:22–37.e29. doi:10.1016/j.molcel.2017.02.01728344082
  • Granados-Riveron JT, Aquino-Jarquin G. The complexity of the translation ability of circRNAs. Biochim Biophys Acta. 2016;1859:1245–1251. doi:10.1016/j.bbagrm.2016.07.00927449861
  • AbouHaidar MG, Venkataraman S, Golshani A, Liu B, Ahmad T. Novel coding, translation, and gene expression of a replicating covalently closed circular RNA of 220 nt. Proc Natl Acad Sci U S A. 2014;111:14542–14547. doi:10.1073/pnas.140281411125253891
  • Flores R, et al. Rolling-circle replication of viroids, viroid-like satellite RNAs and hepatitis delta virus: variations on a theme. RNA Biol. 2011;8:200–206. doi:10.4161/rna.8.2.1423821358283
  • Kos A, Dijkema R, Arnberg AC, van der Meide PH, Schellekens H. The hepatitis delta (delta) virus possesses a circular RNA. Nature. 1986;323:558–560. doi:10.1038/323558a02429192
  • Zhang M, et al. A peptide encoded by circular form of LINC-PINT suppresses oncogenic transcriptional elongation in glioblastoma. Nat Commun. 2018;9:4475. doi:10.1038/s41467-018-06862-230367041
  • Ye F, et al. circFBXW7 Inhibits Malignant Progression by Sponging miR-197-3p and Encoding a 185-aa Protein in Triple-Negative Breast Cancer. Mol Ther Nucleic Acids. 2019;18:88–98. doi:10.1016/j.omtn.2019.07.02331536884
  • Suzuki H, Tsukahara T. A view of pre-mRNA splicing from RNase R resistant RNAs. Int J Mol Sci. 2014;15:9331–9342. doi:10.3390/ijms1506933124865493
  • Huang C, Shan G. What happens at or after transcription: insights into circRNA biogenesis and function. Transcription. 2015;6:61–64. doi:10.1080/21541264.2015.107130126177684
  • Lei K, et al. The mechanism and function of circular RNAs in human diseases. Exp Cell Res. 2018;368:147–158. doi:10.1016/j.yexcr.2018.05.00229730164
  • Huang A, Zheng H, Wu Z, Chen M, Huang Y. Circular RNA-protein interactions: functions, mechanisms, and identification. Theranostics. 2020;10:3503–3517. doi:10.7150/thno.4217432206104
  • Patop IL, Wüst S, Kadener S. Past, present, and future of circRNAs. EMBO J. 2019;38:e100836. doi:10.15252/embj.201810083631343080
  • Salzman J, Chen RE, Olsen MN, Wang PL, Brown PO. Cell-type specific features of circular RNA expression. PLoS Genet. 2013;9:e1003777. doi:10.1371/journal.pgen.100377724039610
  • Maass PG, et al. A map of human circular RNAs in clinically relevant tissues. J Mol Med (Berl). 2017;95:1179–1189. doi:10.1007/s00109-017-1582-928842720
  • Perriman R, Ares M. Circular mRNA can direct translation of extremely long repeating-sequence proteins in vivo. Rna. 1998;4:1047–1054. doi:10.1017/s135583829898061x9740124
  • Haddad G, Lorenzen JM. Biogenesis and Function of Circular RNAs in Health and in Disease. Front Pharmacol. 2019;10:428. doi:10.3389/fphar.2019.0042831080413
  • Huang C, Liang D, Tatomer DC, Wilusz JE. A length-dependent evolutionarily conserved pathway controls nuclear export of circular RNAs. Genes Dev. 2018;32:639–644. doi:10.1101/gad.314856.11829773557
  • Cai H, et al. Circular RNA hsa_circ_0000263 participates in cervical cancer development by regulating target gene of miR-150-5p. J Cell Physiol. 2019;234:11391–11400. doi:10.1002/jcp.2779630569515
  • Gao YL, et al. Circular RNA expression profiles reveal that hsa_circ_0018289 is up-regulated in cervical cancer and promotes the tumorigenesis. Oncotarget. 2017;8:86625–86633. doi:10.18632/oncotarget.2125729156822
  • Ma HB, Yao YN, Yu JJ, Chen XX, Li HF. Extensive profiling of circular RNAs and the potential regulatory role of circRNA-000284 in cell proliferation and invasion of cervical cancer via sponging miR-506. Am J Transl Res. 2018;10:592–604.29511454
  • Tian JDC, Liang L. Involvement of circular RNA SMARCA5/microRNA-620 axis in the regulation of cervical cancer cell proliferation, invasion and migration. Eur Rev Med Pharmacol Sci. 2018;22:8589–8598. doi:10.26355/eurrev_201812_1662230575898
  • Zhang J, Zhao X, Zhang J, Zheng X, Circular LF. RNA hsa_circ_0023404 exerts an oncogenic role in cervical cancer through regulating miR-136/TFCP2/YAP pathway. Biochem Biophys Res Commun. 2018;501:428–433. doi:10.1016/j.bbrc.2018.05.00629738762
  • Chaichian S, Shafabakhsh R, Mirhashemi SM, Moazzami B, Asemi Z. Circular RNAs: a novel biomarker for cervical cancer. J Cell Physiol. 2020;235:718–724. doi:10.1002/jcp.2900931240697
  • Liu N, Zhang J, Zhang LY, Wang L. CircHIPK3 is upregulated and predicts a poor prognosis in epithelial ovarian cancer. Eur Rev Med Pharmacol Sci. 2018;22:3713–3718. doi:10.26355/eurrev_201806_1525029949144
  • Hill HA, et al. Racial differences in endometrial cancer survival: the black/white cancer survival study. Obstet Gynecol. 1996;88:919–926. doi:10.1016/s0029-7844(96)00341-98942828
  • Madison T, Schottenfeld D, James SA, Schwartz AG, Gruber SB. Endometrial cancer: socioeconomic status and racial/ethnic differences in stage at diagnosis, treatment, and survival. Am J Public Health. 2004;94:2104–2111. doi:10.2105/ajph.94.12.210415569961
  • Torre LA, et al. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65:87–108. doi:10.3322/caac.2126225651787
  • Morice P, Leary A, Creutzberg C, Abu-Rustum N, Darai E. Endometrial cancer. Lancet. 2016;387:1094–1108. doi:10.1016/s0140-6736(15)00130-026354523
  • Zaino RJ, Kurman RJ, Diana KL, Morrow CP. The utility of the revised International Federation of Gynecology and Obstetrics histologic grading of endometrial adenocarcinoma using a defined nuclear grading system. A Gynecologic Oncology Group study. Cancer. 2015;75:81–86.
  • Luoto R, Raitanen J, Pukkala E, Anttila A. Effect of hysterectomy on incidence trends of endometrial and cervical cancer in Finland 1953-2010. Br J Cancer. 2004;90:1756–1759. doi:10.1038/sj.bjc.660176315208619
  • Schouten LJ, Goldbohm RA, van den Brandt PA. Anthropometry, physical activity, and endometrial cancer risk: results from the Netherlands Cohort Study. J Natl Cancer Inst. 2004;96:1635–1638. doi:10.1093/jnci/djh29115523093
  • Dou Y, et al. Proteogenomic Characterization of Endometrial Carcinoma. Cell. 2020;180:729–748.e726. doi:10.1016/j.cell.2020.01.02632059776
  • Vausort M, et al. Myocardial Infarction-Associated Circular RNA Predicting Left Ventricular Dysfunction. J Am Coll Cardiol. 2016;68:1247–1248. doi:10.1016/j.jacc.2016.06.04027609688
  • Salgado-Somoza A, Zhang L, Vausort M, Devaux Y. The circular RNA MICRA for risk stratification after myocardial infarction. Int J Cardiol Heart Vasc. 2017;17:33–36. doi:10.1016/j.ijcha.2017.11.00129159270
  • Chen B, et al. circEPSTI1 as a Prognostic Marker and Mediator of Triple-Negative Breast Cancer Progression. Theranostics. 2018;8:4003–4015. doi:10.7150/thno.2410630083277
  • Chen X, et al. Circular RNA circHIPK3 modulates autophagy via MIR124-3p-STAT3-PRKAA/AMPKα signaling in STK11 mutant lung cancer. Autophagy. 2020;16:659–671. doi:10.1080/15548627.2019.163494531232177
  • Liu CX, et al. Structure and Degradation of Circular RNAs Regulate PKR Activation in Innate Immunity. Cell. 2019;177:865–880.e821. doi:10.1016/j.cell.2019.03.04631031002
  • Carrara M, Fuschi P, Ivan C, Martelli F. Circular RNAs: methodological challenges and perspectives in cardiovascular diseases. J Cell Mol Med. 2018;22:5176–5187. doi:10.1111/jcmm.1378930277664
  • Chen S, et al. Widespread and Functional RNA Circularization in Localized Prostate Cancer. Cell. 2019;176:831–843.e822. doi:10.1016/j.cell.2019.01.02530735634
  • Dragomir M, Calin GA. Circular RNAs in Cancer - Lessons Learned From microRNAs. Front Oncol. 2018;8:179. doi:10.3389/fonc.2018.0017929911069
  • Kristensen LS, Hansen TB, Venø MT, Kjems J. Circular RNAs in cancer: opportunities and challenges in the field. Oncogene. 2018;37:555–565. doi:10.1038/onc.2017.36128991235
  • Yang Y, et al. Novel Role of FBXW7 Circular RNA in Repressing Glioma Tumorigenesis. J Natl Cancer Inst. 2018;110:304–315. doi:10.1093/jnci/djx166
  • Zhang XL, Xu LL, Wang F. Hsa_circ_0020397 regulates colorectal cancer cell viability, apoptosis and invasion by promoting the expression of the miR-138 targets TERT and PD-L1. Cell Biol Int. 2017;41:1056–1064. doi:10.1002/cbin.1082628707774
  • Zheng Q, et al. Circular RNA profiling reveals an abundant circHIPK3 that regulates cell growth by sponging multiple miRNAs. Nat Commun. 2016;7:11215. doi:10.1038/ncomms1121527050392
  • Bachmayr-Heyda A, et al. Correlation of circular RNA abundance with proliferation–exemplified with colorectal and ovarian cancer, idiopathic lung fibrosis, and normal human tissues. Sci Rep. 2015;5:8057. doi:10.1038/srep0805725624062
  • Li Y, et al. Circular RNA is enriched and stable in exosomes: a promising biomarker for cancer diagnosis. Cell Res. 2015;25:981–984. doi:10.1038/cr.2015.8226138677
  • Memczak S, Papavasileiou P, Peters O, Rajewsky N. Identification and Characterization of Circular RNAs As a New Class of Putative Biomarkers in Human Blood. PLoS One. 2015;10:e0141214. doi:10.1371/journal.pone.014121426485708
  • Suzuki H, Aoki Y, Kameyama T, et al. Endogenous Multiple Exon Skipping and Back-Splicing at the DMD Mutation Hotspot. Int J Mol Sci. 2016;17(10):1722. doi:10.3390/ijms17101722
  • Goeppert B, Roessler S, Becker N, et al. DMBT1 expression in biliary carcinogenesis with correlation of clinicopathological data. Histopathology. 2017;70(7):1064–1071. doi:10.1111/his.1317528130841
  • Chang YS, Huang HD, Yeh KT, Chang JG. Identification of novel mutations in endometrial cancer patients by whole-exome sequencing. Int J Oncol. 2017;50:1778–1784. doi:10.3892/ijo.2017.391928339086
  • Kodama J, Kusumoto T. Loss of basement membrane heparan sulfate expression is associated with tumor progression in endometrial cancer.. Eur J Gynaecol Oncol. 2005;26(4):403–406.16122188
  • Bernassola F, Karin M, Ciechanover A, Melino G. The HECT family of E3 ubiquitin ligases: multiple players in cancer development. Cancer Cell. 2008;14(1):10–21. doi:10.1016/j.ccr.2008.06.00118598940
  • Huang G, Zhu H, Shi Y, et al. cir-ITCH plays an inhibitory role in colorectal cancer by regulating the Wnt/β-catenin pathway. PLoS One. 2015;10(6):e0131225. doi:10.1371/journal.pone.013122526110611
  • Yang C, Yuan W, Yang X, et al. Circular RNA circ-ITCH inhibits bladder cancer progression by sponging miR-17/miR-224 and regulating p21, PTEN expression. Mol Cancer. 2018;17(1):19. doi:10.1186/s12943-018-0771-729386015
  • Gu J, Wang D, Zhang J, et al. GFRα2 prompts cell growth and chemoresistance through down-regulating tumor suppressor gene PTEN via Mir-17-5p in pancreatic cancer. Cancer Lett. 2016;380(2):434–441. doi:10.1016/j.canlet.2016.06.01627400681
  • Ye J, Yao Y, Song Q, et al. Up-regulation of miR-95-3p in hepatocellular carcinoma promotes tumorigenesis by targeting p21 expression. Sci Rep. 2016;6(1):34034. doi:10.1038/srep3403427698442
  • Li F, Zhang L, Li W, et al. Circular RNA ITCH has inhibitory effect on ESCC by suppressing the Wnt/β-catenin pathway. Oncotarget. 2015;6(8):6001–6013. doi:10.18632/oncotarget.346925749389
  • Wan L, Zhang L, Fan K, et al. Circular RNA-ITCH Suppresses Lung Cancer Proliferation via Inhibiting the Wnt/β-Catenin Pathway.. Biomed Res Int. 2016;2016:1579490. doi:10.1155/2016/157949027642589
  • Guo W, Zhang J, Zhang D, et al. Polymorphisms and expression pattern of circular RNA circ-ITCH contributes to the carcinogenesis of hepatocellular carcinoma. Oncotarget. 2017;8(29):48169–48177. doi:10.18632/oncotarget.1832728636993
  • Tang K, Wang C, Chen Z, Xu H, Ye Z. Clinicopathologic and prognostic significance of p21 (Cip1/Waf1) expression in bladder cancer.. Int J Clin Exp Pathol. 2005;26(5):4999–5007.
  • Cazier JB, Rao SR, McLean CM, et al. Whole-genome sequencing of bladder cancers reveals somatic CDKN1A mutations and clinicopathological associations with mutation burden. Nat Commun. 2014;5(1):3756. doi:10.1038/ncomms475624777035
  • Anderson DM, Anderson K, Chang C-L, et al. A micropeptide encoded by a putative long noncoding RNA regulates muscle performance. Cell. 2015;160(4):595–606. doi:10.1016/j.cell.2015.01.00925640239
  • Xie H, Ren X, Xin S, et al. Emerging roles of circRNA_001569 targeting miR-145 in the proliferation and invasion of colorectal cancer. Oncotarget. 2016;7(18):26680–26691. doi:10.18632/oncotarget.858927058418
  • Yang W, Du WW, Li X, Yee AJ, Yang BB. Foxo3 activity promoted by non-coding effects of circular RNA and Foxo3 pseudogene in the inhibition of tumor growth and angiogenesis. Oncogene. 2016;35(30):3919–3931. doi:10.1038/onc.2015.46026657152
  • Zhong Z, Lv M, Chen J. Screening differential circular RNA expression profiles reveals the regulatory role of circTCF25-miR-103a-3p/miR-107-CDK6 pathway in bladder carcinoma. Sci Rep. 2016;6:30919. doi:10.1038/srep3091927484176
  • Schnall-Levin M, et al. Unusually effective microRNA targeting within repeat-rich coding regions of mammalian mRNAs. Genome Res. 2011;21:1395–1403. doi:10.1101/gr.121210.11121685129
  • Guo JU, Agarwal V, Guo H, Bartel DP. Expanded identification and characterization of mammalian circular RNAs. Genome Biol. 2014;15:409. doi:10.1186/s13059-014-0409-z25070500
  • Zhang H, et al. Genome-wide functional screening of miR-23b as a pleiotropic modulator suppressing cancer metastasis. Nat Commun. 2011;2:554. doi:10.1038/ncomms155522109528
  • Greenbaum LE. Cell cycle regulation and hepatocarcinogenesis. Cancer Biol Ther. 2004;3:1200–1207. doi:10.4161/cbt.3.12.139215662121
  • Wang G, et al. Centrosomal Protein of 55 Regulates Glucose Metabolism, Proliferation and Apoptosis of Glioma Cells via the Akt/mTOR Signaling Pathway. J Cancer. 2016;7:1431–1440. doi:10.7150/jca.1549727471559
  • Liu X, et al. Circ-8073 regulates CEP55 by sponging miR-449a to promote caprine endometrial epithelial cells proliferation via the PI3K/AKT/mTOR pathway. Biochim Biophys Acta Mol Cell Res. 2018;1865:1130–1147. doi:10.1016/j.bbamcr.2018.05.01129800603
  • Zong ZH, Liu Y, Chen S, Circ_PUM1 ZY. promotes the development of endometrial cancer by targeting the miR-136/NOTCH3 pathway. J Cell Mol Med. 2020;24:4127–4135. doi:10.1111/jcmm.1506932073729
  • Yan M, et al. miR-136 suppresses tumor invasion and metastasis by targeting RASAL2 in triple-negative breast cancer. Oncol Rep. 2016;36:65–71. doi:10.3892/or.2016.476727108696
  • Ren H, Qi Y, Yin X, Gao J. miR-136 targets MIEN1 and involves the metastasis of colon cancer by suppressing epithelial-to-mesenchymal transition. Onco Targets Ther. 2018;11:67–74. doi:10.2147/ott.S11335929339925
  • Shen S, et al. Upregulation of miR-136 in human non-small cell lung cancer cells promotes Erk1/2 activation by targeting PPP2R2A. Tumour Biol. 2014;35:631–640. doi:10.1007/s13277-013-1087-223959478
  • Radtke F, Raj K. The role of Notch in tumorigenesis: oncogene or tumour suppressor? Nat Rev Cancer. 2003;3:756–767. doi:10.1038/nrc118614570040
  • Devor EJ, et al. Cullin-5, a ubiquitin ligase scaffold protein, is significantly underexpressed in endometrial adenocarcinomas and is a target of miR-182. Oncol Rep. 2016;35:2461–2465. doi:10.3892/or.2016.460526847831
  • Jia Y, Liu M, Wang S. CircRNA hsa_circRNA_0001776 inhibits proliferation and promotes apoptosis in endometrial cancer via downregulating LRIG2 by sponging miR-182. Cancer Cell Int. 2020;20:412. doi:10.1186/s12935-020-01437-y32863771
  • Conn SJ, et al. The RNA binding protein quaking regulates formation of circRNAs. Cell. 2015;160:1125–1134. doi:10.1016/j.cell.2015.02.01425768908
  • Nieto MA, Huang RY, Jackson RA, Thiery JPEMT. (2016). Cell. 2016;166:21–45. doi:10.1016/j.cell.2016.06.02827368099
  • Pillman KA, et al. miR-200/375 control epithelial plasticity-associated alternative splicing by repressing the RNA-binding protein Quaking. EMBO J. 2018;37. doi:10.15252/embj.201899016
  • Krebs AM, et al. The EMT-activator Zeb1 is a key factor for cell plasticity and promotes metastasis in pancreatic cancer. Nat Cell Biol. 2017;19:518–529. doi:10.1038/ncb351328414315
  • Zhang P, Sun Y, Ma L. ZEB1: at the crossroads of epithelial-mesenchymal transition, metastasis and therapy resistance. Cell Cycle. 2015;14:481–487. doi:10.1080/15384101.2015.100604825607528
  • Warzecha CC, Carstens RP. Complex changes in alternative pre-mRNA splicing play a central role in the epithelial-to-mesenchymal transition (EMT). Semin Cancer Biol. 2012;22:417–427. doi:10.1016/j.semcancer.2012.04.00322548723
  • Warzecha CC, Sato TK, Nabet B, Hogenesch JB, Carstens RP. ESRP1 and ESRP2 are epithelial cell-type-specific regulators of FGFR2 splicing. Mol Cell. 2009;33:591–601. doi:10.1016/j.molcel.2009.01.02519285943
  • Mizutani A, Koinuma D, Seimiya H, Miyazono K. The Arkadia-ESRP2 axis suppresses tumor progression: analyses in clear-cell renal cell carcinoma. Oncogene. 2016;35:3514–3523. doi:10.1038/onc.2015.41226522722
  • Ishii H, et al. Epithelial splicing regulatory proteins 1 (ESRP1) and 2 (ESRP2) suppress cancer cell motility via different mechanisms. J Biol Chem. 2014;289:27386–27399. doi:10.1074/jbc.M114.58943225143390
  • Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 2014;15:178–196. doi:10.1038/nrm375824556840
  • Zaravinos A. The Regulatory Role of MicroRNAs in EMT and Cancer. J Oncol. 2015;2015:865816. doi:10.1155/2015/86581625883654
  • Yilmaz M, Christofori G. EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev. 2009;28:15–33. doi:10.1007/s10555-008-9169-019169796
  • Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest. 2009;119:1420–1428. doi:10.1172/jci3910419487818
  • Tanaka Y, et al. Prognostic impact of EMT (epithelial-mesenchymal-transition)-related protein expression in endometrial cancer. Cancer Biol Ther. 2013;14:13–19. doi:10.4161/cbt.2262523114646
  • Zhang B, Pan X, Cobb GP, Anderson T. A. microRNAs as oncogenes and tumor suppressors. Dev Biol. 2007;302:1–12. doi:10.1016/j.ydbio.2006.08.02816989803
  • Adam L, et al. miR-200 expression regulates epithelial-to-mesenchymal transition in bladder cancer cells and reverses resistance to epidermal growth factor receptor therapy. Clin Cancer Res. 2009;15:5060–5072. doi:10.1158/1078-0432.Ccr-08-224519671845
  • Wiklund ED, et al. Coordinated epigenetic repression of the miR-200 family and miR-205 in invasive bladder cancer. Int J Cancer. 2011;128:1327–1334. doi:10.1002/ijc.2546120473948
  • Koutsaki M, Spandidos DA, Zaravinos A. Epithelial-mesenchymal transition-associated miRNAs in ovarian carcinoma, with highlight on the miR-200 family: prognostic value and prospective role in ovarian cancer therapeutics. Cancer Lett. 2014;351:173–181. doi:10.1016/j.canlet.2014.05.02224952258
  • Díaz-López A, Moreno-Bueno G, Cano A. Role of microRNA in epithelial to mesenchymal transition and metastasis and clinical perspectives. Cancer Manag Res. 2014;6:205–216. doi:10.2147/cmar.S3815624812525
  • Shen Y, et al. Bortezomib induces apoptosis of endometrial cancer cells through microRNA-17-5p by targeting p21. Cell Biol Int. 2013;37:1114–1121. doi:10.1002/cbin.1013923716467
  • Li J, Sun H, Liu T, Kong J. MicroRNA-423 promotes proliferation, migration and invasion and induces chemoresistance of endometrial cancer cells. Exp Ther Med. 2018;16:4213–4224. doi:10.3892/etm.2018.671030344696
  • Chou YT, et al. EGFR promotes lung tumorigenesis by activating miR-7 through a Ras/ERK/Myc pathway that targets the Ets2 transcriptional repressor ERF. Cancer Res. 2010;70:8822–8831. doi:10.1158/0008-5472.Can-10-063820978205
  • Gottardo F, et al. Micro-RNA profiling in kidney and bladder cancers. Urol Oncol. 2007;25:387–392. doi:10.1016/j.urolonc.2007.01.01917826655
  • Meng F, Henson R, Lang M, et al. Involvement of human micro-RNA in growth and response to chemotherapy in human cholangiocarcinoma cell lines. Gastroenterology. 2006;130:2113–2129. doi:10.1053/j.gastro.2006.02.05716762633
  • Zhang N, Li X, Wu C, et al. microRNA-7 is a novel inhibitor of YY1 contributing to colorectal tumorigenesis. Oncogene. 2013;32:5078–5088. doi:10.1038/onc.2012.52623208495
  • Gao Y, Zhang C, Liu Y, Wang M. Circular RNA profiling reveals circRNA1656 as a novel biomarker in high grade serous ovarian cancer. Biosci Trends. 2019;13:204–211. doi:10.5582/bst.2019.0102131019161
  • Wang J, Wu A, Yang B, et al. Profiling and bioinformatics analyses reveal differential circular RNA expression in ovarian cancer. Gene. 2020;724:144150. doi:10.1016/j.gene.2019.14415031589961
  • Guan X, Zong ZH, Liu Y, et al. circPUM1 Promotes Tumorigenesis and Progression of Ovarian Cancer by Sponging miR-615-5p and miR-6753-5p. Mol Ther Nucleic Acids. 2019;18:882–892. doi:10.1016/j.omtn.2019.09.03231751911
  • Wang W, Wang J, Zhang X, Liu G. Serum circSETDB1 is a promising biomarker for predicting response to platinum-taxane-combined chemotherapy and relapse in high-grade serous ovarian cancer. Onco Targets Ther. 2019;12:7451–7457. doi:10.2147/ott.S22070031686850
  • Pant S, Hilton H, Burczynski ME. The multifaceted exosome: biogenesis, role in normal and aberrant cellular function, and frontiers for pharmacological and biomarker opportunities. Biochem Pharmacol. 2012;83:1484–1494. doi:10.1016/j.bcp.2011.12.03722230477