Regulatory circular RNAs in viral diseases: applications in diagnosis and therapy

References

• Carninci P, Kasukawa T, Katayama S, et al. The transcriptional landscape of the mammalian Genome. Science. 2005;309(5740):1559–1563. doi: 10.1126/science.1112014
   PubMed Web of Science ®Google Scholar
• Elgar G, Vavouri T. Tuning in to the signals: noncoding sequence conservation in vertebrate genomes. Trends Genet. 2008;24(7):344–352. doi: 10.1016/j.tig.2008.04.005
   PubMed Web of Science ®Google Scholar
• Adelman K, Egan E. More uses for genomic junk. Nature. 2017;543(7644):183–185. doi: 10.1038/543183a
   PubMed Web of Science ®Google Scholar
• Jeck WR, Sorrentino JA, Wang K, et al. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA. 2013;19(2):141–157. doi: 10.1261/rna.035667.112
   PubMed Web of Science ®Google Scholar
• Memczak S, Jens M, Elefsinioti A, et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature. 2013;495(7441):333–338. doi: 10.1038/nature11928
   PubMed Web of Science ®Google Scholar
• Liu X, Hu Z, Zhou J, et al. Interior circular RNA. RNA Biol. 2020;17(1):87–97. doi: 10.1080/15476286.2019.1669391
   PubMed Web of Science ®Google Scholar
• Zhao Q, Liu J, Deng H, et al. Targeting mitochondria-located circRNA SCAR alleviates NASH via reducing mROS Output. Cell. 2020;183(1):76–93.e22. doi: 10.1016/j.cell.2020.08.009
   PubMed Web of Science ®Google Scholar
• Jiao J, Li C, Ning L, et al. Electrochemical detection of circRnas based on the combination of back-splice junction and duplex-specific nuclease. Sensors And Actuat B Chem. 2020;302:127166. doi: 10.1016/j.snb.2019.127166
   Web of Science ®Google Scholar
• Vincent HA, Deutscher MP. Substrate recognition and catalysis by the exoribonuclease RNase R. J Biol Chem. 2006;281(40):29769–29775. doi: 10.1074/jbc.M606744200
   PubMed Web of Science ®Google Scholar
• Suzuki H. Characterization of RNase R-digested cellular RNA source that consists of lariat and circular RNAs from pre-mRNA splicing. Nucleic Acids Res. 2006;34(8):e63–e63. doi: 10.1093/nar/gkl151
   PubMed Web of Science ®Google Scholar
• Wang Y, Wu C, Du Y, et al. Expanding uncapped translation and emerging function of circular RNA in carcinomas and noncarcinomas. Mol Cancer. 2022;21(1):13. doi: 10.1186/s12943-021-01484-7
   PubMed Web of Science ®Google Scholar
• Huang A, Zheng H, Wu Z, et al. Circular RNA-protein interactions: functions, mechanisms, and identification. Theranostics. 2020;10(8):3503–3517. doi: 10.7150/thno.42174
   PubMed Web of Science ®Google Scholar
• Niu M, Ju Y, Lin C, et al. Characterizing viral circRnas and their application in identifying circRnas in viruses. Brief Bioinform. 2022;23(1):bbab404. doi: 10.1093/bib/bbab404
   PubMed Web of Science ®Google Scholar
• Yan L, Chen YG. Circular RNAs in immune response and viral infection. Trends Biochem Sci. 2020;45(12):1022–1034. doi: 10.1016/j.tibs.2020.08.006
   PubMed Web of Science ®Google Scholar
• Tagawa T, Oh D, Dremel S, et al. A virus-induced circular RNA maintains latent infection of Kaposi’s sarcoma herpesvirus. Proc Natl Acad Sci, USA. 2023;120(6):e2212864120. doi: 10.1073/pnas.2212864120
   PubMed Web of Science ®Google Scholar
• Liu C-X, Li X, Nan F, et al. Structure and degradation of circular RNAs regulate PKR activation in innate immunity. Cell. 2019;177(4):865–880.e21. doi: 10.1016/j.cell.2019.03.046
   PubMed Web of Science ®Google Scholar
• Gong L, Chen J, Dong M, et al. Epstein–Barr virus‐derived circular RNA lMP2A induces stemness in EBV‐associated gastric cancer. EMBO Rep. 2020;21(10):e49689. doi: 10.15252/embr.201949689
   PubMed Web of Science ®Google Scholar
• Niu M, Zhang J, Li Y, et al. CirRNAPL: a web server for the identification of circRNA based on extreme learning machine. Computat Struct Biotechnol J. 2020;18:834–842. doi: 10.1016/j.csbj.2020.03.028
   PubMed Web of Science ®Google Scholar
• Berman TA, Schiller JT. Human papillomavirus in cervical cancer and oropharyngeal cancer: one cause, two diseases. Cancer. 2017;123(12):2219–2229. doi: 10.1002/cncr.30588
   PubMed Web of Science ®Google Scholar
• Torresi J, Tran BM, Christiansen D, et al. HBV-related hepatocarcinogenesis: the role of signalling pathways and innovative ex vivo research models. BMC Cancer. 2019;19(1):707. doi: 10.1186/s12885-019-5916-6
   PubMedGoogle Scholar
• Abere B, Li J, Zhou H, et al. Kaposi’s sarcoma-associated herpesvirus-encoded circRnas are expressed in infected tumor tissues and are incorporated into Virions. MBio. 2020;11(1):e03027–19. doi: 10.1128/mBio.03027-19
   PubMed Web of Science ®Google Scholar
• Ungerleider N, Concha M, Lin Z, et al. The Epstein Barr virus circRnaome. PLOS Pathog. 2018;14(8):e1007206. doi: 10.1371/journal.ppat.1007206
   PubMed Web of Science ®Google Scholar
• Huang J, Chen J, Gong L, et al. Identification of virus-encoded circular RNA. Virology. 2019;529:144–151. doi: 10.1016/j.virol.2019.01.014
   PubMed Web of Science ®Google Scholar
• Wu F, Cheng W, Zhao F, et al. Association of N6-methyladenosine with viruses and related diseases. Virol J. 2019;16(1):133. doi: 10.1186/s12985-019-1236-3
   PubMed Web of Science ®Google Scholar
• Tonkin J, Rosenthal N. One small step for muscle: a New micropeptide regulates performance. Cell Metab. 2015;21(4):515–516. doi: 10.1016/j.cmet.2015.03.013
   PubMed Web of Science ®Google Scholar
• Granados-Riveron JT, Aquino-Jarquin G. The complexity of the translation ability of circRnas. Biochim Biophys Acta Gene Regul Mech. 2016;1859(10):1245–1251. doi: 10.1016/j.bbagrm.2016.07.009
   PubMed Web of Science ®Google Scholar
• Legnini I, Di Timoteo G, Rossi F, et al. Circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis. Molecular Cell. 2017;66(1):22–37.e9. doi: 10.1016/j.molcel.2017.02.017
   PubMed Web of Science ®Google Scholar
• Pamudurti NR, Bartok O, Jens M, et al. Translation of CircRNAs. Molecular Cell. 2017;66(1):9–21.e7. doi: 10.1016/j.molcel.2017.02.021
   PubMed Web of Science ®Google Scholar
• van Heesch S, Witte F, Schneider-Lunitz V, et al. The translational landscape of the human heart. Cell. 2019;178(1):242–260.e29. doi: 10.1016/j.cell.2019.05.010
   PubMed Web of Science ®Google Scholar
• Gao X, Xia X, Li F, et al. Circular RNA-encoded oncogenic E-cadherin variant promotes glioblastoma tumorigenicity through activation of EGFR–STAT3 signalling. Nat Cell Biol. 2021;23(3):278–291. doi: 10.1038/s41556-021-00639-4
   PubMed Web of Science ®Google Scholar
• Liang W-C, Wong C-W, Liang P-P, et al. Translation of the circular RNA circβ-catenin promotes liver cancer cell growth through activation of the wnt pathway. Genome Biol. 2019;20(1):84. doi: 10.1186/s13059-019-1685-4
   PubMed Web of Science ®Google Scholar
• Zheng X, Chen L, Zhou Y, et al. A novel protein encoded by a circular RNA circPPP1R12A promotes tumor pathogenesis and metastasis of colon cancer via hippo-YAP signaling. Mol Cancer. 2019;18(1):47. doi: 10.1186/s12943-019-1010-6
   PubMed Web of Science ®Google Scholar
• Wu X, Xiao S, Zhang M, et al. A novel protein encoded by circular SMO RNA is essential for hedgehog signaling activation and glioblastoma tumorigenicity. Genome Biol. 2021;22(1):33. doi: 10.1186/s13059-020-02250-6
   PubMed Web of Science ®Google Scholar
• Yang Y, Fan X, Mao M, et al. Extensive translation of circular RNAs driven by N6-methyladenosine. Cell Res. 2017;27(5):626–641. doi: 10.1038/cr.2017.31
   PubMed Web of Science ®Google Scholar
• Petkovic S, Müller S. RNA circularization strategies in vivo and in vitro. Nucleic Acids Res. 2015;43(4):2454–2465. doi: 10.1093/nar/gkv045
   PubMed Web of Science ®Google Scholar
• Chen L-L. The expanding regulatory mechanisms and cellular functions of circular RNAs. Nat Rev Mol Cell Biol. 2020;21(8):475–490. doi: 10.1038/s41580-020-0243-y
   PubMed Web of Science ®Google Scholar
• Yang L, Wilusz JE, Chen L-L. Biogenesis and regulatory roles of circular RNAs. Annu Rev Cell Dev Biol. 2022;38(1):263–289. doi: 10.1146/annurev-cellbio-120420-125117
   PubMedGoogle Scholar
• Zhang X-O, Wang H-B, Zhang Y, et al. Complementary sequence-mediated Exon Circularization. Cell. 2014;159(1):134–147. doi: 10.1016/j.cell.2014.09.001
   PubMed Web of Science ®Google Scholar
• Ivanov A, Memczak S, Wyler E, et al. Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals. Cell Rep. 2015;10(2):170–177. doi: 10.1016/j.celrep.2014.12.019
   PubMed Web of Science ®Google Scholar
• Wilusz JE. Circular RNAs: unexpected outputs of many protein-coding genes. RNA Biol. 2017;14(8):1007–1017. doi: 10.1080/15476286.2016.1227905
   PubMed Web of Science ®Google Scholar
• Ashwal-Fluss R, Meyer M, Pamudurti NR, et al. circRNA biogenesis competes with pre-mRNA splicing. Molecular Cell. 2014;56(1):55–66. doi: 10.1016/j.molcel.2014.08.019
   PubMed Web of Science ®Google Scholar
• Aktaş T, Avşar Ilık İ, Maticzka D, et al. DHX9 suppresses RNA processing defects originating from the Alu invasion of the human genome. Nature. 2017;544(7648):115–119. doi: 10.1038/nature21715
   PubMed Web of Science ®Google Scholar
• Li X, Liu C-X, Xue W, et al. Coordinated circRNA biogenesis and function with NF90/NF110 in viral infection. Molecular Cell. 2017;67(2):214–227.e7. doi: 10.1016/j.molcel.2017.05.023
   PubMed Web of Science ®Google Scholar
• Fei T, Chen Y, Xiao T, et al. Genome-wide CRISPR screen identifies HNRNPL as a prostate cancer dependency regulating RNA splicing. Proc Natl Acad Sci, USA Internet. 2017 [[cited 2023 Mar 9]];114(26): doi: 10.1073/pnas.1617467114
   Web of Science ®Google Scholar
• Conn SJ, Pillman KA, Toubia J, et al. The RNA binding protein quaking regulates formation of circRnas. Cell. 2015;160(6):1125–1134. doi: 10.1016/j.cell.2015.02.014
   PubMed Web of Science ®Google Scholar
• Stagsted LVW, O’Leary ET, Ebbesen KK, et al. The RNA-binding protein SFPQ preserves long-intron splicing and regulates circRNA biogenesis in mammals. Elife. 2021;10:e63088. doi: 10.7554/eLife.63088
   PubMed Web of Science ®Google Scholar
• Errichelli L, Dini Modigliani S, Laneve P, et al. FUS affects circular RNA expression in murine embryonic stem cell-derived motor neurons. Nat Commun. 2017;8(1):14741. doi: 10.1038/ncomms14741
   PubMed Web of Science ®Google Scholar
• Kramer MC, Liang D, Tatomer DC, et al. Combinatorial control of Drosophila circular RNA expression by intronic repeats, hnRnps, and SR proteins. Genes Dev. 2015;29(20):2168–2182. doi: 10.1101/gad.270421.115
   PubMed Web of Science ®Google Scholar
• Liang D, Tatomer DC, Luo Z, et al. The output of protein-coding genes shifts to circular RNAs when the pre-mRNA processing machinery is limiting. Molecular Cell. 2017;68(5):940–954.e3. doi: 10.1016/j.molcel.2017.10.034
   PubMed Web of Science ®Google Scholar
• Chen X, Lu Y. Circular RNA: biosynthesis in vitro. Front Bioeng Biotechnol. 2021;9:787881. doi: 10.3389/fbioe.2021.787881
   PubMed Web of Science ®Google Scholar
• Moore MJ. Joining RNA molecules with T4 DNA ligase [Internet. In RNA-Protein interaction protocols. New Jersey: Humana Press; 1999. cited 2023 Mar 9 pp. 11–19. http://link.springer.com/10.1385/1-59259-676-2:11
   Google Scholar
• Umekage S, Kikuchi Y. In vitro and in vivo production and purification of circular RNA aptamer. J Biotechnol. 2009;139(4):265–272. doi: 10.1016/j.jbiotec.2008.12.012
   PubMed Web of Science ®Google Scholar
• Wesselhoeft RA, Kowalski PS, Anderson DG. Engineering circular RNA for potent and stable translation in eukaryotic cells. Nat Commun. 2018;9(1):2629. doi: 10.1038/s41467-018-05096-6
   PubMed Web of Science ®Google Scholar
• Rausch JW, Heinz WF, Payea MJ, et al. Characterizing and circumventing sequence restrictions for synthesis of circular RNA in vitro. Science. 2021;49(6):e35–e35. doi: 10.1093/nar/gkaa1256
   Google Scholar
• Chen YG, Kim MV, Chen X, et al. Sensing self and foreign circular RNAs by intron identity. Molecular Cell. 2017;67(2):228–238.e5. doi: 10.1016/j.molcel.2017.05.022
   PubMed Web of Science ®Google Scholar
• Meganck RM, Liu J, Hale AE, et al. Engineering highly efficient backsplicing and translation of synthetic circRnas. Mol Ther Nucleic Acids. 2021;23:821–834. doi: 10.1016/j.omtn.2021.01.003
   PubMedGoogle Scholar
• Chen R, Wang SK, Belk JA, et al. Author correction: engineering circular RNA for enhanced protein production. Nature Biotechnol. 2022;1–11. doi: 10.1038/s41587-022-01472-2
   PubMed Web of Science ®Google Scholar
• Huang X, Kong N, Zhang X, et al. The landscape of mRNA nanomedicine. Nat Med. 2022;28(11):2273–2287. doi: 10.1038/s41591-022-02061-1
   PubMed Web of Science ®Google Scholar
• Paludan SR, Pradeu T, Masters SL, et al. Constitutive immune mechanisms: mediators of host defence and immune regulation. Nat Rev Immunol. 2021;21(3):137–150. doi: 10.1038/s41577-020-0391-5
   PubMed Web of Science ®Google Scholar
• Chen X, Yang T, Wang W, et al. Circular RNAs in immune responses and immune diseases. Theranostics. 2019;9(2):588–607. doi: 10.7150/thno.29678
   PubMed Web of Science ®Google Scholar
• Wang X, Lu Z, Gomez A, et al. N6-methyladenosine-dependent regulation of messenger RNA stability. Nature. 2014;505(7481):117–120. doi: 10.1038/nature12730
   PubMed Web of Science ®Google Scholar
• Lu M, Zhang Z, Xue M, et al. N6-methyladenosine modification enables viral RNA to escape recognition by RNA sensor RIG-I. Nat Microbiol. 2020;5(4):584–598. doi: 10.1038/s41564-019-0653-9
   PubMed Web of Science ®Google Scholar
• Baquero-Perez B, Geers D, Díez J. From a to m6A: the emerging viral epitranscriptome. Viruses. 2021;13(6):1049. doi: 10.3390/v13061049
   PubMed Web of Science ®Google Scholar
• Tan K, Lim Y. Viruses join the circular RNA world. FEBS J. 2021;288(15):4488–4502. doi: 10.1111/febs.15639
   PubMed Web of Science ®Google Scholar
• Du L, Wang X, Liu J, et al. A Previously undiscovered circular RNA, circTNFAIP3, and its role in coronavirus replication. MBio. 2021;12(6):e02984–21. doi: 10.1128/mBio.02984-21
   PubMed Web of Science ®Google Scholar
• Zhang X, Liang Z, Wang C, et al. Viral circular RNAs and their possible roles in virus-host interaction. Front Immunol. 2022;13:939768. doi: 10.3389/fimmu.2022.939768
   PubMed Web of Science ®Google Scholar
• Role of non­coding RNAs in dengue virus­host interaction. Front Biosci (Schol Ed) 2021;13:44.
   PubMedGoogle Scholar
• Toptan T, Abere B, Nalesnik MA, et al. Circular DNA tumor viruses make circular RNAs. Proc Natl Acad Sci, USA Internet. 2018 [cited 2023 Mar 9];115(37). doi:10.1073/pnas.1811728115
   PubMed Web of Science ®Google Scholar
• Tagawa T, Gao S, Koparde VN, et al. Discovery of Kaposi’s sarcoma herpesvirus-encoded circular RNAs and a human antiviral circular RNA. Proc Natl Acad Sci, USA. 2018;115(50):12805–12810. doi: 10.1073/pnas.1816183115
   PubMed Web of Science ®Google Scholar
• Zhao J, Lee EE, Kim J, et al. Translation and transforming activity of a circular RNA from human papillomavirus [Internet]. Mol Biol. 2019 [cited 2023 Mar 9]. Available from: doi: 10.1101/600056
   PubMedGoogle Scholar
• Zhu M, Liang Z, Pan J, et al. Hepatocellular carcinoma progression mediated by hepatitis B virus-encoded circRNA HBV_circ_1 through interaction with CDK1. Mol Ther Nucleic Acids. 2021;25:668–682. doi: 10.1016/j.omtn.2021.08.011
   PubMedGoogle Scholar
• Chasseur AS, Trozzi G, Istasse C, et al. Marek’s disease virus virulence genes encode circular RNAs. J Virol. 2022;96(9):e00321–22. doi: 10.1128/jvi.00321-22
   PubMed Web of Science ®Google Scholar
• Cai Z, Lu C, He J, et al. Identification and characterization of circRnas encoded by MERS-CoV, SARS-CoV-1 and SARS-CoV-2. Brief Bioinform. 2021;22(2):1297–1308. doi: 10.1093/bib/bbaa334
   PubMed Web of Science ®Google Scholar
• Pan J, Zhang X, Zhang Y, et al. Grass carp reovirus encoding circular RNAs with antiviral activity. Aquaculture. 2021;533:736135. doi: 10.1016/j.aquaculture.2020.736135
   Web of Science ®Google Scholar
• Yang R, Lee EE, Kim J, et al. Characterization of ALTO-encoding circular RNAs expressed by Merkel cell p olyomavirus and trichodysplasia spinulosa polyomavirus. PLOS Pathog. 2021;17(5):e1009582. doi: 10.1371/journal.ppat.1009582
   PubMed Web of Science ®Google Scholar
• Li X, Yang L, Chen L-L. The biogenesis, functions, and challenges of circular RNAs. Molecular Cell. 2018;71(3):428–442. doi: 10.1016/j.molcel.2018.06.034
   PubMed Web of Science ®Google Scholar
• Zhang J, Du Y, Gong L, et al. Ebv-circRPMS1 promotes the progression of EBV-associated gastric carcinoma via Sam68-dependent activation of METTL3. Cancer Lett. 2022;535:215646. doi: 10.1016/j.canlet.2022.215646
   PubMed Web of Science ®Google Scholar
• Chen YG, Chen R, Ahmad S, et al. N6-methyladenosine modification controls circular RNA immunity. Molecular Cell. 2019;76(1):96–109.e9. doi: 10.1016/j.molcel.2019.07.016
   PubMed Web of Science ®Google Scholar
• Uppal T, Banerjee S, Sun Z, et al. KSHV LANA—the master regulator of KSHV latency. Viruses. 2014;6(12):4961–4998. doi: 10.3390/v6124961
   PubMed Web of Science ®Google Scholar
• Yu T, Ding Y, Zhang Y, et al. Circular RNA GATAD2A promotes H1N1 replication through inhibiting autophagy. Vet Microbiol. 2019;231:238–245. doi: 10.1016/j.vetmic.2019.03.012
   PubMed Web of Science ®Google Scholar
• Chen T-C, Tallo-Parra M, Cao QM, et al. Host-derived circular RNAs display proviral activities in hepatitis C virus-infected cells. PLOS Pathog. 2020;16(8):e1008346. doi: 10.1371/journal.ppat.1008346
   PubMed Web of Science ®Google Scholar
• Zhang X, Chu H, Wen L, et al. Competing endogenous RNA network profiling reveals novel host dependency factors required for MERS-CoV propagation. Emerg Microbes Infect. 2020;9(1):733–746. doi: 10.1080/22221751.2020.1738277
   PubMed Web of Science ®Google Scholar
• Koh W, Pan W, Gawad C, et al. Noninvasive in vivo monitoring of tissue-specific global gene expression in humans. Proc Natl Acad Sci, USA. 2014;111(20):7361–7366. doi: 10.1073/pnas.1405528111
   PubMed Web of Science ®Google Scholar
• Memczak S, Papavasileiou P, Peters O, et al. Identification and characterization of circular RNAs as a New class of putative biomarkers in human blood. PLoS One. 2015;10(10):e0141214. doi: 10.1371/journal.pone.0141214
   PubMed Web of Science ®Google Scholar
• Zebardast A, Latifi T, Shirzad M, et al. Critical involvement of circular RNAs in virus-associated cancers. Genes Dis. 2022;10(6):S2296–2305. doi: 10.1016/j.gendis.2022.04.009
   PubMed Web of Science ®Google Scholar
• Chamseddin BH, Lee EE, Kim J, et al. Assessment of circularized E7 RNA, GLUT1, and PD-L1 in anal squamous cell carcinoma. Oncotarget. 2019;10(57):5958–5969. doi: 10.18632/oncotarget.27234
   PubMedGoogle Scholar
• Su H, Chu Q, Zheng W, et al. Circular RNA circPikfyve acts as a sponge of miR-21-3p to enhance antiviral immunity through regulation of MAVS in teleost fish. J Virol. 2021;95(8):e02296–20. doi: 10.1128/JVI.02296-20
   PubMed Web of Science ®Google Scholar
• Su H, Zheng W, Pan J, et al. Circular RNA circSamd4a regulates antiviral immunity in teleost fish by Upregulating STING through sponging miR-29a-3p. J Immunol. 2021;207(11):2770–2784. doi: 10.4049/jimmunol.2100469
   PubMed Web of Science ®Google Scholar
• Chu Q, Zheng W, Su H, et al. A highly conserved circular RNA, circRasgef1b, enhances antiviral immunity by regulating the miR-21-3p/MITA pathway in lower vertebrates. J Virol. 2021;95(7):e02145–20. doi: 10.1128/JVI.02145-20
   PubMed Web of Science ®Google Scholar
• Yao W, Pan J, Liu Z, et al. The cellular and viral circRnaome induced by Respiratory syncytial virus infection. MBio. 2021;12(6):e03075–21. doi: 10.1128/mBio.03075-21
   PubMed Web of Science ®Google Scholar
• Kurreck J. RNA interference: from basic research to therapeutic applications. Angew Chem Int Ed. 2009;48(8):1378–1398. doi: 10.1002/anie.200802092
   PubMed Web of Science ®Google Scholar
• Setten RL, Rossi JJ, Han S. The current state and future directions of RNAi-based therapeutics. Nat Rev Drug Discov. 2019;18(6):421–446. doi: 10.1038/s41573-019-0017-4
   PubMed Web of Science ®Google Scholar
• Ni S, Zhuo Z, Pan Y, et al. Recent progress in aptamer discoveries and modifications for therapeutic applications. ACS Appl Mater Interfaces. 2021;13(8):9500–9519. doi: 10.1021/acsami.0c05750
   PubMed Web of Science ®Google Scholar
• Pfafenrot C, Schneider T, Müller C, et al. Inhibition of SARS-CoV-2 coronavirus proliferation by designer antisense-circRnas. Nucleic Acids Res. 2021;49(21):12502–12516. doi: 10.1093/nar/gkab1096
   PubMed Web of Science ®Google Scholar
• Henke JI, Goergen D, Zheng J, et al. microRNA-122 stimulates translation of hepatitis C virus RNA. EMBO J. 2008;27(24):3300–3310. doi: 10.1038/emboj.2008.244
   PubMed Web of Science ®Google Scholar
• Jost I, Shalamova LA, Gerresheim GK, et al. Functional sequestration of microRNA-122 from hepatitis C virus by circular RNA sponges. RNA Biol. 2018;1–8. doi: 10.1080/15476286.2018.1435248
   Web of Science ®Google Scholar
• Kristensen LS, Andersen MS, Stagsted LVW, et al. The biogenesis, biology and characterization of circular RNAs. Nat Rev Genet. 2019;20(11):675–691. doi: 10.1038/s41576-019-0158-7
   PubMed Web of Science ®Google Scholar
• Chen C, Sarnow P. Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs. Science. 1995;268(5209):415–417. doi: 10.1126/science.7536344
   PubMed Web of Science ®Google Scholar
• Wang K-S, Choo Q-L, Weiner AJ, et al. Structure, sequence and expression of the hepatitis delta (δ) viral genome. Nature. 1986;323(6088):508–514. doi: 10.1038/323508a0
   PubMed Web of Science ®Google Scholar
• Makino S, Chang M-F, Shieh C-K, et al. Molecular cloning and sequencing of a human hepatitis delta (δ) virus RNA. Nature. 1987;329(6137):343–346. doi: 10.1038/329343a0
   PubMed Web of Science ®Google Scholar
• AbouHaidar MG, Venkataraman S, Golshani A, et al. Novel coding, translation, and gene expression of a replicating covalently closed circular RNA of 220 nt. Proc Natl Acad Sci, USA. 2014;111(40):14542–14547. doi: 10.1073/pnas.1402814111
   PubMed Web of Science ®Google Scholar
• Wang Y, Wang Z. Efficient backsplicing produces translatable circular mRnas. RNA. 2015;21(2):172–179. doi: 10.1261/rna.048272.114
   PubMed Web of Science ®Google Scholar
• Abe N, Hiroshima M, Maruyama H, et al. Rolling circle amplification in a prokaryotic translation System using small circular RNA. Angew Chem Int Ed. 2013;52(27):7004–7008. doi: 10.1002/anie.201302044
   PubMed Web of Science ®Google Scholar
• Abe N, Matsumoto K, Nishihara M, et al. Rolling circle translation of circular RNA in living human cells. Sci Rep. 2015;5(1):16435. doi: 10.1038/srep16435
   PubMedGoogle Scholar
• Fan X, Yang Y, Chen C, et al. Pervasive translation of circular RNAs driven by short IRES-like elements. Nat Commun. 2022;13(1):3751. doi: 10.1038/s41467-022-31327-y
   PubMed Web of Science ®Google Scholar
• Zhou C, Molinie B, Daneshvar K, et al. Genome-wide maps of m6A circRnas identify widespread and Cell-type-specific methylation patterns that are distinct from mRnas. Cell Rep. 2017;20(9):2262–2276. doi: 10.1016/j.celrep.2017.08.027
   PubMed Web of Science ®Google Scholar
• Koch L. Translated circular RNAs. Nat Rev Genet. 2017;18(5):272–273. doi: 10.1038/nrg.2017.27
   PubMed Web of Science ®Google Scholar
• Qu L, Yi Z, Shen Y, et al. Circular RNA vaccines against SARS-CoV-2 and emerging variants. Cell. 2022;185(10):1728–1744.e16. doi: 10.1016/j.cell.2022.03.044
   PubMed Web of Science ®Google Scholar
• Deng Y-Q, Zhang N-N, Zhang Y-F, et al. Lipid nanoparticle-encapsulated mRNA antibody provides long-term protection against SARS-CoV-2 in mice and hamsters. Cell Res. 2022;32(4):375–382. doi: 10.1038/s41422-022-00630-0
   PubMed Web of Science ®Google Scholar
• Pardi N, Secreto AJ, Shan X, et al. Administration of nucleoside-modified mRNA encoding broadly neutralizing antibody protects humanized mice from HIV-1 challenge. Nat Commun. 2017;8(1):14630. doi: 10.1038/ncomms14630
   PubMedGoogle Scholar
• Rurik JG, Tombácz I, Yadegari A, et al. CAR T cells produced in vivo to treat cardiac injury. Science. 2022;375(6576):91–96. doi: 10.1126/science.abm0594
   PubMed Web of Science ®Google Scholar
• Chen Y, Li C, Tan C, et al. Circular RNAs: a new frontier in the study of human diseases. J Med Genet. 2016;53(6):359–365. doi: 10.1136/jmedgenet-2016-103758
   PubMed Web of Science ®Google Scholar
• Ye D, Gong M, Deng Y, et al. Roles and clinical application of exosomal circRnas in the diagnosis and treatment of malignant tumors. J Transl Med. 2022;20(1):161. doi: 10.1186/s12967-022-03367-x
   PubMed Web of Science ®Google Scholar
• Wesselhoeft RA, Kowalski PS, Parker-Hale FC, et al. RNA circularization diminishes immunogenicity and can extend translation duration in vivo. Molecular Cell. 2019;74(3):508–520.e4. doi: 10.1016/j.molcel.2019.02.015
   PubMed Web of Science ®Google Scholar
• Litke JL, Jaffrey SR. Highly efficient expression of circular RNA aptamers in cells using autocatalytic transcripts. Nat Biotechnol. 2019;37(6):667–675. doi: 10.1038/s41587-019-0090-6
   PubMed Web of Science ®Google Scholar
• Lokugamage MP, Gan Z, Zurla C, et al. Mild innate immune activation overrides efficient nanoparticle‐mediated RNA delivery. Adv Mater. 2020;32(1):1904905. doi: 10.1002/adma.201904905
   Web of Science ®Google Scholar
• Paunovska K, Da Silva Sanchez A, Foster MT, et al. Increased PIP3 activity blocks nanoparticle mRNA delivery. Sci Adv. 2020;6(30):eaba5672. doi: 10.1126/sciadv.aba5672
   PubMed Web of Science ®Google Scholar
• Westholm JO, Miura P, Olson S, et al. Genome-wide Analysis of Drosophila circular RNAs reveals their structural and sequence properties and age-dependent neural accumulation. Cell Rep. 2014;9(5):1966–1980. doi: 10.1016/j.celrep.2014.10.062
   PubMed Web of Science ®Google Scholar
• Hansen TB, Jensen TI, Clausen BH, et al. Natural RNA circles function as efficient microRNA sponges. Nature. 2013;495(7441):384–388. doi: 10.1038/nature11993
   PubMed Web of Science ®Google Scholar
• Meng J, Chen S, Han J-X, et al. Twist1 regulates Vimentin through Cul2 circular RNA to promote EMT in hepatocellular carcinoma. Cancer Res. 2018;78(15):4150–4162. doi: 10.1158/0008-5472.CAN-17-3009
   PubMed Web of Science ®Google Scholar
• Xie H, Sun H, Mu R, et al. The role of circular RNAs in viral infection and related diseases. Virus res. 2021;291:198205. doi: 10.1016/j.virusres.2020.198205
   PubMed Web of Science ®Google Scholar