3,749
Views
78
CrossRef citations to date
0
Altmetric
Reviews

Circular RNAs: Unexpected outputs of many protein-coding genes

Pages 1007-1017 | Received 28 Jun 2016, Accepted 19 Aug 2016, Published online: 26 Sep 2016

References

  • Crick FH. On protein synthesis. Symp Soc Exp Biol 1958; 12:138-63; PMID:13580867
  • Wilusz JE, Sunwoo H, Spector DL. Long noncoding RNAs: functional surprises from the RNA world. Genes Dev 2009; 23:1494-504; PMID:19571179; https://doi.org/10.1101/gad.1800909
  • Cech TR, Steitz JA. The noncoding RNA revolution-trashing old rules to forge new ones. Cell 2014; 157:77-94; PMID:24679528; https://doi.org/10.1016/j.cell.2014.03.008
  • Yang L, Froberg JE, Lee JT. Long noncoding RNAs: fresh perspectives into the RNA world. Trends Biochem Sci 2014; 39:35-43; PMID:24290031; https://doi.org/10.1016/j.tibs.2013.10.002
  • Kapranov P, Willingham AT, Gingeras TR. Genome-wide transcription and the implications for genomic organization. Nat Rev Genet 2007; 8:413-23; PMID:17486121; https://doi.org/10.1038/nrg2083
  • Jeck WR, Sharpless NE. Detecting and characterizing circular RNAs. Nature Biotechnol 2014; 32:453-61; PMID:24811520; https://doi.org/10.1038/nbt.2890
  • Chen LL. The biogenesis and emerging roles of circular RNAs. Nat Rev Mol Cell Biol 2016; 17:205-11; PMID:26908011; https://doi.org/10.1038/nrm.2015.32
  • Wilusz JE. Repetitive elements regulate circular RNA biogenesis. Mob Genet Elements 2015; 5:1-7; PMID:26442181; https://doi.org/10.1080/2159256X.2015.1045682
  • Barrett SP, Salzman J. Circular RNAs: analysis, expression and potential functions. Development 2016; 143:1838-47; PMID:27246710; https://doi.org/10.1242/dev.128074
  • Ebbesen KK, Kjems J, Hansen TB. Circular RNAs: Identification, biogenesis and function. Biochim Biophys Acta 2016; 1859:163-8; PMID:26171810; https://doi.org/10.1016/j.bbagrm.2015.07.007
  • Lasda E, Parker R. Circular RNAs: diversity of form and function. RNA 2014; 20:1829-42; PMID:25404635; https://doi.org/10.1261/rna.047126.114
  • Chen I, Chen CY, Chuang TJ. Biogenesis, identification, and function of exonic circular RNAs. Wiley Interdiscip Rev RNA 2015; 6:563-79; PMID:26230526; https://doi.org/10.1002/wrna.1294
  • 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; PMID:22319583; https://doi.org/10.1371/journal.pone.0030733
  • Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE, Liu J, Marzluff WF, Sharpless NE. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 2013; 19:141-57; PMID:23249747; https://doi.org/10.1261/rna.035667.112
  • Fu XD, Ares M, Jr. Context-dependent control of alternative splicing by RNA-binding proteins. Nat Rev Genet 2014; 15:689-701; PMID:25112293; https://doi.org/10.1038/nrg3778
  • Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. Alternative isoform regulation in human tissue transcriptomes. Nature 2008; 456:470-6; PMID:18978772; https://doi.org/10.1038/nature07509
  • Smith CW, Valcarcel J. Alternative pre-mRNA splicing: the logic of combinatorial control. Trends Biochem Sci 2000; 25:381-8; PMID:10916158; https://doi.org/10.1016/S0968-0004(00)01604-2
  • Carrillo Oesterreich F, Herzel L, Straube K, Hujer K, Howard J, Neugebauer KM. Splicing of Nascent RNA Coincides with Intron Exit from RNA Polymerase II. Cell 2016; 165:372-81; PMID:27020755; https://doi.org/10.1016/j.cell.2016.02.045
  • Bentley DL. Coupling mRNA processing with transcription in time and space. Nat Rev Genet 2014; 15:163-75; PMID:24514444; https://doi.org/10.1038/nrg3662
  • Pandya-Jones A, Black DL. Co-transcriptional splicing of constitutive and alternative exons. RNA 2009; 15:1896-908; PMID:19656867; https://doi.org/10.1261/rna.1714509
  • Boutz PL, Bhutkar A, Sharp PA. Detained introns are a novel, widespread class of post-transcriptionally spliced introns. Genes Dev 2015; 29:63-80; PMID:25561496; https://doi.org/10.1101/gad.247361.114
  • Vargas DY, Shah K, Batish M, Levandoski M, Sinha S, Marras SA, Schedl P, Tyagi S. Single-molecule imaging of transcriptionally coupled and uncoupled splicing. Cell 2011; 147:1054-65; PMID:22118462; https://doi.org/10.1016/j.cell.2011.10.024
  • Braunschweig U, Gueroussov S, Plocik AM, Graveley BR, Blencowe BJ. Dynamic integration of splicing within gene regulatory pathways. Cell 2013; 152:1252-69; PMID:23498935; https://doi.org/10.1016/j.cell.2013.02.034
  • Braunschweig U, Barbosa-Morais NL, Pan Q, Nachman EN, Alipanahi B, Gonatopoulos-Pournatzis T, Frey B, Irimia M, Blencowe BJ. Widespread intron retention in mammals functionally tunes transcriptomes. Genome Res 2014; 24:1774-86; PMID:25258385; https://doi.org/10.1101/gr.177790.114
  • Ashwal-Fluss R, Meyer M, Pamudurti NR, Ivanov A, Bartok O, Hanan M, Evantal N, Memczak S, Rajewsky N, Kadener S. circRNA biogenesis competes with pre-mRNA splicing. Mol Cell 2014; 56:55-66; PMID:25242144; https://doi.org/10.1016/j.molcel.2014.08.019
  • Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J. Natural RNA circles function as efficient microRNA sponges. Nature 2013; 495:384-8; PMID:23446346; https://doi.org/10.1038/nature11993
  • Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 2013; 495:333-8; PMID:23446348; https://doi.org/10.1038/nature11928
  • Wilusz JE, Sharp PA. Molecular biology. A circuitous route to noncoding RNA. Science 2013; 340:440-1; PMID:23620042; https://doi.org/10.1126/science.1238522
  • Westholm JO, Miura P, Olson S, Shenker S, Joseph B, Sanfilippo P, Celniker SE, Graveley BR, Lai EC. Genome-wide analysis of drosophila circular RNAs reveals their structural and sequence properties and age-dependent neural accumulation. Cell Rep 2014; 9:1966-80; PMID:25544350; https://doi.org/10.1016/j.celrep.2014.10.062
  • Enuka Y, Lauriola M, Feldman ME, Sas-Chen A, Ulitsky I, Yarden Y. Circular RNAs are long-lived and display only minimal early alterations in response to a growth factor. Nucleic Acids Res 2016; 44:1370-83; PMID:26657629; https://doi.org/10.1093/nar/gkv1367
  • Guo JU, Agarwal V, Guo H, Bartel DP. Expanded identification and characterization of mammalian circular RNAs. Genome Biol 2014; 15:409; PMID:25070500; https://doi.org/10.1186/s13059-014-0409-z
  • You X, Vlatkovic I, Babic A, Will T, Epstein I, Tushev G, Akbalik G, Wang M, Glock C, Quedenau C, et al. Neural circular RNAs are derived from synaptic genes and regulated by development and plasticity. Nature Neurosci 2015; 18:603-10; PMID:25714049; https://doi.org/10.1038/nn.3975
  • Rybak-Wolf A, Stottmeister C, Glazar P, Jens M, Pino N, Giusti S, Hanan M, Behm M, Bartok O, Ashwal-Fluss R, et al. Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed. Mol Cell 2015; 58:870-85; PMID:25921068; https://doi.org/10.1016/j.molcel.2015.03.027
  • Chen CY, Sarnow P. Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs. Science 1995; 268:415-7; PMID:7536344; https://doi.org/10.1126/science.7536344
  • Wang Y, Wang Z. Efficient backsplicing produces translatable circular mRNAs. RNA 2015; 21:172-9; PMID:25449546; https://doi.org/10.1261/rna.048272.114
  • Abe N, Matsumoto K, Nishihara M, Nakano Y, Shibata A, Maruyama H, Shuto S, Matsuda A, Yoshida M, Ito Y, et al. Rolling Circle Translation of Circular RNA in Living Human Cells. Sci Rep 2015; 5:16435; PMID:26553571; https://doi.org/10.1038/srep16435
  • Kramer MC, Liang D, Tatomer DC, Gold B, March ZM, Cherry S, Wilusz JE. Combinatorial control of Drosophila circular RNA expression by intronic repeats, hnRNPs, and SR proteins. Genes Dev 2015; 29:2168-82; PMID:26450910; https://doi.org/10.1101/gad.270421.115
  • Salzman J, Chen RE, Olsen MN, Wang PL, Brown PO. Cell-type specific features of circular RNA expression. PLoS Genet 2013; 9:e1003777; PMID:24039610; https://doi.org/10.1371/journal.pgen.1003777
  • Zhang Y, Xue W, Li X, Zhang J, Chen S, Zhang JL, Yang L, Chen LL. The biogenesis of nascent circular RNAs. Cell Rep 2016; 15:611-24; PMID:27068474; https://doi.org/10.1016/j.celrep.2016.03.058
  • Zhang XO, Wang HB, Zhang Y, Lu X, Chen LL, Yang L. Complementary sequence-mediated exon circularization. Cell 2014; 159:134-47; PMID:25242744; https://doi.org/10.1016/j.cell.2014.09.001
  • Barrett SP, Wang PL, Salzman J. Circular RNA biogenesis can proceed through an exon-containing lariat precursor. Elife 2015; 4:e07540; PMID:26057830; https://doi.org/10.7554/eLife.07540
  • Zhang Y, Zhang XO, Chen T, Xiang JF, Yin QF, Xing YH, Zhu S, Yang L, Chen LL. Circular intronic long noncoding RNAs. Mol Cell 2013; 51:792-806; PMID:24035497; https://doi.org/10.1016/j.molcel.2013.08.017
  • Sanger HL, Klotz G, Riesner D, Gross HJ, Kleinschmidt AK. Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proc Natl Acad Sci U S A 1976; 73:3852-6; PMID:1069269; https://doi.org/10.1073/pnas.73.11.3852
  • Kos A, Dijkema R, Arnberg AC, van der Meide PH, Schellekens H. The hepatitis delta (delta) virus possesses a circular RNA. Nature 1986; 323:558-60; PMID:2429192; https://doi.org/10.1038/323558a0
  • Nigro JM, Cho KR, Fearon ER, Kern SE, Ruppert JM, Oliner JD, Kinzler KW, Vogelstein B. Scrambled exons. Cell 1991; 64:607-13; PMID:1991322; https://doi.org/10.1016/0092-8674(91)90244-S
  • Cocquerelle C, Daubersies P, Majerus MA, Kerckaert JP, Bailleul B. Splicing with inverted order of exons occurs proximal to large introns. EMBO J 1992; 11:1095-8; PMID:1339341
  • Cocquerelle C, Mascrez B, Hetuin D, Bailleul B. Mis-splicing yields circular RNA molecules. FASEB J 1993; 7:155-60; PMID:7678559
  • Capel B, Swain A, Nicolis S, Hacker A, Walter M, Koopman P, Goodfellow P, Lovell-Badge R. Circular transcripts of the testis-determining gene Sry in adult mouse testis. Cell 1993; 73:1019-30; PMID:7684656; https://doi.org/10.1016/0092-8674(93)90279-Y
  • Zaphiropoulos PG. Circular RNAs from transcripts of the rat cytochrome P450 2C24 gene: correlation with exon skipping. Proc Natl Acad Sci U S A 1996; 93:6536-41; PMID:8692851; https://doi.org/10.1073/pnas.93.13.6536
  • Zaphiropoulos PG. Exon skipping and circular RNA formation in transcripts of the human cytochrome P-450 2C18 gene in epidermis and of the rat androgen binding protein gene in testis. Mol Cell Biol 1997; 17:2985-93; PMID:9154796; https://doi.org/10.1128/MCB.17.6.2985
  • Chao CW, Chan DC, Kuo A, Leder P. The mouse formin (Fmn) gene: abundant circular RNA transcripts and gene-targeted deletion analysis. Mol Med 1998; 4:614-28; PMID:9848078
  • Surono A, Takeshima Y, Wibawa T, Ikezawa M, Nonaka I, Matsuo M. Circular dystrophin RNAs consisting of exons that were skipped by alternative splicing. Hum Mol Genet 1999; 8:493-500; PMID:9949208; https://doi.org/10.1093/hmg/8.3.493
  • Li XF, Lytton J. A circularized sodium-calcium exchanger exon 2 transcript. J Biol Chem 1999; 274:8153-60; PMID:10075718; https://doi.org/10.1074/jbc.274.12.8153
  • Houseley JM, Garcia-Casado Z, Pascual M, Paricio N, O'Dell KM, Monckton DG, Artero RD. Noncanonical RNAs from transcripts of the Drosophila muscleblind gene. J Hered 2006; 97:253-60; PMID:16714427; https://doi.org/10.1093/jhered/esj037
  • Burd CE, Jeck WR, Liu Y, Sanoff HK, Wang Z, Sharpless NE. Expression of linear and novel circular forms of an INK4/ARF-associated non-coding RNA correlates with atherosclerosis risk. PLoS Genet 2010; 6:e1001233
  • Hansen TB, Wiklund ED, Bramsen JB, Villadsen SB, Statham AL, Clark SJ, Kjems J. miRNA-dependent gene silencing involving Ago2-mediated cleavage of a circular antisense RNA. EMBO J 2011; 30:4414-22; PMID:21964070; https://doi.org/10.1038/emboj.2011.359
  • Glazar P, Papavasileiou P, Rajewsky N. circBase: a database for circular RNAs. RNA 2014; 20:1666-70; PMID:25234927; https://doi.org/10.1261/rna.043687.113
  • Hansen TB, Veno MT, Damgaard CK, Kjems J. Comparison of circular RNA prediction tools. Nucleic Acids Res 2016; 44:e58; PMID:26657634; https://doi.org/10.1093/nar/gkv1458
  • Zhang XO, Dong R, Zhang Y, Zhang JL, Luo Z, Zhang J, Chen LL, Yang L. Diverse alternative back-splicing and alternative splicing landscape of circular RNAs. Genome Res 2016; 26:1277-87; PMID: 27365365; https://doi.org/10.1101/gr.202895.115
  • Gao Y, Wang J, Zheng Y, Zhang J, Chen S, Zhao F. Comprehensive identification of internal structure and alternative splicing events in circular RNAs. Nature Commun 2016; 7:12060; PMID: 27350239; https://doi.org/10.1038/ncomms12060
  • Li 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; 22:256-64; PMID:25664725; https://doi.org/10.1038/nsmb.2959
  • Veno MT, Hansen TB, Veno ST, Clausen BH, Grebing M, Finsen B, Holm IE, Kjems J. Spatio-temporal regulation of circular RNA expression during porcine embryonic brain development. Genome Biol 2015; 16:245; PMID:26541409; https://doi.org/10.1186/s13059-015-0801-3
  • Garneau NL, Wilusz J, Wilusz CJ. The highways and byways of mRNA decay. Nat Rev Mol Cell Biol 2007; 8:113-26; PMID:17245413; https://doi.org/10.1038/nrm2104
  • Neff AT, Lee JY, Wilusz J, Tian B, Wilusz CJ. Global analysis reveals multiple pathways for unique regulation of mRNA decay in induced pluripotent stem cells. Genome Res 2012; 22:1457-67; PMID:22534399; https://doi.org/10.1101/gr.134312.111
  • Liang D, Wilusz JE. Short intronic repeat sequences facilitate circular RNA production. Genes Dev 2014; 28:2233-47; PMID:25281217; https://doi.org/10.1101/gad.251926.114
  • Dubin RA, Kazmi MA, Ostrer H. Inverted repeats are necessary for circularization of the mouse testis Sry transcript. Gene 1995; 167:245-8; PMID:8566785; https://doi.org/10.1016/0378-1119(95)00639-7
  • Pasman Z, Been MD, Garcia-Blanco MA. Exon circularization in mammalian nuclear extracts. RNA 1996; 2:603-10; PMID:8718689
  • Ivanov A, Memczak S, Wyler E, Torti F, Porath HT, Orejuela MR, Piechotta M, Levanon EY, Landthaler M, Dieterich C, et al. Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals. Cell Rep 2015; 10:170-7; PMID:25558066; https://doi.org/10.1016/j.celrep.2014.12.019
  • Starke S, Jost I, Rossbach O, Schneider T, Schreiner S, Hung LH, Bindereif A. Exon circularization requires canonical splice signals. Cell Rep 2015; 10:103-11; PMID:25543144; https://doi.org/10.1016/j.celrep.2014.12.002
  • Zheng Q, Bao C, Guo W, Li S, Chen J, Chen B, Luo Y, Lyu D, Li Y, Shi G, et al. Circular RNA profiling reveals an abundant circHIPK3 that regulates cell growth by sponging multiple miRNAs. Nature Commun 2016; 7:11215; PMID:27050392; https://doi.org/10.1038/ncomms11215
  • Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, et al. Initial sequencing and analysis of the human genome. Nature 2001; 409:860-921; PMID:11237011; https://doi.org/10.1038/35057062
  • de Koning AP, Gu W, Castoe TA, Batzer MA, Pollock DD. Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet 2011; 7:e1002384; PMID:22144907; https://doi.org/10.1371/journal.pgen.1002384
  • Daniel C, Behm M, Ohman M. The role of Alu elements in the cis-regulation of RNA processing. Cell Mol Life Sci 2015; 72:4063-76; PMID:26223268; https://doi.org/10.1007/s00018-015-1990-3
  • Elbarbary RA, Lucas BA, Maquat LE. Retrotransposons as regulators of gene expression. Science 2016; 351:aac7247; PMID:26912865; https://doi.org/10.1126/science.aac7247
  • Shedlock AM, Okada N. SINE insertions: powerful tools for molecular systematics. BioEssays 2000; 22:148-60; PMID:10655034; https://doi.org/10.1002/(SICI)1521-1878(200002)22:2%3c148::AID-BIES6%3e3.0.CO;2-Z
  • Bunting SF, Nussenzweig A. End-joining, translocations and cancer. Nat Rev Cancer 2013; 13:443-54; PMID:23760025; https://doi.org/10.1038/nrc3537
  • Mitelman F, Johansson B, Mertens F. The impact of translocations and gene fusions on cancer causation. Nat Rev Cancer 2007; 7:233-45; PMID:17361217; https://doi.org/10.1038/nrc2091
  • Guarnerio J, Bezzi M, Jeong JC, Paffenholz SV, Berry K, Naldini MM, Lo-Coco F, Tay Y, Beck AH, Pandolfi PP. Oncogenic Role of Fusion-circRNAs Derived from Cancer-Associated Chromosomal Translocations. Cell 2016; 165:289-302; PMID:27040497; https://doi.org/10.1016/j.cell.2016.03.020
  • Song X, Zhang N, Han P, Moon BS, Lai RK, Wang K, Lu W. Circular RNA profile in gliomas revealed by identification tool UROBORUS. Nucleic Acids Res 2016; 44:e87; PMID:26873924; https://doi.org/10.1093/nar/gkw075
  • Bachmayr-Heyda A, Reiner AT, Auer K, Sukhbaatar N, Aust S, Bachleitner-Hofmann T, Mesteri I, Grunt TW, Zeillinger R, Pils D. 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; PMID:25624062; https://doi.org/10.1038/srep08057
  • Ahmed I, Karedath T, Andrews SS, Al-Azwani IK, Ali Mohamoud Y, Querleu D, Rafii A, Malek JA. Altered expression pattern of circular RNAs in primary and metastatic sites of epithelial ovarian carcinoma. Oncotarget 2016; PMID:27119352; https://doi.org/10.18632/oncotarget.8917
  • Conn SJ, Pillman KA, Toubia J, Conn VM, Salmanidis M, Phillips CA, Roslan S, Schreiber AW, Gregory PA, Goodall GJ. The RNA Binding Protein Quaking Regulates Formation of circRNAs. Cell 2015; 160:1125-34; PMID:25768908; https://doi.org/10.1016/j.cell.2015.02.014
  • Dang Y, Yan L, Hu B, Fan X, Ren Y, Li R, Lian Y, Yan J, Li Q, Zhang Y, et al. Tracing the expression of circular RNAs in human pre-implantation embryos. Genome Biol 2016; 17:130; PMID:27315811; https://doi.org/10.1186/s13059-016-0991-3
  • Szabo L, Morey R, Palpant NJ, Wang PL, Afari N, Jiang C, Parast MM, Murry CE, Laurent LC, Salzman J. Statistically based splicing detection reveals neural enrichment and tissue-specific induction of circular RNA during human fetal development. Genome Biol 2015; 16:126; PMID:26076956; https://doi.org/10.1186/s13059-015-0690-5
  • Lareau LF, Brooks AN, Soergel DA, Meng Q, Brenner SE. The coupling of alternative splicing and nonsense-mediated mRNA decay. Adv Exp Med Biol 2007; 623:190-211; PMID:18380348; https://doi.org/10.1007/978-0-387-77374-2_12
  • Barash Y, Calarco JA, Gao W, Pan Q, Wang X, Shai O, Blencowe BJ, Frey BJ. Deciphering the splicing code. Nature 2010; 465:53-9; PMID:20445623; https://doi.org/10.1038/nature09000
  • Wang PL, Bao Y, Yee MC, Barrett SP, Hogan GJ, Olsen MN, Dinneny JR, Brown PO, Salzman J. Circular RNA is expressed across the eukaryotic tree of life. PLoS One 2014; 9:e90859; PMID:24609083; https://doi.org/10.1371/journal.pone.0090859
  • Bitton DA, Atkinson SR, Rallis C, Smith GC, Ellis DA, Chen YY, Malecki M, Codlin S, Lemay JF, Cotobal C, et al. Widespread exon skipping triggers degradation by nuclear RNA surveillance in fission yeast. Genome Res 2015; 25:884-96; PMID:25883323; https://doi.org/10.1101/gr.185371.114
  • Awan AR, Manfredo A, Pleiss JA. Lariat sequencing in a unicellular yeast identifies regulated alternative splicing of exons that are evolutionarily conserved with humans. Proc Natl Acad Sci U S A 2013; 110:12762-7; PMID:23861491; https://doi.org/10.1073/pnas.1218353110
  • Kelly S, Greenman C, Cook PR, Papantonis A. Exon skipping is correlated with exon circularization. J Mol Biol 2015; 427:2414-7; PMID:25728652; https://doi.org/10.1016/j.jmb.2015.02.018
  • Gardner EJ, Nizami ZF, Talbot CC, Jr., Gall JG. Stable intronic sequence RNA (sisRNA), a new class of noncoding RNA from the oocyte nucleus of Xenopus tropicalis. Genes Dev 2012; 26:2550-9; PMID:23154985; https://doi.org/10.1101/gad.202184.112
  • Ford E, Ares M, Jr. Synthesis of circular RNA in bacteria and yeast using RNA cyclase ribozymes derived from a group I intron of phage T4. Proc Natl Acad Sci U S A 1994; 91:3117-21; PMID:7512723; https://doi.org/10.1073/pnas.91.8.3117
  • Lu Z, Filonov GS, Noto JJ, Schmidt CA, Hatkevich TL, Wen Y, Jaffrey SR, Matera AG. Metazoan tRNA introns generate stable circular RNAs in vivo. RNA 2015; 21:1554-65; PMID:26194134; https://doi.org/10.1261/rna.052944.115
  • Schmidt CA, Noto JJ, Filonov GS, Matera AG. A Method for Expressing and Imaging Abundant, Stable, Circular RNAs In Vivo Using tRNA Splicing. Methods Enzymol 2016; 572:215-36; PMID:27241756; https://doi.org/10.1016/bs.mie.2016.02.018
  • Petkovic S, Muller S. RNA circularization strategies in vivo and in vitro. Nucleic Acids Res 2015; 43:2454-65; PMID:25662225; https://doi.org/10.1093/nar/gkv045
  • Carmody SR, Wente SR. mRNA nuclear export at a glance. J Cell Sci 2009; 122:1933-7; PMID:19494120; https://doi.org/10.1242/jcs.041236
  • Schoenberg DR. Mechanisms of endonuclease-mediated mRNA decay. Wiley Interdiscip Rev RNA 2011; 2:582-600; PMID:21957046; https://doi.org/10.1002/wrna.78
  • Lasda E, Parker R. Circular RNAs Co-precipitate with extracellular vesicles: A possible mechanism for circRNA clearance. PLoS One 2016; 11:e0148407; PMID:26848835; https://doi.org/10.1371/journal.pone.0148407
  • Li Y, Zheng Q, Bao C, Li S, Guo W, Zhao J, Chen D, Gu J, He X, Huang S. Circular RNA is enriched and stable in exosomes: a promising biomarker for cancer diagnosis. Cell Res 2015; 25:981-4; PMID:26138677; https://doi.org/10.1038/cr.2015.82
  • 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; PMID:26485708; https://doi.org/10.1371/journal.pone.0141214
  • Wilusz JE. Long noncoding RNAs: Re-writing dogmas of RNA processing and stability. Biochim Biophys Acta 2016; 1859:128-38; PMID:26073320; https://doi.org/10.1016/j.bbagrm.2015.06.003
  • Zhang Y, Yang L, Chen LL. Life without A tail: new formats of long noncoding RNAs. Int J Biochem Cell Biol 2014; 54:338-49; PMID:24513732; https://doi.org/10.1016/j.biocel.2013.10.009
  • Peart N, Sataluri A, Baillat D, Wagner EJ. Non-mRNA 3′ end formation: how the other half lives. Wiley Interdiscip Rev RNA 2013; 4:491-506; PMID:23754627; https://doi.org/10.1002/wrna.1174
  • Pickrell JK, Pai AA, Gilad Y, Pritchard JK. Noisy splicing drives mRNA isoform diversity in human cells. PLoS Genet 2010; 6:e1001236; PMID:21151575; https://doi.org/10.1371/journal.pgen.1001236
  • Lu T, Cui L, Zhou Y, Zhu C, Fan D, Gong H, Zhao Q, Zhou C, Zhao Y, Lu D, et al. Transcriptome-wide investigation of circular RNAs in rice. RNA 2015; 21:2076-87; PMID:26464523; https://doi.org/10.1261/rna.052282.115

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.