RNA修饰在病毒复制中的功能The Function of RNA Modifications in Viral Replication
郝好杰;余宝成;胡章立;袁建辉;关武祥;
摘要(Abstract):
早在60多年前科学家已经发现RNA化学修饰的存在,但直到近年来关于RNA修饰功能的研究才得到广泛关注及蓬勃发展,其中病毒RNA修饰的功能成为了病毒学研究领域新的热点。目前已有150多种RNA修饰被发现,这些修饰在调控RNA结构、剪接、核运输、翻译、稳定性等多种生物过程中发挥重要作用。目前病毒RNA修饰中最受关注的7种化学修饰包括N6-甲基腺苷(m6A)、5-甲基胞苷(m5C)、N1-甲基腺苷(m1A)、N7-甲基鸟苷(m7G)、N4-乙酰胞苷(ac4C)、假尿苷(Ψ)和核糖甲基化(Nm)。本文介绍了细胞中的修饰系统,讨论了当前各种修饰的检测方法并对这些修饰在病毒复制中的功能进行了归纳总结。此外,我们提出了病毒RNA修饰未来可能的一些研究方向。
关键词(KeyWords): RNA化学修饰;病毒感染;甲基化修饰;乙酰化修饰;假尿嘧啶
基金项目(Foundation): 国家自然科学基金项目(项目号:32000114),题目:N4-acetylcytidine调控肠病毒71型复制的分子机制~~
作者(Authors): 郝好杰;余宝成;胡章立;袁建辉;关武祥;
DOI: 10.13242/j.cnki.bingduxuebao.220182
参考文献(References):
- [1]Davis F F,Allen F W. Ribonucleic acids from yeast which contain a fifth nucleotide[J]. J Biol Chem,1957,227(2):907-915.
- [2]Lence T,Paolantoni C,Worpenberg L,Roignant J Y.Mechanistic insights into m(6)A RNA enzymes[J].Biochim Biophys Acta Gene Regul Mech,2019,1862(3):222-229.
- [3]Roundtree I A,Evans M E,Pan T,He C. Dynamic RNA modifications in gene expression regulation[J].Cell,2017,169(7):1187-1200.
- [4]Zhao B S,Roundtree I A,He C. Post-transcriptional gene regulation by mRNA modifications[J]. Nat Rev Mol Cell Biol,2017,18(1):31-42.
- [5]McIntyre W,Netzband R,Bonenfant G,Biegel J M,Miller C,Fuchs G,Henderson E,Arra M,Canki M,Fabris D, Pager C T. Positive-sense RNA viruses reveal the complexity and dynamics of the cellular and viral epitranscriptomes during infection[J]. Nucleic Acids Res,2018,46(11):5776-5791.
- [6]Baquero-Perez B,Geers D,Diez J. From A to m(6)A:the emerging viral epitranscriptome[J/OL]. Viruses,2021,13(6):1049. DOI:10.3390/v13061049.
- [7]Wei C M, Gershowitz A, Moss B. Methylated nucleotides block 5'terminus of HeLa cell messenger RNA[J]. Cell,1975,4(4):379-386.
- [8]Ping X L,Sun B F,Wang L,Xiao W,Yang X,Wang W J,Adhikari S,Shi Y,Lv Y,Chen Y S,Zhao X,Li A,Yang Y,Dahal U,Lou X M,Liu X,Huang J,Yuan W P,Zhu X F,Cheng T,Zhao Y L,Wang X,Rendtlew Danielsen J M, Liu F, Yang Y G.Mammalian WTAP is a regulatory subunit of the RNA N6-methyladenosine methyltransferase[J]. Cell Res,2014,24(2):177-189.
- [9]Weng H,Huang H,Wu H,Qin X,Zhao B S,Dong L,Shi H,Skibbe J,Shen C,Hu C,Sheng Y,Wang Y,Wunderlich M,Zhang B,Dore L C,Su R,Deng X,Ferchen K,Li C,Sun M,Lu Z,Jiang X,Marcucci G,Mulloy J C,Yang J,Qian Z,Wei M,He C,Chen J. METTL14 inhibits hematopoietic stem/progenitor differentiation and promotes leukemogenesis via mRNA m(6)a modification[J/OL]. Cell Stem Cell,2018,22(2):191-205 e199.
- [10]Bokar J A,Shambaugh M E,Polayes D,Matera A G,Rottman F M. Purification and cDNA cloning of the AdoMet-binding subunit of the human mRNA(N6-adenosine)-methyltransferase[J]. RNA,1997,3(11):1233-1247.
- [11]Wen J,Lv R,Ma H,Shen H,He C,Wang J,Jiao F,Liu H,Yang P,Tan L,Lan F,Shi Y G,He C,Shi Y, Diao J. Zc3h13 regulates nuclear RNA m(6)a methylation and mouse embryonic stem cell self-renewal[J/OL]. Mol Cell,2018,69(6):1028-1038 e1026.
- [12]Knuckles P, Lence T, Haussmann I U, Jacob D,Kreim N,Carl S H,Masiello I,Hares T,Villasenor R,Hess D,Andrade-Navarro M A,Biggiogera M,Helm M,Soller M,Buhler M,Roignant J Y. Zc3h13/Flacc is required for adenosine methylation by bridging the mRNA-binding factor Rbm15/Spenito to the m(6)A machinery component Wtap/Fl(2)d[J]. Genes Dev,2018,32(5-6):415-429.
- [13]Ruzicka K,Zhang M,Campilho A,Bodi Z,Kashif M,Saleh M,Eeckhout D,El-Showk S,Li H,Zhong S,De Jaeger G,Mongan N P,Hejatko J,Helariutta Y,Fray R G. Identification of factors required for m(6)A mRNA methylation in Arabidopsis reveals a role for the conserved E3 ubiquitin ligase HAKAI[J]. New Phytol,2017,215(1):157-172.
- [14]Horiuchi K,Kawamura T,Iwanari H,Ohashi R,Naito M,Kodama T,Hamakubo T. Identification of Wilms'tumor 1-associating protein complex and its role in alternative splicing and the cell cycle[J]. J Biol Chem,2013,288(46):33292-33302.
- [15]Yue Y,Liu J,Cui X,Cao J,Luo G,Zhang Z,Cheng T,Gao M,Shu X,Ma H,Wang F,Wang X,Shen B,Wang Y,Feng X,He C,Liu J. VIRMA mediates preferential m(6)A mRNA methylation in 3'UTR and near stop codon and associates with alternative polyadenylation[J]. Cell Discov,2018,4:10.
- [16]Schwartz S,Mumbach M R,Jovanovic M,Wang T,Maciag K,Bushkin G G,Mertins P,Ter-Ovanesyan D,Habib N,Cacchiarelli D,Sanjana N E,Freinkman E,Pacold M E,Satija R,Mikkelsen T S,Hacohen N,Zhang F, Carr S A, Lander E S, Regev A.Perturbation of m6A writers reveals two distinct classes of mRNA methylation at internal and 5'sites[J]. Cell Rep,2014,8(1):284-296.
- [17]Warda A S,Kretschmer J,Hackert P,Lenz C,Urlaub H,Hobartner C,Sloan K E,Bohnsack M T. Human METTL16 is a N(6)-methyladenosine(m(6)A)methyltransferase that targets pre-mRNAs and various non-coding RNAs[J]. EMBO Rep,2017,18(11):2004-2014.
- [18]Pendleton K E,Chen B,Liu K,Hunter O V,Xie Y,Tu B P, Conrad N K. The U6 snRNA m(6)A methyltransferase METTL16 Regulates SAM synthetase intron retention[J/OL]. Cell, 2017, 169(5):824-835 e814.
- [19]Chen B,Li Y,Song R,Xue C,Xu F. Functions of RNA N6-methyladenosine modification in cancer progression[J]. Mol Biol Rep,2019,46(2):2567-2575.
- [20]Xu C,Wang X,Liu K,Roundtree I A,Tempel W,Li Y,Lu Z,He C,Min J. Structural basis for selective binding of m6A RNA by the YTHDC1 YTH domain[J]. Nat Chem Biol,2014,10(11):927-929.
- [21]Zhang Z,Theler D,Kaminska K H,Hiller M,de la Grange P,Pudimat R,Rafalska I,Heinrich B,Bujnicki J M,Allain F H,Stamm S. The YTH domain is a novel RNA binding domain[J]. J Biol Chem,2010,285(19):14701-14710.
- [22]Wang X,Zhao B S,Roundtree I A,Lu Z,Han D,Ma H, Weng X, Chen K, Shi H, He C. N(6)-methyladenosine modulates messenger rna translation efficiency[J]. Cell,2015,161(6):1388-1399.
- [23]Wang X, He C. Reading RNA methylation codes through methyl-specific binding proteins[J]. RNA Biol,2014,11(6):669-672.
- [24]Li A,Chen Y S,Ping X L,Yang X,Xiao W,Yang Y,Sun H Y,Zhu Q,Baidya P,Wang X,Bhattarai D P,Zhao Y L,Sun B F,Yang Y G. Cytoplasmic m6A reader YTHDF3 promotes mRNA translation[J]. Cell Res,2017,27(3):444-447.
- [25]Shi H,Wang X,Lu Z,Zhao B S,Ma H,Hsu P J,Liu C,He C. YTHDF3 facilitates translation and decay of N(6)-methyladenosine-modified RNA[J]. Cell Res,2017,27(3):315-328.
- [26]Roundtree I A,Luo G Z,Zhang Z,Wang X,Zhou T,Cui Y,Sha J,Huang X,Guerrero L,Xie P,He E,Shen B,He C. YTHDC1 mediates nuclear export of N(6)-methyladenosine methylated mRNAs[J]. Elife,2017,6.
- [27]Hsu P J,Zhu Y,Ma H,Guo Y,Shi X,Liu Y,Qi M,Lu Z,Shi H,Wang J,Cheng Y,Luo G,Dai Q,Liu M,Guo X,Sha J,Shen B,He C. Ythdc2 is an N6-methyladenosine binding protein that regulates mammalian spermatogenesis[J]. Cell Res,2017,27(9):1115-1127.
- [28]Meyer K D,Patil D P,Zhou J,Zinoviev A,Skabkin M A,Elemento O,Pestova T V,Qian S B,Jaffrey S R.5'UTR m(6)A promotes cap-independent translation[J]. Cell,2015,163(4):999-1010.
- [29]Alarcon C R,Goodarzi H,Lee H,Liu X,Tavazoie S,Tavazoie S F. HNRNPA2B1 is a mediator of m(6)adependent nuclear RNA processing events[J]. Cell,2015,162(6):1299-1308.
- [30]Liu N,Dai Q,Zheng G,He C,Parisien M,Pan T. N(6)-methyladenosine-dependent RNA structural switches regulate RNA-protein interactions[J]. Nature,2015,518(7540):560-564.
- [31]Huang H,Weng H,Sun W,Qin X,Shi H,Wu H,Zhao B S,Mesquita A,Liu C,Yuan C L,Hu Y C,Huttelmaier S,Skibbe J R,Su R,Deng X,Dong L,Sun M, Li C, Nachtergaele S, Wang Y, Hu C,Ferchen K,Greis K D,Jiang X,Wei M,Qu L,Guan J L,He C,Yang J,Chen J. Recognition of RNA N(6)-methyladenosine by IGF2BP proteins enhances mRNA stability and translation[J]. Nat Cell Biol,2018,20(3):285-295.
- [32]Shao J,Liu J,Zuo S. Roles of epigenetics in cardiac fibroblast activation and fibrosis[J]. Cells, 2022,11(15):2347.
- [33]Zhu H, Wang G, Qian J. Transcription factors as readers and effectors of DNA methylation[J]. Nat Rev Genet,2016,17(9):551-565.
- [34]Neri F,Rapelli S,Krepelova A,Incarnato D,Parlato C, Basile G, Maldotti M, Anselmi F, Oliviero S.Intragenic DNA methylation prevents spurious transcription initiation[J]. Nature,2017,543(7643):72-77.
- [35]Bohnsack K E, Hobartner C, Bohnsack M T.Eukaryotic 5-methylcytosine(m(5)C)RNA methyltransferases:mechanisms,cellular functions,and links to disease[J]. Genes(Basel),2019,10(2).
- [36]Song H,Zhang J,Liu B,Xu J,Cai B,Yang H,Straube J,Yu X,Ma T. Biological roles of RNA m(5)C modification and its implications in Cancer immunotherapy[J]. Biomark Res,2022,10(1):15.
- [37]Tsai K,Cullen B R. Epigenetic and epitranscriptomic regulation of viral replication[J]. Nat Rev Microbiol,2020.
- [38]Schosserer M,Minois N,Angerer T B,Amring M,Dellago H,Harreither E,Calle-Perez A,Pircher A,Gerstl M P,Pfeifenberger S,Brandl C,Sonntagbauer M,Kriegner A,Linder A,Weinhausel A,Mohr T,Steiger M,Mattanovich D,Rinnerthaler M,Karl T,Sharma S, Entian K D, Kos M, Breitenbach M,Wilson I B, Polacek N, Grillari-Voglauer R,Breitenbach-Koller L, Grillari J. Methylation of ribosomal RNA by NSUN5 is a conserved mechanism modulating organismal lifespan[J]. Nat Commun,2015,6:6158.
- [39]Xu Y,Zhang M,Zhang Q,Yu X,Sun Z,He Y,Guo W. Role of main RNA methylation in hepatocellular carcinoma:n6-methyladenosine,5-methylcytosine,and n1-methyladenosine[J]. Front Cell Dev Biol,2021,9:767668.
- [40]Heissenberger C, Rollins J A, Krammer T L,Nagelreiter F,Stocker I,Wacheul L,Shpylovyi A,Tav K,Snow S,Grillari J,Rogers A N,Lafontaine D L J, Schosserer M. The ribosomal RNA m(5)C methyltransferase NSUN-1 modulates healthspan and oogenesis in Caenorhabditis elegans[J]. Elife,2020,9.
- [41]Tuorto F,Liebers R,Musch T,Schaefer M,Hofmann S,Kellner S,Frye M,Helm M,Stoecklin G,Lyko F.RNA cytosine methylation by Dnmt2 and NSun2promotes tRNA stability and protein synthesis[J]. Nat Struct Mol Biol,2012,19(9):900-905.
- [42]Shen Q,Zhang Q,Shi Y,Shi Q,Jiang Y,Gu Y,Li Z, Li X, Zhao K, Wang C, Li N, Cao X. Tet2promotes pathogen infection-induced myelopoiesis through mRNA oxidation[J]. Nature, 2018, 554(7690):123-127.
- [43]Shen H, Ontiveros R J, Owens M C, Liu M Y,Ghanty U,Kohli R M,Liu K F. TET-mediated 5-methylcytosine oxidation in tRNA promotes translation[J]. J Biol Chem,2021,296:100087.
- [44]Haag S, Sloan K E, Ranjan N, Warda A S,Kretschmer J,Blessing C,Hubner B,Seikowski J,Dennerlein S,Rehling P,Rodnina M V,Hobartner C,Bohnsack M T. NSUN3 and ABH1 modify the wobble position of mt-tRNAMet to expand codon recognition in mitochondrial translation[J]. EMBO J,2016,35(19):2104-2119.
- [45]Yang X,Yang Y,Sun B F,Chen Y S,Xu J W,Lai W Y,Li A,Wang X,Bhattarai D P,Xiao W,Sun H Y,Zhu Q,Ma H L,Adhikari S,Sun M,Hao Y J,Zhang B,Huang C M,Huang N,Jiang G B,Zhao Y L,Wang H L,Sun Y P,Yang Y G. 5-methylcytosine promotes mRNA export-NSUN2 as the methyltransferase and ALYREF as an m(5)C reader[J]. Cell Res,2017,27(5):606-625.
- [46]Zou F,Tu R,Duan B,Yang Z,Ping Z,Song X,Chen S,Price A,Li H,Scott A,Perera A,Li S,Xie T.Drosophila YBX1 homolog YPS promotes ovarian germ line stem cell development by preferentially recognizing 5-methylcytosine RNAs[J]. Proc Natl Acad Sci U S A,2020,117(7):3603-3609.
- [47]Dunn D B. The occurrence of 1-methyladenine in ribonucleic acid[J]. Biochim Biophys Acta,1961,46:198-200.
- [48]Wiener D,Schwartz S. The epitranscriptome beyond m(6)A[J]. Nat Rev Genet,2020(2):119-131.
- [49]Kuang W,Jin H,Yang F,Chen X,Liu J,Li T,Chang Y,Liu M,Xu Z,Huo C,Yan X,Yang Y,Liu W,Shu Q,Xie S,Zhou T. ALKBH3-dependent m(1)A demethylation of Aurora A mRNA inhibits ciliogenesis[J]. Cell Discov,2022,8(1):25.
- [50]Furuichi Y. Discovery of m(7)G-cap in eukaryotic mRNAs[J]. Proc Jpn Acad Ser B Phys Biol Sci,2015,91(8):394-409.
- [51]Cowling V H. Regulation of mRNA cap methylation[J].Biochem J,2009,425(2):295-302.
- [52]Guy M P, Phizicky E M. Two-subunit enzymes involved in eukaryotic post-transcriptional tRNA modification[J]. RNA Biol,2014,11(12):1608-1618.
- [53]Sloan K E, Warda A S, Sharma S, Entian K D,Lafontaine D L J, Bohnsack M T. Tuning the ribosome:The influence of rRNA modification on eukaryotic ribosome biogenesis and function[J]. RNA Biol,2017,14(9):1138-1152.
- [54]Zhang L S,Liu C,Ma H,Dai Q,Sun H L,Luo G,Zhang Z, Zhang L, Hu L, Dong X, He C.Transcriptome-wide mapping of internal n(7)-methylguanosine methylome in mammalian mRNA[J/OL]. Mol Cell,2019,74(6):1304-1316 e1308.
- [55]Ito S,Horikawa S,Suzuki T,Kawauchi H,Tanaka Y,Suzuki T,Suzuki T. Human NAT10 is an ATPdependent RNA acetyltransferase responsible for N4-acetylcytidine formation in 18 S ribosomal RNA(rRNA)[J]. J Biol Chem,2014,289(52):35724-35730.
- [56]Courtney D G. Post-transcriptional regulation of viral rna through epitranscriptional modification[J/OL]. Cells,2021,10(5):1129. DOI:10.3390/cells10051129.
- [57]Kawai G,Hashizume T,Miyazawa T,McCloskey J A,Yokoyama S. Conformational characteristics of 4-acetylcytidine found in tRNA[J]. Nucleic Acids Symp Ser,1989(21):61-62.
- [58]Kumbhar B V, Kamble A D, Sonawane K D.Conformational preferences of modified nucleoside N(4)-acetylcytidine,ac4C occur at"wobble"34th position in the anticodon loop of tRNA[J]. Cell Biochem Biophys,2013,66(3):797-816.
- [59]Ito S,Akamatsu Y,Noma A,Kimura S,Miyauchi K,Ikeuchi Y,Suzuki T,Suzuki T. A single acetylation of18 S rRNA is essential for biogenesis of the small ribosomal subunit in Saccharomyces cerevisiae[J]. J Biol Chem,2014,289(38):26201-26212.
- [60]Johansson M J, Bystrom A S. The Saccharomyces cerevisiae TAN1 gene is required for N4-acetylcytidine formation in tRNA[J]. RNA,2004,10(4):712-719.
- [61]Sharma S,Langhendries J L,Watzinger P,Kotter P,Entian K D,Lafontaine D L. Yeast Kre33 and human NAT10 are conserved 18S rRNA cytosine acetyltransferases that modify tRNAs assisted by the adaptor Tan1/THUMPD1[J]. Nucleic Acids Res,2015,43(4):2242-2258.
- [62]Stern L,Schulman L H. The role of the minor base N4-acetylcytidine in the function of the Escherichia coli noninitiator methionine transfer RNA[J]. J Biol Chem,1978,253(17):6132-6139.
- [63]Orita I,Futatsuishi R,Adachi K,Ohira T,Kaneko A,Minowa K, Suzuki M, Tamura T, Nakamura S,Imanaka T,Suzuki T,Fukui T. Random mutagenesis of a hyperthermophilic archaeon identified tRNA modificationsassociatedwithcellular hyperthermotolerance[J]. Nucleic Acids Res,2019,47(4):1964-1976.
- [64]Arango D,Sturgill D,Alhusaini N,Dillman A A,Sweet T J,Hanson G,Hosogane M,Sinclair W R,Nanan K K,Mandler M D,Fox S D,Zengeya T T,Andresson T,Meier J L,Coller J,Oberdoerffer S.Acetylation of cytidine in mRNA promotes translation efficiency[J]. Cell,2018,175(7):1872-1886 e1824.
- [65]Nance K D,Gamage S T,Alam M M,Yang A,Levy M J,Link C N,Florens L,Washburn M P,Gu S,Oppenheim J J,Meier J L. Cytidine acetylation yields a hypoinflammatory synthetic messenger RNA[J/OL].Cell Chem Biol,2022,29(2):312-320 e317.
- [66]Thomas J M,Bryson K M,Meier J L. Nucleotide resolution sequencing of N4-acetylcytidine in RNA[J].Methods Enzymol,2019,621:31-51.
- [67]Yang C,Wu T,Zhang J,Liu J,Zhao K,Sun W,Zhou X,Kong X,Shi J. Prognostic and immunological role of mRNA ac4C regulator NAT10 in pan-cancer:new territory for cancer research?[J]. Front Oncol,2021,11:630417.
- [68]Sharma S,Yang J,van Nues R,Watzinger P,Kotter P, Lafontaine D L J, Granneman S, Entian K D.Specialized box C/D snoRNPs act as antisense guides to target RNA base acetylation[J/OL]. PLoS Genet,2017,13(5):e1006804.
- [69]Schattner P, Barberan-Soler S, Lowe T M. A computational screen for mammalian pseudouridylation guide H/ACA RNAs[J]. RNA,2006,12(1):15-25.
- [70]Ge J,Yu Y T. RNA pseudouridylation:new insights into an old modification[J]. Trends Biochem Sci,2013,38(4):210-218.
- [71]Karijolich J,Yu Y T. Converting nonsense codons into sense codons by targeted pseudouridylation[J]. Nature,2011,474(7351):395-398.
- [72]Pereira-Montecinos C,Valiente-Echeverria F,SotoRifo R. Epitranscriptomic regulation of viral replication[J]. Biochim Biophys Acta,2017,1860(4):460-471.
- [73]Schwartz S,Bernstein D A,Mumbach M R,Jovanovic M,Herbst R H,Leon-Ricardo B X,Engreitz J M,Guttman M,Satija R,Lander E S,Fink G,Regev A.Transcriptome-wide mapping reveals widespread dynamic-regulated pseudouridylation of ncRNA and mRNA[J]. Cell,2014,159(1):148-162.
- [74]Safra M, Nir R, Farouq D, Vainberg Slutskin I,Schwartz S. TRUB1 is the predominant pseudouridine synthase acting on mammalian mRNA via a predictable and conserved code[J]. Genome Res,2017,27(3):393-406.
- [75]Carlile T M,Rojas-Duran M F,Zinshteyn B,Shin H,Bartoli K M, Gilbert W V. Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells[J]. Nature,2014,515(7525):143-146.
- [76]Smith J D,Dunn D B. An additional sugar component of ribonucleic acids[J]. Biochim Biophys Acta,1959,31(2):573-575.
- [77]Cantara W A,Crain P F,Rozenski J,McCloskey J A,Harris K A,Zhang X,Vendeix F A,Fabris D,Agris P F. The RNA modification database,RNAMDB:2011update[J]. Nucleic Acids Res, 2011, 39(Database issue):D195-201.
- [78]Ayadi L,Galvanin A,Pichot F,Marchand V,Motorin Y. RNA ribose methylation(2'-O-methylation):Occurrence, biosynthesis and biological functions[J].Biochim Biophys Acta Gene Regul Mech,2019,1862(3):253-269.
- [79]Belanger F,Stepinski J,Darzynkiewicz E,Pelletier J.Characterization of hMTr1,a human Cap1 2'-O-ribose methyltransferase[J]. J Biol Chem,2010,285(43):33037-33044.
- [80]Werner M,Purta E,Kaminska K H,Cymerman I A,Campbell D A,Mittra B,Zamudio J R,Sturm N R,Jaworski J,Bujnicki J M. 2'-O-ribose methylation of cap2 in human:function and evolution in a horizontally mobile family[J]. Nucleic Acids Res,2011,39(11):4756-4768.
- [81]Smietanski M,Werner M,Purta E,Kaminska K H,Stepinski J,Darzynkiewicz E,Nowotny M,Bujnicki J M. Structural analysis of human 2'-O-ribose methyltransferases involved in mRNA cap structure formation[J]. Nat Commun,2014,5:3004.
- [82]Dai Q, Moshitch-Moshkovitz S, Han D, Kol N,Amariglio N,Rechavi G,Dominissini D,He C. Nmseq maps 2'-O-methylation sites in human mRNA with base precision[J]. Nat Methods,2017,14(7):695-698.
- [83]Ringeard M, Marchand V, Decroly E, Motorin Y,Bennasser Y. FTSJ3 is an RNA 2'-O-methyltransferase recruited by HIV to avoid innate immune sensing[J].Nature,2019,565(7740):500-504.
- [84]Beal P A,Maydanovych O,Pokharel S. The chemistry and biology of RNA editing by adenosine deaminases[J]. Nucleic Acids Symp Ser(Oxf),2007(51):83-84.
- [85]Brandmayr C, Wagner M, Bruckl T, Globisch D,Pearson D,Kneuttinger A C,Reiter V,Hienzsch A,Koch S,Thoma I,Thumbs P,Michalakis S,Muller M,Biel M,Carell T. Isotope-based analysis of modified tRNA nucleosides correlates modification density with translational efficiency[J]. Angew Chem Int Ed Engl,2012,51(44):11162-11165.
- [86]Wetzel C,Limbach P A. Mass spectrometry of modified RNAs:recent developments[J]. Analyst,2016,141(1):16-23.
- [87]Su D,Chan C T,Gu C,Lim K S,Chionh Y H,McBee M E,Russell B S,Babu I R,Begley T J,Dedon P C. Quantitative analysis of ribonucleoside modifications in tRNA by HPLC-coupled mass spectrometry[J]. Nat Protoc,2014,9(4):828-841.
- [88]Linder B,Jaffrey S R. Discovering and Mapping the ModifiedNucleotidesThatComprisethe Epitranscriptome of mRNA[J]. Cold Spring Harb Perspect Biol,2019,11(6):a032201.
- [89]Legrand C,Tuorto F,Hartmann M,Liebers R,Jacob D,Helm M,Lyko F. Statistically robust methylation calling for whole-transcriptome bisulfite sequencing reveals distinct methylation patterns for mouse RNAs[J]. Genome Res,2017,27(9):1589-1596.
- [90]Chen K,Lu Z,Wang X,Fu Y,Luo G Z,Liu N,Han D, Dominissini D, Dai Q, Pan T, He C. Highresolution N(6)-methyladenosine(m(6)A)map using photo-crosslinking-assisted m(6)A sequencing[J].Angew Chem Int Ed Engl,2015,54(5):1587-1590.
- [91]Linder B,Grozhik A V,Olarerin-George A O,Meydan C, Mason C E, Jaffrey S R. Single-nucleotideresolution mapping of m6A and m6Am throughout the transcriptome[J]. Nat Methods,2015,12(8):767-772.
- [92]Boileau E, Dieterich C. RNA Modification Level Estimation with pulseR[J]. Genes(Basel),2018,9(12):619.
- [93]Tsai K,Jaguva Vasudevan A A,Martinez Campos C,Emery A,Swanstrom R,Cullen B R. Acetylation of cytidine residues boosts HIV-1 gene expression by increasing viral RNA stability[J/OL]. Cell Host Microbe,2020,28(2):306-312 e306.
- [94]Courtney D G,Tsai K,Bogerd H P,Kennedy E M,Law B A, Emery A, Swanstrom R, Holley C L,Cullen B R. Epitranscriptomic addition of m(5)C to HIV-1 transcripts regulates viral gene expression[J/OL].Cell Host Microbe,2019,26(2):217-227 e216.
- [95]Hussain S, Sajini A A, Blanco S, Dietmann S,Lombard P,Sugimoto Y,Paramor M,Gleeson J G,Odom D T,Ule J,Frye M. NSun2-mediated cytosine-5methylation of vault noncoding RNA determines its processing into regulatory small RNAs[J]. Cell Rep,2013,4(2):255-261.
- [96]Khoddami V,Cairns B R. Identification of direct targets and modified bases of RNA cytosine methyltransferases[J]. Nat Biotechnol,2013,31(5):458-464.
- [97]Safra M,Sas-Chen A,Nir R,Winkler R,Nachshon A,Bar-Yaacov D,Erlacher M,Rossmanith W,SternGinossar N, Schwartz S. The m1A landscape on cytosolic and mi