Guidance of circular RNAs to proteins’ behavior as binding partners

Nigro JM, Cho KR, Fearon ER, Kern SE, Ruppert JM, Oliner JD, Kinzler KW, Vogelstein B (1991) Scrambled exons. Cell 64:607–613 Cocquerelle C, Daubersies P, Majerus MA, Kerckaert JP, Bailleul B (1992) Splicing with inverted order of exons occurs proximal to large introns. EMBO J 11:1095–1098 Cocquerelle C, Mascrez B, Hetuin D, Bailleul B (1993) Mis-splicing yields circular RNA molecules. FASEB J 7:155–160 Capel B, Swain A, Nicolis S, Hacker A, Walter M, Koopman P, Goodfellow P, Lovell-Badge R (1993) Circular transcripts of the testis-determining gene Sry in adult mouse testis. Cell 73:1019–1030 Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, Loewer A, Ziebold U, Landthaler M, Kocks C, le Noble F, Rajewsky N (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495:333–338 Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495:384–388 Hansen TB, Wiklund ED, Bramsen JB, Villadsen SB, Statham AL, Clark SJ, Kjems J (2011) miRNA-dependent gene silencing involving Ago2-mediated cleavage of a circular antisense RNA. EMBO J 30:4414–4422 Pasman Z, Been MD, Garcia-Blanco MA (1996) Exon circularization in mammalian nuclear extracts. RNA 2:603–610 Zhang Y, Zhang XO, Chen T, Xiang JF, Yin QF, Xing YH, Zhu S, Yang L, Chen LL (2013) Circular intronic long noncoding RNAs. Mol Cell 51:792–806 Li Z, Huang C, Bao C, Chen L, Lin M, Wang X, Zhong G, Yu B, Hu W, Dai L, Zhu P, Chang Z, Wu Q, Zhao Y, Jia Y, Xu P, Liu H, Shan G (2015) Exon–intron circular RNAs regulate transcription in the nucleus. Nat Struct Mol Biol 22:256–264 Guarnerio J, Bezzi M, Jeong JC, Paffenholz SV, Berry K, Naldini MM, Lo-Coco F, Tay Y, Beck AH, Pandolfi PP (2016) Oncogenic role of fusion-circRNAs derived from cancer-associated chromosomal translocations. Cell 165:289–302 Zhang Y, Xue W, Li X, Zhang J, Chen S, Zhang JL, Yang L, Chen LL (2016) The biogenesis of nascent circular RNAs. Cell Rep 15:611–624 Wilusz JE (2018) A 360 degrees view of circular RNAs: from biogenesis to functions. Wiley Interdiscip Rev RNA 9:e1478 Legnini I, Di Timoteo G, Rossi F, Morlando M, Briganti F, Sthandier O, Fatica A, Santini T, Andronache A, Wade M, Laneve P, Rajewsky N, Bozzoni I (2017) Circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis. Mol Cell 66(22–37):e29 Piwecka M, Glazar P, Hernandez-Miranda LR, Memczak S, Wolf SA, Rybak-Wolf A, Filipchyk A, Klironomos F, Cerda Jara CA, Fenske P, Trimbuch T, Zywitza V, Plass M, Schreyer L, Ayoub S, Kocks C, Kuhn R, Rosenmund C, Birchmeier C, Rajewsky N (2017) Loss of a mammalian circular RNA locus causes miRNA deregulation and affects brain function. Science 357:eaam8526 Zhang X, Yan Y, Lin W, Li A, Zhang H, Lei X, Dai Z, Li X, Li H, Chen W, Chen F, Ma J, Xie Q (2019) Circular RNA Vav3 sponges gga-miR-375 to promote epithelial–mesenchymal transition. RNA Biol 16:118–132 Li M, Ding W, Tariq MA, Chang W, Zhang X, Xu W, Hou L, Wang Y, Wang J (2018) A circular transcript of ncx1 gene mediates ischemic myocardial injury by targeting miR-133a-3p. Theranostics 8:5855–5869 Hall IF, Climent M, Quintavalle M, Farina FM, Schorn T, Zani S, Carullo P, Kunderfranco P, Civilini E, Condorelli G, Elia L (2019) Circ_Lrp6, a circular RNA enriched in vascular smooth muscle cells, acts as a sponge regulating miRNA-145 function. Circ Res 124:498–510 Qiu M, Xia W, Chen R, Wang S, Xu Y, Ma Z, Xu W, Zhang E, Wang J, Fang T, Hu J, Dong G, Yin R, Wang J, Xu L (2018) The circular RNA circPRKCI promotes tumor growth in lung adenocarcinoma. Can Res 78:2839–2851 Li Z, Yanfang W, Li J, Jiang P, Peng T, Chen K, Zhao X, Zhang Y, Zhen P, Zhu J, Li X (2018) Tumor-released exosomal circular RNA PDE8A promotes invasive growth via the miR-338/MACC1/MET pathway in pancreatic cancer. Cancer Lett 432:237–250 Vo JN, Cieslik M, Zhang Y, Shukla S, Xiao L, Zhang Y, Wu YM, Dhanasekaran SM, Engelke CG, Cao X, Robinson DR, Nesvizhskii AI, Chinnaiyan AM (2019) The landscape of circular RNA in cancer. Cell 176(869–881):e813 Chen S, Huang V, Xu X, Livingstone J, Soares F, Jeon J, Zeng Y, Hua JT, Petricca J, Guo H, Wang M, Yousif F, Zhang Y, Donmez N, Ahmed M, Volik S, Lapuk A, Chua MLK, Heisler LE, Foucal A, Fox NS, Fraser M, Bhandari V, Shiah YJ, Guan J, Li J, Orain M, Picard V, Hovington H, Bergeron A, Lacombe L, Fradet Y, Tetu B, Liu S, Feng F, Wu X, Shao YW, Komor MA, Sahinalp C, Collins C, Hoogstrate Y, de Jong M, Fijneman RJA, Fei T, Jenster G, van der Kwast T, Bristow RG, Boutros PC, He HH (2019) Widespread and functional RNA circularization in localized prostate cancer. Cell 176(831–843):e822 Conn SJ, Pillman KA, Toubia J, Conn VM, Salmanidis M, Phillips CA, Roslan S, Schreiber AW, Gregory PA, Goodall GJ (2015) The RNA binding protein quaking regulates formation of circRNAs. Cell 160:1125–1134 Schneider T, Hung LH, Schreiner S, Starke S, Eckhof H, Rossbach O, Reich S, Medenbach J, Bindereif A (2016) CircRNA–protein complexes: iMP3 protein component defines subfamily of circRNPs. Sci Rep 6:31313 Zhang J, Zhang X, Li C, Yue L, Ding N, Riordan T, Yang L, Li Y, Jen C, Lin S, Zhou D, Chen F (2019) Circular RNA profiling provides insights into their subcellular distribution and molecular characteristics in HepG2 cells. RNA Biol 16:220–232 Yang Y, Fan X, Mao M, Song X, Wu P, Zhang Y, Jin Y, Yang Y, Chen LL, Wang Y, Wong CC, Xiao X, Wang Z (2017) Extensive translation of circular RNAs driven by N(6)-methyladenosine. Cell Res 27:626–641 Pamudurti NR, Bartok O, Jens M, Ashwal-Fluss R, Stottmeister C, Ruhe L, Hanan M, Wyler E, Perez-Hernandez D, Ramberger E, Shenzis S, Samson M, Dittmar G, Landthaler M, Chekulaeva M, Rajewsky N, Kadener S (2017) Translation of CircRNAs. Mol Cell 66(9–21):e27 Wesselhoeft RA, Kowalski PS, Parker-Hale FC, Huang Y, Bisaria N, Anderson DG (2019) RNA circularization diminishes immunogenicity and can extend translation duration in vivo. Mol Cell 74:508–520 Zhao J, Lee EE, Kim J, Yang R, Chamseddin B, Ni C, Gusho E, Xie Y, Chiang CM, Buszczak M, Zhan X, Laimins L, Wang RC (2019) Transforming activity of an oncoprotein-encoding circular RNA from human papillomavirus. Nat Commun 10:2300 van Heesch S, Witte F, Schneider-Lunitz V, Schulz JF, Adami E, Faber AB, Kirchner M, Maatz H, Blachut S, Sandmann CL, Kanda M, Worth CL, Schafer S, Calviello L, Merriott R, Patone G, Hummel O, Wyler E, Obermayer B, Mucke MB, Lindberg EL, Trnka F, Memczak S, Schilling M, Felkin LE, Barton PJR, Quaife NM, Vanezis K, Diecke S, Mukai M, Mah N, Oh SJ, Kurtz A, Schramm C, Schwinge D, Sebode M, Harakalova M, Asselbergs FW, Vink A, de Weger RA, Viswanathan S, Widjaja AA, Gartner-Rommel A, Milting H, Dos Remedios C, Knosalla C, Mertins P, Landthaler M, Vingron M, Linke WA, Seidman JG, Seidman CE, Rajewsky N, Ohler U, Cook SA, Hubner N (2019) The translational landscape of the human heart. Cell 178:242–260 Hutvagner G, Simard MJ (2008) Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol 9:22–32 Yu CY, Li TC, Wu YY, Yeh CH, Chiang W, Chuang CY, Kuo HC (2017) The circular RNA circBIRC6 participates in the molecular circuitry controlling human pluripotency. Nat Commun 8:1149 Yang R, Xing L, Zheng X, Sun Y, Wang X, Chen J (2019) The circRNA circAGFG1 acts as a sponge of miR-195-5p to promote triple-negative breast cancer progression through regulating CCNE1 expression. Mol Cancer 18:4 Kwek KY, Murphy S, Furger A, Thomas B, O’Gorman W, Kimura H, Proudfoot NJ, Akoulitchev A (2002) U1 snRNA associates with TFIIH and regulates transcriptional initiation. Nat Struct Biol 9:800–805 Damgaard CK, Kahns S, Lykke-Andersen S, Nielsen AL, Jensen TH, Kjems J (2008) A 5′ splice site enhances the recruitment of basal transcription initiation factors in vivo. Mol Cell 29:271–278 Conn VM, Hugouvieux V, Nayak A, Conos SA, Capovilla G, Cildir G, Jourdain A, Tergaonkar V, Schmid M, Zubieta C, Conn SJ (2017) A circRNA from SEPALLATA3 regulates splicing of its cognate mRNA through R-loop formation. Nat Plants 3:17053 Zhu P, Zhu X, Wu J, He L, Lu T, Wang Y, Liu B, Ye B, Sun L, Fan D, Wang J, Yang L, Qin X, Du Y, Li C, He L, Ren W, Wu X, Tian Y, Fan Z (2019) IL-13 secreted by ILC2 s promotes the self-renewal of intestinal stem cells through circular RNA circPan3. Nat Immunol 20:183–194 Du WW, Zhang C, Yang W, Yong T, Awan FM, Yang BB (2017) Identifying and characterizing circRNA–protein interaction. Theranostics 7:4183–4191 Yang Q, Du WW, Wu N, Yang W, Awan FM, Fang L, Ma J, Li X, Zeng Y, Yang Z, Dong J, Khorshidi A, Yang BB (2017) A circular RNA promotes tumorigenesis by inducing c-myc nuclear translocation. Cell Death Differ 24:1609–1620 Yang ZG, Awan FM, Du WW, Zeng Y, Lyu J, Wu Gupta S, Yang W, Yang BB (2017) The circular RNA interacts with STAT3, increasing its nuclear translocation and wound repair by modulating Dnmt3a and miR-17 function. Mol Ther 25:2062–2074 Zeng Y, Du WW, Wu Y, Yang Z, Awan FM, Li X, Yang W, Zhang C, Yang Q, Yee A, Chen Y, Yang F, Sun H, Huang R, Yee AJ, Li RK, Wu Z, Backx PH, Yang BB (2017) A circular RNA binds to and activates AKT phosphorylation and nuclear localization reducing apoptosis and enhancing cardiac repair. Theranostics 7:3842–3855 Du WW, Yang W, Li X, Awan FM, Yang Z, Fang L, Lyu J, Li F, Peng C, Krylov SN, Xie Y, Zhang Y, He C, Wu N, Zhang C, Sdiri M, Dong J, Ma J, Gao C, Hibberd S, Yang BB (2018) A circular RNA circ-DNMT1 enhances breast cancer progression by activating autophagy. Oncogene 37:5829–5842 Lin CY, Loven J, Rahl PB, Paranal RM, Burge CB, Bradner JE, Lee TI, Young RA (2012) Transcriptional amplification in tumor cells with elevated c-Myc. Cell 151:56–67 Baldanzi G, Filigheddu N, Cutrupi S, Catapano F, Bonissoni S, Fubini A, Malan D, Baj G, Granata R, Broglio F, Papotti M, Surico N, Bussolino F, Isgaard J, Deghenghi R, Sinigaglia F, Prat M, Muccioli G, Ghigo E, Graziani A (2002) Ghrelin and des-acyl ghrelin inhibit cell death in cardiomyocytes and endothelial cells through ERK1/2 and PI 3-kinase/AKT. J Cell Biol 159:1029–1037 Di R, Wu X, Chang Z, Zhao X, Feng Q, Lu S, Luan Q, Hemmings BA, Li X, Yang Z (2012) S6 K inhibition renders cardiac protection against myocardial infarction through PDK1 phosphorylation of Akt. Biochem J 441:199–207 White E (2016) Autophagy and p53. Cold Spring Harb Perspect Med 6:a026120 Tasdemir E, Chiara Maiuri M, Morselli E, Criollo A, D’Amelio M, Djavaheri-Mergny M, Cecconi F, Tavernarakis N, Kroemer G (2008) A dual role of p53 in the control of autophagy. Autophagy 4:810–814 Torrisani J, Unterberger A, Tendulkar SR, Shikimi K, Szyf M (2007) AUF1 cell cycle variations define genomic DNA methylation by regulation of DNMT1 mRNA stability. Mol Cell Biol 27:395–410 Georgia S, Kanji M, Bhushan A (2013) DNMT1 represses p53 to maintain progenitor cell survival during pancreatic organogenesis. Genes Dev 27:372–377 Du WW, Yang W, Chen Y, Wu ZK, Foster FS, Yang Z, Li X, Yang BB (2017) Foxo3 circular RNA promotes cardiac senescence by modulating multiple factors associated with stress and senescence responses. Eur Heart J 38:1402–1412 Chen Y, Yang F, Fang E, Xiao W, Mei H, Li H, Li D, Song H, Wang J, Hong M, Wang X, Huang K, Zheng L, Tong Q (2019) Circular RNA circAGO2 drives cancer progression through facilitating HuR-repressed functions of AGO2-miRNA complexes. Cell Death Differ 26:1346–1364 Fan XC, Steitz JA (1998) Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J 17:3448–3460 Zhou LY, Zhai M, Huang Y, Xu S, An T, Wang YH, Zhang RC, Liu CY, Dong YH, Wang M, Qian LL, Ponnusamy M, Zhang YH, Zhang J, Wang K (2019) The circular RNA ACR attenuates myocardial ischemia/reperfusion injury by suppressing autophagy via modulation of the Pink1/FAM65B pathway. Cell Death Differ 26:1299–1315 Ashwal-Fluss R, Meyer M, Pamudurti NR, Ivanov A, Bartok O, Hanan M, Evantal N, Memczak S, Rajewsky N, Kadener S (2014) circRNA biogenesis competes with pre-mRNA splicing. Mol Cell 56:55–66 Starke S, Jost I, Rossbach O, Schneider T, Schreiner S, Hung LH, Bindereif A (2015) Exon circularization requires canonical splice signals. Cell Rep 10:103–111 Abdelmohsen K, Panda AC, Munk R, Grammatikakis I, Dudekula DB, De S, Kim J, Noh JH, Kim KM, Martindale JL, Gorospe M (2017) Identification of HuR target circular RNAs uncovers suppression of PABPN1 translation by CircPABPN1. RNA Biol 14:361–369 Barnhart MD, Moon SL, Emch AW, Wilusz CJ, Wilusz J (2013) Changes in cellular mRNA stability, splicing, and polyadenylation through HuR protein sequestration by a cytoplasmic RNA virus. Cell Rep 5:909–917 Liu L, Zhuang R, Xiao L, Chung HK, Luo J, Turner DJ, Rao JN, Gorospe M, Wang JY (2017) HuR enhances early restitution of the intestinal epithelium by increasing Cdc42 translation. Mol Cell Biol 37:e00574-16 Nan A, Chen L, Zhang N, Jia Y, Li X, Zhou H, Ling Y, Wang Z, Yang C, Liu S, Jiang Y (2019) Circular RNA circNOL10 inhibits lung cancer development by promoting SCLM1-mediated transcriptional regulation of the humanin polypeptide family. Adv Sci 6:1800654 Du WW, Yang W, Liu E, Yang Z, Dhaliwal P, Yang BB (2016) Foxo3 circular RNA retards cell cycle progression via forming ternary complexes with p21 and CDK2. Nucleic Acids Res 44:2846–2858 Du WW, Fang L, Yang W, Wu N, Awan FM, Yang Z, Yang BB (2017) Induction of tumor apoptosis through a circular RNA enhancing Foxo3 activity. Cell Death Differ 24:357–370 Harper JW, Adami GR, Wei N, Keyomarsi K, Elledge SJ (1993) The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75:805–816 Haupt Y, Maya R, Kazaz A, Oren M (1997) Mdm2 promotes the rapid degradation of p53. Nature 387:296–299 Yang JY, Zong CS, Xia W, Yamaguchi H, Ding Q, Xie X, Lang JY, Lai CC, Chang CJ, Huang WC, Huang H, Kuo HP, Lee DF, Li LY, Lien HC, Cheng X, Chang KJ, Hsiao CD, Tsai FJ, Tsai CH, Sahin AA, Muller WJ, Mills GB, Yu D, Hortobagyi GN, Hung MC (2008) ERK promotes tumorigenesis by inhibiting FOXO3a via MDM2-mediated degradation. Nat Cell Biol 10:138–148 Ekoff M, Kaufmann T, Engstrom M, Motoyama N, Villunger A, Jonsson JI, Strasser A, Nilsson G (2007) The BH3-only protein Puma plays an essential role in cytokine deprivation induced apoptosis of mast cells. Blood 110:3209–3217 Sun L, Huang Y, Liu Y, Zhao Y, He X, Zhang L, Wang F, Zhang Y (2018) Ipatasertib, a novel Akt inhibitor, induces transcription factor FoxO3a and NF-kappaB directly regulates PUMA-dependent apoptosis. Cell Death Dis 9:911 Holdt LM, Stahringer A, Sass K, Pichler G, Kulak NA, Wilfert W, Kohlmaier A, Herbst A, Northoff BH, Nicolaou A, Gabel G, Beutner F, Scholz M, Thiery J, Musunuru K, Krohn K, Mann M, Teupser D (2016) Circular non-coding RNA ANRIL modulates ribosomal RNA maturation and atherosclerosis in humans. Nat Commun 7:12429 Grimm T, Holzel M, Rohrmoser M, Harasim T, Malamoussi A, Gruber-Eber A, Kremmer E, Eick D (2006) Dominant-negative Pes1 mutants inhibit ribosomal RNA processing and cell proliferation via incorporation into the PeBoW-complex. Nucleic Acids Res 34:3030–3043 Guevara NV, Kim HS, Antonova EI, Chan L (1999) The absence of p53 accelerates atherosclerosis by increasing cell proliferation in vivo. Nat Med 5:335–339 Wu G, Cai J, Han Y, Chen J, Huang ZP, Chen C, Cai Y, Huang H, Yang Y, Liu Y, Xu Z, He D, Zhang X, Hu X, Pinello L, Zhong D, He F, Yuan GC, Wang DZ, Zeng C (2014) LincRNA-p21 regulates neointima formation, vascular smooth muscle cell proliferation, apoptosis, and atherosclerosis by enhancing p53 activity. Circulation 130:1452–1465 Chen N, Zhao G, Yan X, Lv Z, Yin H, Zhang S, Song W, Li X, Li L, Du Z, Jia L, Zhou L, Li W, Hoffman AR, Hu JF, Cui J (2018) A novel FLI1 exonic circular RNA promotes metastasis in breast cancer by coordinately regulating TET1 and DNMT1. Genome Biol 19:218 Xia P, Wang S, Ye B, Du Y, Li C, Xiong Z, Qu Y, Fan Z (2018) A circular RNA protects dormant hematopoietic stem cells from DNA sensor cGAS-mediated exhaustion. Immunity 48(688–701):e687 Good CR, Panjarian S, Kelly AD, Madzo J, Patel B, Jelinek J, Issa JJ (2018) TET1-mediated hypomethylation activates oncogenic signaling in triple-negative breast cancer. Can Res 78:4126–4137 Galluzzi L, Vanpouille-Box C, Bakhoum SF, Demaria S (2018) SnapShot: CGAS-STING signaling. Cell 173(276–276):e271 Essers MA, Offner S, Blanco-Bose WE, Waibler Z, Kalinke U, Duchosal MA, Trumpp A (2009) IFNalpha activates dormant haematopoietic stem cells in vivo. Nature 458:904–908 Sato T, Onai N, Yoshihara H, Arai F, Suda T, Ohteki T (2009) Interferon regulatory factor-2 protects quiescent hematopoietic stem cells from type I interferon-dependent exhaustion. Nat Med 15:696–700 Bellaousov S, Reuter JS, Seetin MG, Mathews DH (2013) RNAstructure: web servers for RNA secondary structure prediction and analysis. Nucleic Acids Res 41:W471–W474 Gruber AR, Lorenz R, Bernhart SH, Neubock R, Hofacker IL (2008) The Vienna RNA websuite. Nucleic Acids Res 36:W70–74 Bellucci M, Agostini F, Masin M, Tartaglia GG (2011) Predicting protein associations with long noncoding RNAs. Nat Methods 8:444–445 Muppirala UK, Honavar VG, Dobbs D (2011) Predicting RNA–protein interactions using only sequence information. BMC Bioinf 12:489 De Gregorio E, Preiss T, Hentze MW (1999) Translation driven by an eIF4G core domain in vivo. EMBO J 18:4865–4874 Hirsch JD, Eslamizar L, Filanoski BJ, Malekzadeh N, Haugland RP, Beechem JM, Haugland RP (2002) Easily reversible desthiobiotin binding to streptavidin, avidin, and other biotin-binding proteins: uses for protein labeling, detection, and isolation. Anal Biochem 308:343–357