How are circRNAs translated by non-canonical initiation mechanisms?

Nigro, 1991, Scrambled exons, Cell, 64, 607, 10.1016/0092-8674(91)90244-S Cocquerelle, 1993, Mis-splicing yields circular RNA molecules, FASEB J., 7, 155, 10.1096/fasebj.7.1.7678559 Huang, 2017, The emerging role of circular RNAs in transcriptome regulation, Genomics, 109, 401, 10.1016/j.ygeno.2017.06.005 Bolha, 2017, Circular rnas: biogenesis, function, and a role as possible cancer biomarkers, Int. J. Genomics., 2017, 10.1155/2017/6218353 Dragomir, 2018, Circular RNAs in cancer - lessons learned from microRNAs, Front. Oncol., 8, 179, 10.3389/fonc.2018.00179 Xu, 2018, A comprehensive review of circRNA: from purification and identification to disease marker potential, PeerJ, 6, e5503, 10.7717/peerj.5503 Salzman, 2012, Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types, PLoS One, 7, e30733, 10.1371/journal.pone.0030733 Memczak, 2013, Circular RNAs are a large class of animal RNAs with regulatory potency, Nature, 495, 333, 10.1038/nature11928 Jeck, 2013, Circular RNAs are abundant, conserved, and associated with ALU repeats, RNA, 19, 141, 10.1261/rna.035667.112 Westholm, 2014, Genome-wide analysis of drosophila circular RNAs reveals their structural and sequence properties and age-dependent neural accumulation, Cell Rep., 9, 1966, 10.1016/j.celrep.2014.10.062 Zhang, 2016, Diverse alternative back-splicing and alternative splicing landscape of circular RNAs, Genome Res., 26, 1277, 10.1101/gr.202895.115 Gao, 2015, CIRI: an efficient and unbiased algorithm for de novo circular RNA identification, Genome Biol., 16, 4, 10.1186/s13059-014-0571-3 Wang, 2010, MapSplice: accurate mapping of RNA-seq reads for splice junction discovery, Nucleic Acids Res., 38, e178, 10.1093/nar/gkq622 Eger, 2018, Circular RNA splicing, Adv. Exp. Med. Biol., 1087, 41, 10.1007/978-981-13-1426-1_4 Ashwal-Fluss, 2014, circRNA biogenesis competes with pre-mRNA splicing, Mol. Cell, 56, 55, 10.1016/j.molcel.2014.08.019 Starke, 2015, Exon circularization requires canonical splice signals, Cell Rep., 10, 103, 10.1016/j.celrep.2014.12.002 Liang, 2014, Short intronic repeat sequences facilitate circular RNA production, Genes Dev., 28, 2233, 10.1101/gad.251926.114 Ivanov, 2015, Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals, Cell Rep., 10, 170, 10.1016/j.celrep.2014.12.019 Conn, 2015, The RNA binding protein quaking regulates formation of circRNAs, Cell, 160, 1125, 10.1016/j.cell.2015.02.014 Li, 2017, Coordinated circRNA biogenesis and function with NF90/NF110 in viral infection, Mol. Cell, 67, 214, 10.1016/j.molcel.2017.05.023 Rybak-Wolf, 2015, Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed, Mol. Cell, 58, 870, 10.1016/j.molcel.2015.03.027 Enuka, 2016, Circular RNAs are long-lived and display only minimal early alterations in response to a growth factor, Nucleic Acids Res., 44, 1370, 10.1093/nar/gkv1367 Memczak, 2015, Identification and characterization of circular rnas as a new class of putative biomarkers in human blood, PLoS One, 10, e0141214, 10.1371/journal.pone.0141214 Salzman, 2013, Cell-type specific features of circular RNA expression, PLoS Genet., 9, e1003777, 10.1371/journal.pgen.1003777 Yang, 2018, Novel role of FBXW7 circular RNA in repressing glioma tumorigenesis, J. Natl. Cancer Inst., 110, 10.1093/jnci/djx166 Zhang, 2018, A peptide encoded by circular form of LINC-PINT suppresses oncogenic transcriptional elongation in glioblastoma, Nat. Commun., 9, 4475, 10.1038/s41467-018-06862-2 Li, 2015, Exon-intron circular RNAs regulate transcription in the nucleus, Nat. Struct. Mol. Biol., 22, 256, 10.1038/nsmb.2959 Hansen, 2013, Natural RNA circles function as efficient microRNA sponges, Nature, 495, 384, 10.1038/nature11993 Conn, 2017, A circRNA from SEPALLATA3 regulates splicing of its cognate mRNA through R-loop formation, Native Plants, 3, 17053, 10.1038/nplants.2017.53 Huang, 2018, A length-dependent evolutionarily conserved pathway controls nuclear export of circular RNAs, Genes Dev., 32, 639, 10.1101/gad.314856.118 Zhang, 2016, The biogenesis of nascent circular rnas, Cell Rep., 15, 611, 10.1016/j.celrep.2016.03.058 Vicens, 2014, Biogenesis of circular rnas, Cell, 159, 13, 10.1016/j.cell.2014.09.005 Kramer, 2015, Combinatorial control of Drosophila circular RNA expression by intronic repeats, hnRNPs, and SR proteins, Genes Dev., 29, 2168, 10.1101/gad.270421.115 Ebbesen, 2016, Circular RNAs: identification, biogenesis and function, Biochim. Biophys. Acta, 1859, 163, 10.1016/j.bbagrm.2015.07.007 Du, 2016, Foxo3 circular RNA retards cell cycle progression via forming ternary complexes with p21 and CDK2, Nucleic Acids Res., 44, 2846, 10.1093/nar/gkw027 Pamudurti, 2017, Translation of CircRNAs, Mol. Cell, 66, 9, 10.1016/j.molcel.2017.02.021 Legnini, 2017, Circ-ZNF609 is a circular RNA that can Be translated and functions in myogenesis, Mol. Cell, 66, 22, 10.1016/j.molcel.2017.02.017 Yang, 2017, Extensive translation of circular RNAs driven by N6-methyladenosine, Cell Res., 27, 626, 10.1038/cr.2017.31 Wang, 2015, Efficient backsplicing produces translatable circular mRNAs, RNA, 21, 172, 10.1261/rna.048272.114 Zhang, 2018, A novel protein encoded by the circular form of the SHPRH gene suppresses glioma tumorigenesis, Oncogene, 37, 1805, 10.1038/s41388-017-0019-9 Begum, 2018, Novel tumour suppressive protein encoded by circular RNA, circ-SHPRH, in glioblastomas, Oncogene, 37, 4055, 10.1038/s41388-018-0230-3 Wilusz, 2017, Circular RNAs: unexpected outputs of many protein-coding genes, RNA Biol., 14, 1007, 10.1080/15476286.2016.1227905 Tatomer, 2017, An unchartered journey for ribosomes: circumnavigating circular rnas to produce proteins, Mol. Cell, 66, 1, 10.1016/j.molcel.2017.03.011 Chen, 1995, Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs, Science, 268, 415, 10.1126/science.7536344 Guo, 2014, Expanded identification and characterization of mammalian circular RNAs, Genome Biol., 15, 409, 10.1186/s13059-014-0409-z Schneider, 2016, CircRNA-protein complexes: IMP3 protein component defines subfamily of circRNPs, Sci. Rep., 6, 31313, 10.1038/srep31313 I. Legnini, G. Di Timoteo, F. Rossi, M. Morl, F. Briganti, O. Sth, et al., Circ-ZNF609 Is a Circular RNA that Can Be, (n.d.). Zheng, 2019, A novel protein encoded by a circular RNA circPPP1R12A promotes tumor pathogenesis and metastasis of colon cancer via Hippo-YAP signaling, Mol. Cancer, 18, 47, 10.1186/s12943-019-1010-6 Liang, 2019, Translation of the circular RNA circβ-catenin promotes liver cancer cell growth through activation of the Wnt pathway, Genome Biol., 20, 84, 10.1186/s13059-019-1685-4 Ragan, 2019, Insights into the biogenesis and potential functions of exonic circular RNA, Sci. Rep., 9, 2048, 10.1038/s41598-018-37037-0 Floor, 2016, Tunable protein synthesis by transcript isoforms in human cells, Elife, 5, 10.7554/eLife.10921 Gross, 2003, Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E, Cell, 115, 739, 10.1016/S0092-8674(03)00975-9 Schütz, 2008, Crystal structure of the yeast eIF4A-eIF4G complex: an RNA-helicase controlled by protein-protein interactions, Proc. Natl. Acad. Sci. U.S.A., 105, 9564, 10.1073/pnas.0800418105 Marintchev, 2009, Topology and regulation of the human eIF4A/4G/4H helicase complex in translation initiation, Cell, 136, 447, 10.1016/j.cell.2009.01.014 Pause, 1994, Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5’-cap function, Nature, 371, 762, 10.1038/371762a0 Sonenberg, 2009, Regulation of translation initiation in eukaryotes: mechanisms and biological targets, Cell, 136, 731, 10.1016/j.cell.2009.01.042 Ryoo, 2017, Two distinct nodes of translational inhibition in the Integrated Stress Response, BMB Rep, 50, 539, 10.5483/BMBRep.2017.50.11.157 Holcik, 2005, Translational control in stress and apoptosis, Nat. Rev. Mol. Cell Biol., 6, 318, 10.1038/nrm1618 Sonenberg, 2007, New modes of translational control in development, behavior, and disease, Mol. Cell, 28, 721, 10.1016/j.molcel.2007.11.018 Meyer, 2019, m6A-mediated translation regulation, Biochim. Biophys. Acta Gene Regul. Mech., 1862, 301, 10.1016/j.bbagrm.2018.10.006 Godet, 2019, IRES trans-acting factors, key actors of the stress response, Int. J. Mol. Sci., 20, 10.3390/ijms20040924 Fernandez, 2002, Regulation of internal ribosomal entry site-mediated translation by phosphorylation of the translation initiation factor eIF2alpha, J. Biol. Chem., 277, 19198, 10.1074/jbc.M201052200 Jang, 1988, A segment of the 5’ nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation, J. Virol., 62, 2636, 10.1128/JVI.62.8.2636-2643.1988 Macejak, 1991, Internal initiation of translation mediated by the 5’ leader of a cellular mRNA, Nature, 353, 90, 10.1038/353090a0 Meyer, 2015, 5’ UTR m(6)A promotes cap-independent translation, Cell, 163, 999, 10.1016/j.cell.2015.10.012 Zhou, 2018, N6-Methyladenosine guides mRNA alternative translation during integrated stress response, Mol. Cell, 69, 636, 10.1016/j.molcel.2018.01.019 Biamonti, 2009, Cellular stress and RNA splicing, Trends Biochem. Sci., 34, 146, 10.1016/j.tibs.2008.11.004 Yaman, 2003, The zipper model of translational control: a small upstream ORF is the switch that controls structural remodeling of an mRNA leader, Cell, 113, 519, 10.1016/S0092-8674(03)00345-3 Coots, 2017, m6A Facilitates eIF4F-Independent mRNA Translation, Mol. Cell, 68, 504, 10.1016/j.molcel.2017.10.002 Liu, 2014, A METTL3-METTL14 complex mediates mammalian nuclear RNA N6-adenosine methylation, Nat. Chem. Biol., 10, 93, 10.1038/nchembio.1432 Ping, 2014, Mammalian WTAP is a regulatory subunit of the RNA N6-methyladenosine methyltransferase, Cell Res., 24, 177, 10.1038/cr.2014.3 Jia, 2011, N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO, Nat. Chem. Biol., 7, 885, 10.1038/nchembio.687 Zheng, 2013, ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility, Mol. Cell, 49, 18, 10.1016/j.molcel.2012.10.015 Wesselhoeft, 2018, Engineering circular RNA for potent and stable translation in eukaryotic cells, Nat. Commun., 9, 2629, 10.1038/s41467-018-05096-6 Yang, 2018, Constructing GFP-based reporter to study back splicing and translation of circular RNA, Methods Mol. Biol., 1724, 107, 10.1007/978-1-4939-7562-4_9 Meganck, 2018, Tissue-dependent expression and translation of circular RNAs with recombinant AAV vectors in vivo, Mol. Ther. Nucleic Acids, 13, 89, 10.1016/j.omtn.2018.08.008 Costello, 2019, Continuous translation of circularized mRNA improves recombinant protein titer, Metab. Eng., 52, 284, 10.1016/j.ymben.2019.01.002