环状RNA翻译能力研究进展
收稿日期: 2020-01-07
修回日期: 2020-03-24
网络出版日期: 2020-04-01
基金资助
国家自然科学基金项目编号(31772578);国家自然科学基金项目编号(31672402);四川省科技支撑计划项目资助编号(2016NYZ0045)
Progress on translation ability of circular RNA
Received date: 2020-01-07
Revised date: 2020-03-24
Online published: 2020-04-01
Supported by
Supported by the National Natural Science Foundation of China Nos(31772578);Supported by the National Natural Science Foundation of China Nos(31672402);the Science and Technology Program of Sichuan Province No(2016NYZ0045)
郑帅龙, 李利, 张红平 . 环状RNA翻译能力研究进展[J]. 遗传, 2020 , 42(5) : 423 -434 . DOI: 10.16288/j.yczz.19-354
With the rapid development of high-throughput sequencing technology and translatome studies, the translational ability of circular RNA (circRNA) has gradually attracted much attention. Previous studies have shown that circRNA itself can be translated into proteins, whose function is closely related to the occurrence and development of human diseases. And it is expected to become an ideal substitute for mRNA, which can be widely used in protein engineering in the future. In this review, we systematically summarize the sources, biogenesis and features of circRNA, the driving models of circRNA translation, identification and functional verification of circRNA translation. We also sum up the latest research progress of circRNA translation in human diseases and its application in protein engineering, and make prospective anticipations for future research directions, which may offer more theoretical references for related researches in this field.
Key words: circular RNA; protein translation; identification methods
| [1] | 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 USA, 1976,73(11):3852-3856. |
| [2] | Grabowski PJ, Zaug AJ, Cech TR . The intervening sequence of the ribosomal RNA precursor is converted to a circular RNA in isolated nuclei of tetrahymena. Cell, 1981,23(2):467-476. |
| [3] | Kjems J, Garrett RA . Novel splicing mechanism for the ribosomal RNA intron in the archaebacterium desulfurococcus mobilis. Cell, 1988,54(5):693-703. |
| [4] | 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(6):2985-2993. |
| [5] | 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(5):1019-1030. |
| [6] | Zaphiropoulos PG . Circular RNAs from transcripts of the rat cytochrome P450 2C24 gene: correlation with exon skipping. Proc Natl Acad Sci USA, 1996,93(13):6536-6541. |
| [7] | Kos A, Dijkema R, Arnberg AC, van der Meide PH, Schellekens H. The hepatitis delta (δ) virus possesses a circular RNA. Nature, 1986,323(6088):558-560. |
| [8] | Chen CY, Sarnow P . Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs. Science, 1995,268(5209):415-417. |
| [9] | Perriman R, Ares M . Circular mRNA can direct translation of extremely long repeating-sequence proteins in vivo. RNA, 1998,4(9):1047. |
| [10] | Wang Y, Wang Z . Efficient backsplicing produces translatable circular mRNAs. RNA, 2015,21(2):172-179. |
| [11] | Pamudurti NR, Bartok O, Jens M, Ashwalfluss R, Stottmeister C, Ruhe L, Hanan M, Wyler E, Perezhernandez D, Ramberger E, Shenzis S, Samson M, Dittmar G, Landthaler M, Chekulaeva M, Rajewsky N, Kadener S. Translation of circRNAs. Mol Cell, 2017, 66(1): 9-21.e7. |
| [12] | 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 . Circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis. Mol Cell, 2017,66(1):22-37. |
| [13] | Yang Y, Fan XJ, Mao MW, Song XW, Wu P, Zhang Y, Jin YF, Yang Y, Chen LL, Wang Y, Wong CC, Xiao XS, Wang ZF . Extensive translation of circular RNAs driven by N 6-methyladenosine . Cell Res, 2017,27(5):626-641. |
| [14] | Yang YB, Gao XY, Zhang ML, Yan S, Sun CJ, Xiao FZ, Huang NN, Yang XS, Zhao K, Zhou HK . Novel role of FBXW7 circular RNA in repressing glioma tumorigenesis. J Natl Cancer I, 2018,110(3):304-315. |
| [15] | Gao Y, Wang JF, Zheng Y, Zhang JY, Chen S, Zhao FQ . Comprehensive identification of internal structure and alternative splicing events in circular RNAs. Nat Commun, 2016,7:12060. |
| [16] | Chen LL, Yang L . Regulation of circRNA biogenesis. RNA Biol, 2015,12(4):381-388. |
| [17] | 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(6):792-806. |
| [18] | 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(6):1125-1134. |
| [19] | Suzuki H, Tsukahara T . A view of pre-mRNA splicing from RNase R resistant RNAs. Int J Mol Sci, 2014,15(6):9331-9342. |
| [20] | Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE, Liu JZ, Marzluff WF, Sharpless NE . Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA, 2013,19(2):141-157. |
| [21] | Ven? MT, Hansen TB, Ven? 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(1):245. |
| [22] | Rybak-Wolf A, Stottmeister C, Gla?ar P, Jens M, Pino N, Giusti S, Hanan M, Behm M, Bartok O, Ashwal-Fluss R, Herzog M, Schreyer L, Papavasileiou P, Ivanov A, ?hman M, Refojo D, Kadener S, Rajewsky N . Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed. Mol Cell, 2015,58(5):870-885. |
| [23] | 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(1):126. |
| [24] | You XT, Vlatkovic I, Babic A, Will T, Epstein I, Tushev G, Akbalik G, Wang MT, Glock C, Quedenau C, Wang X, Hou JY, Liu HY, Sun W, Sambandan S, Chen T, Schuman EM, Chen W . Neural circular RNAs are derived from synaptic genes and regulated by development and plasticity. Nat Neurosci, 2015,18(4):603-610. |
| [25] | Li ZY, Huang C, Bao C, Chen L, Lin M, Wang XL, Zhong GL, Yu B, Hu WC, Dai LM, Zhu PF, Chang ZX, Wu QF, Zhao Y, Jia Y, Xu P, Liu HJ, Shan G . Exon-intron circular RNAs regulate transcription in the nucleus. Nat Struct Mol Biol, 2015,22(3):256-264. |
| [26] | Conn VM, Hugouvieux V, Nayak A, Conos SA, Capovilla G, Cildir G, Jourdain A, Tergaonkar V, Schmid M, Zubieta C, Conn SJ . A circRNA from SEPALLATA3 regulates splicing of its cognate mRNA through R-loop formation. Nat Plants, 2017,3(5):17053. |
| [27] | Xu HY, Guo S, Li W, Yu P . The circular RNA Cdr1as, via miR-7 and its targets, regulates insulin transcription and secretion in islet cells. Sci Rep, 2015,5(1):12453. |
| [28] | Li H, Wei XF, Yang JM, Dong D, Hao D, Huang YZ, Lan XY, Plath M, Lei CZ, Ma Y, Lin FP, Bai YY, Chen H . CircFGFR4 promotes differentiation of myoblasts via binding miR-107 to relieve its inhibition of Wnt3a. Mol Ther Nucleic Acids, 2018,11:272-283. |
| [29] | Feng Y, Hu AP, Li D, Wang JQ, Guo YH, Liu Y, Li HJ, Chen YJ, Wang XJ, Huang K, Zheng LD, Tong QS . Circ-HuR suppresses HuR expression and gastric cancer progression by inhibiting CNBP transactivation. Mol Cancer, 2019,18(1):158. |
| [30] | Dong R, Zhang XO, Zhang Y, Ma XK, Chen LL, Yang L . CircRNA-derived pseudogenes. Cell Res, 2016,26(6):747-750. |
| [31] | Chen GW, Shi YT, Liu MM, Sun JY. circHIPK3 regulates cell proliferation and migration by sponging miR-124 and regulating AQP3 expression in hepatocellular carcinoma. Cell Death Dis, 2018,9(2):175. |
| [32] | Haimov O, Sinvani H, Dikstein R . Cap-dependent, scanning-free translation initiation mechanisms. Biochim Biophys Acta, 2015,1849(11):1313-1318. |
| [33] | Liu XQ, Gao YB, Zhao LZ, Cai YC, Wang HY, Miao M, Gu LF, Zhang HX . Biogenesis, research methods, and functions of circular RNAs. Hereditas (Beijing), 2019,41(6):469-485. |
| [33] | 刘旭庆, 高宇帮, 赵良真, 蔡宇晨, 王汇源, 苗苗, 顾连峰, 张航晓 . 环状RNA的产生、研究方法及功能. 遗传, 2019,41(6):469-485. |
| [34] | Abe N, Matsumoto K, Nishihara M, Nakano Y, Shibata A, Maruyama H, Shuto S, Matsuda A, Yoshida M, Ito Y, Abe H . Rolling circle translation of circular RNA in living human cells. Sci Rep, 2015,5:16435. |
| [35] | Ruggero D, Sonenberg N . The Akt of translational control. Oncogene, 2005,24(50):7426-7434. |
| [36] | Zhao JW, Lee EE, Kim J, Yang R, Chamseddin B, Ni CY, Gusho E, Xie Y, Chiang CM, Buszczak M, Zhan XW, Laimins L, Wang RC . Transforming activity of an oncoprotein-encoding circular RNA from human papillomavirus. Nat Commun, 2019,10(1):2300. |
| [37] | Zheng Y, Ji PF, Chen S, Hou LL, Zhao FQ. Reconstruction of full-length circular RNAs enables isoform-level quantification. Genome Med, 2019(1), 11:2. |
| [38] | Zhang JY, Chen S, Yang JW, Zhao FQ . Accurate quantification of circular RNAs identififies extensive circular isoform switching events. Nat Commun, 2020,11:90. |
| [39] | Stothard P . The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques, 2000,28(6):1102-1104. |
| [40] | Kong L, Zhang Y, Ye ZQ, Liu XQ, Zhao SQ, Wei LP, Gao G . CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res, 2007,35:345-349. |
| [41] | Wang LG, Park HJ, Dasari S, Wang SQ, Kocher JP, Li W . CPAT: coding-potential assessment tool using an alignment- free logistic regression model. Nucleic Acids Res, 2015,41(6):e74. |
| [42] | Zhao J, Wu J, Xu T, Yang Q, He J, Song X . IRESfinder: Identifying RNA internal ribosome entry site in eukaryotic cell using framed k-mer features. J Genet Genomics, 2018,45(7):403-406. |
| [43] | Mokrejs M, Vopálensky V, Kolenaty O, Masek T, Feketová Z, Sekyrová P, Skaloudová B, Kríz V, Pospísek M . IRESite: the database of experimentally verified IRES structures. Nucleic Acids Res, 2006,34:125-130. |
| [44] | Zhou Y, Zeng P, Li YH, Zhang Z, Cui Q . SRAMP: prediction of mammalian N 6-methyladenosine (m 6A) sites based on sequence-derived features . Nucleic Acids Res, 2016,44(10):e91. |
| [45] | Wei LY, Chen HR, Su R . M6APred-EL: A sequence-based predictor for identifying N 6-methyladenosine sites using ensemble learning . Mol Ther Nuceicl Acids, 2018,12:635-644. |
| [46] | Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer ELL, Tate J, Punta M . Pfam: the protein families database. Nucleic Acids Res, 2013,42(1):222-230. |
| [47] | Sun P, Li GL . CircCode: a powerful tool for identifying circRNA coding ability. Front Genet, 2019,10:981. |
| [48] | Chen XP, Han P, Zhou T, Guo XJ, Song XF, Li Y. circRNADb: a comprehensive database for human circular RNAs with protein-coding annotations. Sci Rep, 2016,6:34985. |
| [49] | Liu M, Wang Q, Shen J, Yang BB, Ding XM . Circbank: a comprehensive database for circRNA with standard nomenclature. Rna Biol, 2019,7:899-905. |
| [50] | Gla?ar P, Papavasileiou P, Rajewsky N . CircBase: a database for circular RNAs. RNA, 2014,20(11):1666-1670. |
| [51] | Xia SY, Feng J, Chen K, Ma YB, Gong J, Cai FF, Jin YX, Gao Y, Xia LJ, Chang H, Wei L, Han L, He CJ . CSCD: a database for cancer-specific circular RNAs. Nucleic Acids Res, 2017,46(D1):925-929. |
| [52] | Xia SY, Feng J, Lei LJ, Hu J, Xia LJ, Wang J, Xiang Y, Liu LJ, Zhong S, Han L, He CJ . Comprehensive characterization of tissue-specific circular RNAs in the human and mouse genomes. Brief Bioinform, 2016,18(6):984-992. |
| [53] | Dong R, Ma XK, Li GW, Yang L . CIRCpedia v2: an updated database for comprehensive circular RNA annotation and expression comparison. Genom Proteom Bioinf, 2018,16(4):226-233. |
| [54] | Panda AC, Dudekula DB, Abdelmohsen K, Gorospe M . Analysis of circular RNAs using the web tool CircInteractome. Methods Mol Biol, 2018,1724:43-56. |
| [55] | Liu YC, Li JR, Sun CH, Andrews E, Chao RF, Lin MF, Weng SL, Hsu SD, Huang CC, Cheng C, Liu CC, Huang HD . CircNet: a database of circular RNAs derived from transcriptome sequencing data. Nucleic Acids Res, 2016,44(1):209-215. |
| [56] | Chu Q, Zhang X, Zhu X, Liu C, Mao L, Ye C, Zhu QH, Fan L . PlantcircBase: a database for plant circular RNAs. Mol Plant, 2017,10(8):1126-1128. |
| [57] | Ghosal S, Das S, Sen R, Basak P, Chakrabarti J . Circ2Traits: a comprehensive database for circular RNA potentially associated with disease and traits. Front Genet, 2013,4:283. |
| [58] | Ji PF, Wu WY, Chen S, Zheng Y, Zhou L, Zhang JY, Cheng H, Yan J, Zhang SG, Yang PH, Zhao FQ. Expanded expression landscape and prioritization of circular RNAs in mammals. Cell Rep, 2019,26(12): 3444-3460. e5. |
| [59] | Ingolia NT, Lareau LF, Weissman JS . Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell, 2011,147(4):789-802. |
| [60] | Ingolia NT, Ghaemmaghami S, Newman JRS, Weissman JS . Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science, 2009,324(5924):218-223. |
| [61] | Xia X, Li XX, Li FY, Wu XJ, Zhang ML, Zhou HK, Huang NN, Yang XS, Xiao FZ, Liu DW, Yang LX, Zhang N . A novel tumor suppressor protein encoded by circular AKT3 RNA inhibits glioblastoma tumorigenicity by competing with active phosphoinositide-dependent Kinase-1. Mol Cancer, 2019,18(1):131. |
| [62] | Tenenbaum SA, Lager PJ, Carson CC, Keene JD . Ribonomics: identifying mRNA subsets in mRNP complexes using antibodies to RNA-binding proteins and genomic arrays. Methods, 2002,26(2):191-198. |
| [63] | Marín-Béjar O, Huarte M . RNA pulldown protocol for in vitro detection and identification of RNA-associated proteins. Methods Mol Biol, 2015,1206:87-95. |
| [64] | Zhang ML, Zhao K, Xu XP, Yang YB, Yan S, Wei P, Liu H, Xu JB, Xiao FZ, Zhou HK, Yang XS, Huang NN, Liu JL, He KJ, Xie KP, Zhang G, Huang SY, Zhang N . A peptide encoded by circular form of LINC-PINT suppresses oncogenic transcriptional elongation in glioblastoma. Nat Commun, 2018,9(1):4475. |
| [65] | Liang WC, Wong CW, Liang PP, Shi M, Cao Y, Rao ST, Tsui SKW, Waye MMY, Zhang Q, Fu WM, Zhang JF . Translation of the circular RNA circβ-catenin promotes liver cancer cell growth through activation of the Wnt pathway. Genome Biol, 2019,20(1):84. |
| [66] | Gu CH, Zhou NC, Wang ZY, Li GR, Kou YP, Yu SL, Feng YJ, Chen L, Yang JJ, Tian FY . CircGprc5a promoted bladder oncogenesis and metastasis through Gprc5a- targeting peptide. Mol Ther Nucleic Acids, 2018,13:633-641. |
| [67] | 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, Mücke MB, Lindberg EL, Trnka F, Memczak S, Schilling M, Felkin LE, Barton PJR, Quaife NM, Vanezis K, Diecke S, Mukai M, Mah N, Oh S-J, Kurtz A, Schramm C, Schwinge D, Sebode M, Harakalova M, Asselbergs FW, Vink A, de Weger RA, Viswanathan S, Widjaja AA, G?rtner-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. The translational landscape of the human heart. Cell, 2019,178(1):242-260. |
| [68] | Zhang ML, Huang NN, Yang XS, Luo JY, Yan S, Xiao FZ, Chen WP, Gao XY, Zhao K, Zhou HK, Li ZQ, Ming L, Xie B, Zhang N . A novel protein encoded by the circular form of the SHPRH gene suppresses glioma tumorigenesis. Oncogene, 2018,37(13):1805-1814. |
| [69] | Wesselhoeft RA, Kowalski PS, Anderson DG . Engineering circular RNA for potent and stable translation in eukaryotic cells. Nat Commun, 2018,9(1):2629. |
| [70] | Wesselhoeft RA, Kowalski PS, Parker-Hale FC, Huang YX, Bisaria N, Anderson DG . RNA circularization diminishes immunogenicity and can extend translation duration in vivo. Mol Cell, 2019,74(3):508-520. |
/
| 〈 |
|
〉 |