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• W3124389218 abstract "Circular RNAs (circRNAs) are covalently closed circular structures that can function in various physiological and pathological processes by acting as microRNA (miRNA) sponges, RNA-binding protein (RBP) sponges, mRNA transcriptional regulators, and protein translational templates. circFoxo3 is one of the most studied circRNAs and is generated from the tumor suppressor gene Foxo3. Increasing studies have demonstrated the multiple functions of circFoxo3 in the pathogenesis of different cancer types. circFoxo3 plays important roles in cancer development mainly by binding to various miRNAs. The diagnostic potential of circFoxo3 has been revealed in several cancers. Some research results have been found to contradict the results of other studies, and this may be due to insufficient sample sizes and inconsistencies in the experimental and nomenclature methods. In this review, we systematically summarize current knowledge about the biogenesis and functions of circRNAs, elucidate the roles of circFoxo3 in different cancers, and explore the clinical applications of circFoxo3. Circular RNAs (circRNAs) are covalently closed circular structures that can function in various physiological and pathological processes by acting as microRNA (miRNA) sponges, RNA-binding protein (RBP) sponges, mRNA transcriptional regulators, and protein translational templates. circFoxo3 is one of the most studied circRNAs and is generated from the tumor suppressor gene Foxo3. Increasing studies have demonstrated the multiple functions of circFoxo3 in the pathogenesis of different cancer types. circFoxo3 plays important roles in cancer development mainly by binding to various miRNAs. The diagnostic potential of circFoxo3 has been revealed in several cancers. Some research results have been found to contradict the results of other studies, and this may be due to insufficient sample sizes and inconsistencies in the experimental and nomenclature methods. In this review, we systematically summarize current knowledge about the biogenesis and functions of circRNAs, elucidate the roles of circFoxo3 in different cancers, and explore the clinical applications of circFoxo3. Noncoding RNAs, such as microRNAs (miRNAs) and long noncoding RNAs (lncRNAs), have been widely studied for their various roles in important disease progression processes and have been shown to be promising diagnostic and prognostic biomarkers for many diseases.1Zhang L. Zhang Y. Zhao Y. Wang Y. Ding H. Xue S. Li P. Circulating miRNAs as biomarkers for early diagnosis of coronary artery disease.Expert Opin. Ther. Pat. 2018; 28: 591-601Crossref PubMed Scopus (11) Google Scholar, 2Zhang Y. Zhang L. Wang Y. Ding H. Xue S. Yu H. Hu L. Qi H. Wang Y. Zhu W. et al.KCNQ1OT1, HIF1A-AS2 and APOA1-AS are promising novel biomarkers for diagnosis of coronary artery disease.Clin. Exp. Pharmacol. Physiol. 2019; 46: 635-642Crossref PubMed Scopus (11) Google Scholar, 3Zhang L. Zhang Y. Xue S. Ding H. Wang Y. Qi H. Wang Y. Zhu W. Li P. Clinical significance of circulating microRNAs as diagnostic biomarkers for coronary artery disease.J. Cell. Mol. Med. 2020; 24: 1146-1150Crossref PubMed Scopus (4) Google Scholar In recent years, circular RNA (circRNA), a special type of noncoding RNA with covalently closed loop structures, has gained much attention for its wide participation in various diseases, including cancer and cardiovascular disease (CVD).4Zhou B. Yu J.W. A novel identified circular RNA, circRNA_010567, promotes myocardial fibrosis via suppressing miR-141 by targeting TGF-β1.Biochem. Biophys. Res. Commun. 2017; 487: 769-775Crossref PubMed Scopus (173) Google Scholar, 5Li M. Ding W. Tariq M.A. Chang W. Zhang X. Xu W. Hou L. Wang Y. 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Complementary sequence-mediated exon circularization.Cell. 2014; 159: 134-147Abstract Full Text Full Text PDF PubMed Scopus (804) Google Scholar Growing mechanistic studies have proven that circRNAs have important biological functions in the physiological and pathological development of many organisms.15Hansen T.B. Kjems J. Damgaard C.K. Circular RNA and miR-7 in cancer.Cancer Res. 2013; 73: 5609-5612Crossref PubMed Scopus (574) Google Scholar,21Geng H.H. Li R. Su Y.M. Xiao J. Pan M. Cai X.X. Ji X.P. The circular RNA Cdr1as promotes myocardial infarction by mediating the regulation of miR-7a on its target genes expression.PLoS ONE. 2016; 11: e0151753Crossref PubMed Scopus (185) Google Scholar, 22Dang R.Y. Liu F.L. Li Y. Circular RNA hsa_circ_0010729 regulates vascular endothelial cell proliferation and apoptosis by targeting the miR-186/HIF-1α axis.Biochem. Biophys. Res. Commun. 2017; 490: 104-110Crossref PubMed Scopus (77) Google Scholar, 23Innes H. Barclay S.T. Hayes P.C. Fraser A. Dillon J.F. Stanley A. Bathgate A. McDonald S.A. Goldberg D. Valerio H. et al.The risk of hepatocellular carcinoma in cirrhotic patients with hepatitis C and sustained viral response: role of the treatment regimen.J. Hepatol. 2018; 68: 646-654Abstract Full Text Full Text PDF PubMed Scopus (37) Google Scholar, 24Zhang S. Liao K. Miao Z. Wang Q. Miao Y. Guo Z. Qiu Y. Chen B. Ren L. Wei Z. et al.circFOXO3 promotes glioblastoma progression by acting as a competing endogenous RNA for NFAT5.Neuro-oncol. 2019; 21: 1284-1296Crossref PubMed Scopus (12) Google Scholar circRNAs can act as important regulatory factors at both the transcriptional and posttranscriptional levels by sponging miRNAs, binding to RNA-binding proteins (RBPs), regulating parental gene expression, or serving as translation templates.25Zhang Y. Zhang X.O. Chen T. Xiang J.F. Yin Q.F. Xing Y.H. Zhu S. Yang L. Chen L.L. Circular intronic long noncoding RNAs.Mol. Cell. 2013; 51: 792-806Abstract Full Text Full Text PDF PubMed Scopus (990) Google Scholar, 26Conn S.J. Pillman K.A. Toubia J. Conn V.M. Salmanidis M. Phillips C.A. Roslan S. Schreiber A.W. Gregory P.A. Goodall G.J. The RNA binding protein quaking regulates formation of circRNAs.Cell. 2015; 160: 1125-1134Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar, 27Wang K. Long B. Liu F. Wang J.X. Liu C.Y. Zhao B. Zhou L.Y. Sun T. Wang M. Yu T. et al.A circular RNA protects the heart from pathological hypertrophy and heart failure by targeting miR-223.Eur. Heart J. 2016; 37: 2602-2611Crossref PubMed Scopus (441) Google Scholar, 28Du W.W. Fang L. Yang W. Wu N. Awan F.M. Yang Z. Yang B.B. Induction of tumor apoptosis through a circular RNA enhancing Foxo3 activity.Cell Death Differ. 2017; 24: 357-370Crossref PubMed Scopus (231) Google Scholar, 29Legnini I. Di Timoteo G. Rossi F. Morlando M. Briganti F. Sthandier O. Fatica A. Santini T. Andronache A. Wade M. et al.circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis.Mol. Cell. 2017; 66: 22-37.e9Abstract Full Text Full Text PDF PubMed Scopus (717) Google Scholar ciRS-7/CDR1as and sex-determining region Y (Sry, a testis-specific circRNA) can bind to miRNAs to regulate the progression of various diseases.15Hansen T.B. Kjems J. Damgaard C.K. Circular RNA and miR-7 in cancer.Cancer Res. 2013; 73: 5609-5612Crossref PubMed Scopus (574) Google Scholar,16Memczak S. Jens M. Elefsinioti A. Torti F. Krueger J. Rybak A. Maier L. Mackowiak S.D. Gregersen L.H. Munschauer M. et al.Circular RNAs are a large class of animal RNAs with regulatory potency.Nature. 2013; 495: 333-338Crossref PubMed Scopus (3330) Google Scholar,30Pan H. Li T. Jiang Y. Pan C. Ding Y. Huang Z. Yu H. Kong D. Overexpression of circular RNA ciRS-7 abrogates the tumor suppressive effect of miR-7 on gastric cancer via PTEN/PI3K/AKT signaling pathway.J. Cell. 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Commun. 2016; 7: 12429Crossref PubMed Scopus (444) Google Scholar ciRNA-ankrd52 can bind to RNA polymerase II (RNA Pol II) of the precursor (pre-)mRNA of the ANKRD52 gene to promote transcription.25Zhang Y. Zhang X.O. Chen T. Xiang J.F. Yin Q.F. Xing Y.H. Zhu S. Yang L. Chen L.L. Circular intronic long noncoding RNAs.Mol. Cell. 2013; 51: 792-806Abstract Full Text Full Text PDF PubMed Scopus (990) Google Scholar circFBXW7 can be a template for translation to generate a functional protein that represses glioma tumorigenesis.6Yang Y. Gao X. Zhang M. Yan S. Sun C. Xiao F. Huang N. Yang X. Zhao K. Zhou H. et al.Novel role of FBXW7 circular RNA in repressing glioma tumorigenesis.J. Natl. Cancer Inst. 2018; 110: 304-315Crossref Scopus (370) Google Scholar circFoxo3 is one of the most studied circRNAs. circFoxo3 is generated from the Foxo3 gene, which is considered a tumor suppressor gene.34Kenyon C.J. The genetics of ageing.Nature. 2010; 464: 504-512Crossref PubMed Scopus (1700) Google Scholar,35Willcox B.J. Tranah G.J. Chen R. Morris B.J. Masaki K.H. He Q. Willcox D.C. Allsopp R.C. Moisyadi S. Poon L.W. et al.The FoxO3 gene and cause-specific mortality.Aging Cell. 2016; 15: 617-624Crossref PubMed Scopus (32) Google Scholar circFoxo3 has been shown to have multiple functions in various cancers.28Du W.W. Fang L. Yang W. Wu N. Awan F.M. Yang Z. Yang B.B. Induction of tumor apoptosis through a circular RNA enhancing Foxo3 activity.Cell Death Differ. 2017; 24: 357-370Crossref PubMed Scopus (231) Google Scholar,36Zhou J. Zhou L.Y. Tang X. Zhang J. Zhai L.L. Yi Y.Y. Yi J. Lin J. Qian J. Deng Z.Q. circ-Foxo3 is positively associated with the Foxo3 gene and leads to better prognosis of acute myeloid leukemia patients.BMC Cancer. 2019; 19: 930Crossref PubMed Scopus (10) Google Scholar,37Shen Z. Zhou L. Zhang C. Xu J. Reduction of circular RNA Foxo3 promotes prostate cancer progression and chemoresistance to docetaxel.Cancer Lett. 2020; 468: 88-101Crossref PubMed Scopus (24) Google Scholar In this review, we summarize the current knowledge on the biogenesis and functions of circRNAs, elucidate the roles of circFoxo3 in cancers, and explore the clinical application of circFoxo3. circRNAs originate from pre-mRNAs by back-splicing, a unique mechanism that differs from canonical splicing, which generates mRNA.38Jeck W.R. Sorrentino J.A. Wang K. Slevin M.K. Burd C.E. Liu J. Marzluff W.F. Sharpless N.E. Circular RNAs are abundant, conserved, and associated with ALU repeats.RNA. 2013; 19: 141-157Crossref PubMed Scopus (1837) Google Scholar There are three types of circRNAs: exonic circRNAs (ecircRNAs or ecRNAs),20Zhang X.O. Wang H.B. Zhang Y. Lu X. Chen L.L. Yang L. Complementary sequence-mediated exon circularization.Cell. 2014; 159: 134-147Abstract Full Text Full Text PDF PubMed Scopus (804) Google Scholar circular intronic RNAs (ciRNAs),25Zhang Y. Zhang X.O. Chen T. Xiang J.F. Yin Q.F. Xing Y.H. Zhu S. Yang L. Chen L.L. Circular intronic long noncoding RNAs.Mol. Cell. 2013; 51: 792-806Abstract Full Text Full Text PDF PubMed Scopus (990) Google Scholar and exon-intron circRNAs (EIciRNAs),39Li Z. Huang C. Bao C. Chen L. Lin M. Wang X. Zhong G. Yu B. Hu W. Dai L. et al.Exon-intron circular RNAs regulate transcription in the nucleus.Nat. Struct. Mol. Biol. 2015; 22: 256-264Crossref PubMed Scopus (1136) Google Scholar which can be generated from different mechanisms. Jeck et al.38Jeck W.R. Sorrentino J.A. Wang K. Slevin M.K. Burd C.E. Liu J. Marzluff W.F. Sharpless N.E. Circular RNAs are abundant, conserved, and associated with ALU repeats.RNA. 2013; 19: 141-157Crossref PubMed Scopus (1837) Google Scholar reported two models of circRNA formation: lariat-driven circularization and intron pairing-driven circularization. In the lariat-driven circularization model, a 5′ splice donor (GU) and a 3′ splice acceptor (AG) in the introns can form a lariat that will then be internally spliced to generate an exonic circle (ecRNAs)38Jeck W.R. Sorrentino J.A. Wang K. Slevin M.K. Burd C.E. Liu J. Marzluff W.F. Sharpless N.E. Circular RNAs are abundant, conserved, and associated with ALU repeats.RNA. 2013; 19: 141-157Crossref PubMed Scopus (1837) Google Scholar,40Jeck W.R. Sharpless N.E. Detecting and characterizing circular RNAs.Nat. Biotechnol. 2014; 32: 453-461Crossref PubMed Scopus (1090) Google Scholar (Figure 1A). In the intron pairing-driven circularization model, the pairing of RNA base motifs (e.g., Alu repeats, the most highly repeated interspersed repeat element in humans that contributes to the occurrence of a wide range of diseases41Deininger P. Alu elements: know the SINEs.Genome Biol. 2011; 12: 236Crossref PubMed Scopus (251) Google Scholar) in the introns of pre-mRNA with reverse complementary sequences can facilitate the generation of ecRNAs (introns removed) or EIciRNAs (introns retained)38Jeck W.R. Sorrentino J.A. Wang K. Slevin M.K. Burd C.E. Liu J. Marzluff W.F. Sharpless N.E. Circular RNAs are abundant, conserved, and associated with ALU repeats.RNA. 2013; 19: 141-157Crossref PubMed Scopus (1837) Google Scholar (Figure 1B). A growing number of studies have illustrated that the intron pairing-driven circularization occurs more frequently than lariat-driven circularization.38Jeck W.R. Sorrentino J.A. Wang K. Slevin M.K. Burd C.E. Liu J. Marzluff W.F. Sharpless N.E. Circular RNAs are abundant, conserved, and associated with ALU repeats.RNA. 2013; 19: 141-157Crossref PubMed Scopus (1837) Google Scholar,39Li Z. Huang C. Bao C. Chen L. Lin M. Wang X. Zhong G. Yu B. Hu W. Dai L. et al.Exon-intron circular RNAs regulate transcription in the nucleus.Nat. Struct. Mol. Biol. 2015; 22: 256-264Crossref PubMed Scopus (1136) Google Scholar Moreover, some recent studies have suggested that RBPs, such as muscleblind (MBL) proteins, also participate in the formation of circRNAs.26Conn S.J. Pillman K.A. Toubia J. Conn V.M. Salmanidis M. Phillips C.A. Roslan S. Schreiber A.W. Gregory P.A. Goodall G.J. The RNA binding protein quaking regulates formation of circRNAs.Cell. 2015; 160: 1125-1134Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar,42Ashwal-Fluss R. Meyer M. Pamudurti N.R. Ivanov A. Bartok O. Hanan M. Evantal N. Memczak S. Rajewsky N. Kadener S. circRNA biogenesis competes with pre-mRNA splicing.Mol. Cell. 2014; 56: 55-66Abstract Full Text Full Text PDF PubMed Scopus (1228) Google Scholar The bridging of RBPs with pre-mRNAs is also a pathway for the production of circRNAs (ecRNAs or EIciRNAs)26Conn S.J. Pillman K.A. Toubia J. Conn V.M. Salmanidis M. Phillips C.A. Roslan S. Schreiber A.W. Gregory P.A. Goodall G.J. The RNA binding protein quaking regulates formation of circRNAs.Cell. 2015; 160: 1125-1134Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar,42Ashwal-Fluss R. Meyer M. Pamudurti N.R. Ivanov A. Bartok O. Hanan M. Evantal N. Memczak S. Rajewsky N. Kadener S. circRNA biogenesis competes with pre-mRNA splicing.Mol. Cell. 2014; 56: 55-66Abstract Full Text Full Text PDF PubMed Scopus (1228) Google Scholar (Figure 1C). Zhang et al.25Zhang Y. Zhang X.O. Chen T. Xiang J.F. Yin Q.F. Xing Y.H. Zhu S. Yang L. Chen L.L. Circular intronic long noncoding RNAs.Mol. Cell. 2013; 51: 792-806Abstract Full Text Full Text PDF PubMed Scopus (990) Google Scholar proposed a model that described the formation of ciRNAs. In the introns, the GU-rich element near the 5′ splice site and the C-rich element close to the branch will bind together during back-splicing.25Zhang Y. Zhang X.O. Chen T. Xiang J.F. Yin Q.F. Xing Y.H. Zhu S. Yang L. Chen L.L. Circular intronic long noncoding RNAs.Mol. Cell. 2013; 51: 792-806Abstract Full Text Full Text PDF PubMed Scopus (990) Google Scholar The other exons and introns are removed by a spliceosome. In this mechanism, only ciRNAs are formed25Zhang Y. Zhang X.O. Chen T. Xiang J.F. Yin Q.F. Xing Y.H. Zhu S. Yang L. Chen L.L. Circular intronic long noncoding RNAs.Mol. Cell. 2013; 51: 792-806Abstract Full Text Full Text PDF PubMed Scopus (990) Google Scholar (Figure 1D). circRNAs have the following common biological properties: (1) high stability: due to their circular structures, circRNAs are more stable than linear RNAs and cannot be cleaved by ribonuclease (RNase).43Suzuki H. Zuo Y. Wang J. Zhang M.Q. Malhotra A. Mayeda A. Characterization of RNase R-digested cellular RNA source that consists of lariat and circular RNAs from pre-mRNA splicing.Nucleic Acids Res. 2006; 34: e63Crossref PubMed Scopus (286) Google Scholar (2) Wide distribution: circRNAs exist in a variety of organisms and all tissues.38Jeck W.R. Sorrentino J.A. Wang K. Slevin M.K. Burd C.E. Liu J. Marzluff W.F. Sharpless N.E. Circular RNAs are abundant, conserved, and associated with ALU repeats.RNA. 2013; 19: 141-157Crossref PubMed Scopus (1837) Google Scholar,44Xu T. Wu J. Han P. Zhao Z. Song X. 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Zou Q. A comprehensive overview and evaluation of circular RNA detection tools.PLoS Comput. Biol. 2017; 13: e1005420Crossref PubMed Scopus (160) Google Scholar (3) Specificity: the expression of circRNAs is tissue-, cell-, and developmental stage-specific.44Xu T. Wu J. Han P. Zhao Z. Song X. Circular RNA expression profiles and features in human tissues: a study using RNA-seq data.BMC Genomics. 2017; 18: 680Crossref PubMed Scopus (86) Google Scholar,47Jakobi T. Czaja-Hasse L.F. Reinhardt R. Dieterich C. Profiling and validation of the circular RNA repertoire in adult murine hearts.Genomics Proteomics Bioinformatics. 2016; 14: 216-223Crossref PubMed Scopus (54) Google Scholar,48Li Y. Zhang J. Huo C. Ding N. Li J. Xiao J. Lin X. Cai B. Zhang Y. Xu J. 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(4) Conservation: many circRNAs are conservatively expressed among species,38Jeck W.R. Sorrentino J.A. Wang K. Slevin M.K. Burd C.E. Liu J. Marzluff W.F. Sharpless N.E. Circular RNAs are abundant, conserved, and associated with ALU repeats.RNA. 2013; 19: 141-157Crossref PubMed Scopus (1837) Google Scholar,50AbouHaidar M.G. 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. USA. 2014; 111: 14542-14547Crossref PubMed Scopus (90) Google Scholar whereas a number of circRNAs are specific to species.19Guo J.U. Agarwal V. Guo H. Bartel D.P. Expanded identification and characterization of mammalian circular RNAs.Genome Biol. 2014; 15: 409Crossref PubMed Scopus (778) Google Scholar,49Werfel S. Nothjunge S. Schwarzmayr T. Strom T.M. Meitinger T. Engelhardt S. Characterization of circular RNAs in human, mouse and rat hearts.J. Mol. Cell. 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Circular RNAs: analysis, expression and potential functions.Development. 2016; 143: 1838-1847Crossref PubMed Scopus (350) Google Scholar also confirmed that only ~5%–30% of sequences are homologous among mammals, including mice, humans, rats, and pigs. (5) Altered expression in normal and pathological conditions: studies have identified the differential expression of circRNAs in various diseases.49Werfel S. Nothjunge S. Schwarzmayr T. Strom T.M. Meitinger T. Engelhardt S. Characterization of circular RNAs in human, mouse and rat hearts.J. Mol. Cell. Cardiol. 2016; 98: 103-107Abstract Full Text Full Text PDF PubMed Google Scholar,54Siede D. Rapti K. Gorska A.A. Katus H.A. Altmüller J. Boeckel J.N. Meder B. Maack C. Völkers M. Müller O.J. et al.Identification of circular RNAs with host gene-independent expression in human model systems for cardiac differentiation and disease.J. Mol. Cell. Cardiol. 2017; 109: 48-56Abstract Full Text Full Text PDF PubMed Google Scholar,55Gupta S.K. 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• W3124389218 title "Pathogenic mechanisms and the potential clinical value of circFoxo3 in cancers" @default.
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