5,211
Views
76
CrossRef citations to date
0
Altmetric
Review

Next-generation sequencing technologies for detection of modified nucleotides in RNAs

&
Pages 1124-1137 | Received 16 Sep 2016, Accepted 18 Oct 2016, Published online: 05 Dec 2016

References

  • Lee Y, Rio DC. Mechanisms and Regulation of Alternative Pre-mRNA Splicing. Annu Rev Biochem 2015; 84:291-323; PMID:25784052; http://dx.doi.org/10.1146/annurev-biochem-060614-034316
  • Licht K, Jantsch MF. Rapid and dynamic transcriptome regulation by RNA editing and RNA modifications. J Cell Biol 2016; 213:15-22; PMID:27044895; http://dx.doi.org/10.1083/jcb.201511041
  • Wu R, Jiang D, Wang Y, Wang X. N (6)-methyladenosine (m(6)A) methylation in mRNA with A dynamic and reversible epigenetic modification. Mol Biotechnol 2016; 58:450-9; PMID:27179969; http://dx.doi.org/10.1007/s12033-016-9947-9
  • Jia G, Fu Y, He C. Reversible RNA adenosine methylation in biological regulation. Trends Genet 2013; 29:108-15; PMID:23218460; http://dx.doi.org/10.1016/j.tig.2012.11.003
  • El Yacoubi B, Bailly M, de Crécy-Lagard V. Biosynthesis and function of posttranscriptional modifications of transfer RNAs. Annu Rev Genet 2012; 46:69-95; PMID:22905870; http://dx.doi.org/10.1146/annurev-genet-110711-155641
  • Yi C, Pan T. Cellular dynamics of RNA modification. Acc Chem Res 2011; 44:1380-8; PMID:21615108; http://dx.doi.org/10.1021/ar200057m
  • Schwartz S, Bernstein DA, Mumbach MR, Jovanovic M, Herbst RH, León-Ricardo BX, Engreitz JM, Guttman M, Satija R, Lander ES, et al. Transcriptome-wide mapping reveals widespread dynamic-regulated pseudouridylation of ncRNA and mRNA. Cell 2014; 159:148-62; PMID:25219674; http://dx.doi.org/10.1016/j.cell.2014.08.028
  • Schwartz S, Agarwala SD, Mumbach MR, Jovanovic M, Mertins P, Shishkin A, Tabach Y, Mikkelsen TS, Satija R, Ruvkun G, et al. High-resolution mapping reveals a conserved, widespread, dynamic mRNA methylation program in yeast meiosis. Cell 2013; 155:1409-21; PMID:24269006; http://dx.doi.org/10.1016/j.cell.2013.10.047
  • Squires JE, Patel HR, Nousch M, Sibbritt T, Humphreys DT, Parker BJ, Suter CM, Preiss T. Widespread occurrence of 5-methylcytosine in human coding and non-coding RNA. Nucleic Acids Res 2012; 40:5023-33; PMID:22344696; http://dx.doi.org/10.1093/nar/gks144
  • Dominissini D, Moshitch-Moshkovitz S, Schwartz S, Salmon-Divon M, Ungar L, Osenberg S, Cesarkas K, Jacob-Hirsch J, Amariglio N, Kupiec M, et al. Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 2012; 485:201-6; PMID:22575960; http://dx.doi.org/10.1038/nature11112
  • Dominissini D, Nachtergaele S, Moshitch-Moshkovitz S, Peer E, Kol N, Ben-Haim MS, Dai Q, Di Segni A, Salmon-Divon M, Clark WC, et al. The dynamic N(1)-methyladenosine methylome in eukaryotic messenger RNA. Nature [ Internet] 2016; 530:441-6; PMID:26863196; http://dx.doi.org/10.1038/nature16998
  • Meyer KD, Saletore Y, Zumbo P, Elemento O, Mason CE, Jaffrey SR. Comprehensive Analysis of mRNA Methylation Reveals Enrichment in 3′ UTRs and near Stop Codons. Cell 2012; 149:1635-46; PMID:22608085; http://dx.doi.org/10.1016/j.cell.2012.05.003
  • Carlile TM, Rojas-Duran MF, Zinshteyn B, Shin H, Bartoli KM, Gilbert WV. Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells. Nature 2014; 515:143-6; PMID:25192136; http://dx.doi.org/10.1038/nature13802
  • Grosjean H, Droogmans L, Roovers M, Keith G. Detection of enzymatic activity of transfer RNA modification enzymes using radiolabeled tRNA substrates. Methods Enzymol 2007; 425:55-101; PMID:17673079; http://dx.doi.org/10.1016/S0076-6879(07)25003-7
  • Grosjean H, Keith G, Droogmans L. Detection and quantification of modified nucleotides in RNA using thin-layer chromatography. Methods Mol Biol 2004; 265:357-91; PMID:15103084; http://dx.doi.org/10.1385/1-59259-775-0:357
  • Keith G. Mobilities of modified ribonucleotides on two-dimensional cellulose thin-layer chromatography. Biochimie 1995; 77:142-4; PMID:7599271; http://dx.doi.org/10.1016/0300-9084(96)88118-1
  • Liu N, Parisien M, Dai Q, Zheng G, He C, Pan T. Probing N6-methyladenosine RNA modification status at single nucleotide resolution in mRNA and long noncoding RNA. RNA 2013; 19:1848-56; PMID:24141618; http://dx.doi.org/10.1261/rna.041178.113
  • Thüring K, Schmid K, Keller P, Helm M. Analysis of RNA modifications by liquid chromatography-tandem mass spectrometry. Methods [ Internet] 2016; 107:48-56; PMID:27020891; http://dx.doi.org/10.1016/j.ymeth.2016.03.019
  • Kellner S, Ochel A, Thüring K, Spenkuch F, Neumann J, Sharma S, Entian K-D, Schneider D, Helm M. Absolute and relative quantification of RNA modifications via biosynthetic isotopomers. Nucleic Acids Res 2014; 42:e142; PMID:25129236; http://dx.doi.org/10.1093/nar/gku733
  • Limbach PA, Paulines MJ. Going global: the new era of mapping modifications in RNA. Wiley Interdiscip Rev RNA 2016 Jun 1; PMID:27251302; http://dx.doi.org/10.1002/wrna.1367
  • Beverly MB. Applications of mass spectrometry to the study of siRNA. Mass Spectrom Rev 2011; 30:979-98; PMID:20201110; http://dx.doi.org/10.1002/mas.20260
  • Basiri B, Bartlett MG. LC-MS of oligonucleotides: applications in biomedical research. Bioanalysis 2014; 6:1525-42; PMID:25046052; http://dx.doi.org/10.4155/bio.14.94
  • Motorin Y, Muller S, Behm‐Ansmant I, Branlant C. Identification of Modified Residues in RNAs by Reverse Transcription‐Based Methods. In: Methods in Enzymology. Academic Press; 2007. page 21-53.
  • Schadt EE, Turner S, Kasarskis A. A window into third-generation sequencing. Hum Mol Genet 2010; 19:R227-40; PMID:20858600; http://dx.doi.org/10.1093/hmg/ddq416
  • Vilfan ID, Tsai YC, Clark TA, Wegener J, Dai Q, Yi C, Pan T, Turner SW, Korlach J. Analysis of RNA base modification and structural rearrangement by single-molecule real-time detection of reverse transcription. J Nanobiotechnology 2013; 11:8; PMID:23552456; http://dx.doi.org/10.1186/1477-3155-11-8
  • Saletore Y, Meyer K, Korlach J, Vilfan ID, Jaffrey S, Mason CE. The birth of the Epitranscriptome: deciphering the function of RNA modifications. Genome Biol 2012; 13:175; PMID:23113984; http://dx.doi.org/10.1186/gb-2012-13-10-175
  • Cahová H, Winz ML, Höfer K, Nübel G, Jäschke A. NAD captureSeq indicates NAD as a bacterial cap for a subset of regulatory RNAs. Nature 2015; 519:374-7; PMID:Can't; http://dx.doi.org/10.1038/nature14020
  • Hauenschild R, Tserovski L, Schmid K, Thüring K, Winz M-L, Sharma S, Entian KD, Wacheul L, Lafontaine DLJ, Anderson J, et al. The reverse transcription signature of N-1-methyladenosine in RNA-Seq is sequence dependent. Nucleic Acids Res 2015; 43:9950-64; PMID:26365242; http://dx.doi.org/10.1093/nar/gkv895
  • Birkedal U, Christensen-Dalsgaard M, Krogh N, Sabarinathan R, Gorodkin J, Nielsen H. Profiling of Ribose Methylations in RNA by High-Throughput Sequencing*. Angew Chem Int Ed Engl 2015; 54:451-5; PMID:25417815; http://dx.doi.org/10.1002/anie.201408362
  • Edelheit S, Schwartz S, Mumbach MR, Wurtzel O, Sorek R. Transcriptome-Wide Mapping of 5-methylcytidine RNA Modifications in Bacteria, Archaea, and Yeast Reveals m 5 C within Archaeal mRNAs. PLoS Genet 2013; 9:e1003602; PMID:23825970; http://dx.doi.org/10.1371/journal.pgen.1003602
  • Hussain S, Sajini AA, Blanco S, Dietmann S, Lombard P, Sugimoto Y, Paramor M, Gleeson JG, Odom DT, Ule J, et al. NSun2-Mediated Cytosine-5 Methylation of Vault Noncoding RNA Determines Its Processing into Regulatory Small RNAs. Cell Rep 2013; 4:255-61; PMID:23871666; http://dx.doi.org/10.1016/j.celrep.2013.06.029
  • Lovejoy AF, Riordan DP, Brown PO. Transcriptome-wide mapping of pseudouridines: pseudouridine synthases modify specific mRNAs in S. cerevisiae. PLoS One 2014; 9:e110799; PMID:25353621; http://dx.doi.org/10.1371/journal.pone.0110799
  • Li X, Zhu P, Ma S, Song J, Bai J, Sun F, Yi C. Chemical pulldown reveals dynamic pseudouridylation of the mammalian transcriptome. Nat Chem Biol 2015; 11:592-7; PMID:26075521; http://dx.doi.org/10.1038/nchembio.1836
  • Marchand V, Blanloeil-Oillo F, Helm M, Motorin Y. Illumina-based RiboMethSeq approach for mapping of 2′-O-Me residues in RNA. Nucleic Acids Res [ Internet] 2016; 44:e135
  • Li X, Xiong X, Wang K, Wang L, Shu X, Ma S, Yi C. Transcriptome-wide mapping reveals reversible and dynamic N1-methyladenosine methylome. Nat Chem Biol [ Internet] 2016 [cited 2016 Feb 15]; 12:311-6
  • Khoddami V, Cairns BR. Identification of direct targets and modified bases of RNA cytosine methyltransferases. Nat Biotechnol 2013; 31:458-64; PMID:23604283; http://dx.doi.org/10.1038/nbt.2566
  • Haag S, Warda AS, Kretschmer J, Günnigmann MA, Höbartner C, Bohnsack MT. NSUN6 is a human RNA methyltransferase that catalyzes formation of m5C72 in specific tRNAs. RNA 2015; 21:1532-43; PMID:26160102; http://dx.doi.org/10.1261/rna.051524.115
  • Khoddami V, Cairns BR. Transcriptome-wide target profiling of RNA cytosine methyltransferases using the mechanism-based enrichment procedure Aza-IP. Nat Protoc 2014; 9:337-61; PMID:24434802; http://dx.doi.org/10.1038/nprot.2014.014
  • Levanon EY, Eisenberg E, Yelin R, Nemzer S, Hallegger M, Shemesh R, Fligelman ZY, Shoshan A, Pollock SR, Sztybel D, et al. Systematic identification of abundant A-to-I editing sites in the human transcriptome. Nat Biotechnol 2004; 22:1001-5; PMID:15258596; http://dx.doi.org/10.1038/nbt996
  • Ryvkin P, Leung YY, Silverman IM, Childress M, Valladares O, Dragomir I, Gregory BD, Wang L-S. HAMR: high-throughput annotation of modified ribonucleotides. RNA 2013; 19:1684-92; PMID:24149843; http://dx.doi.org/10.1261/rna.036806.112
  • Bakin AV, Ofengand J. Mapping of pseudouridine residues in RNA to nucleotide resolution. Methods Mol Biol 1998; 77:297-309; PMID:9770678
  • Ofengand J, Bakin A. Mapping to nucleotide resolution of pseudouridine residues in large subunit ribosomal RNAs from representative eukaryotes, prokaryotes, archaebacteria, mitochondria and chloroplasts. J Mol Biol 1997; 266:246-68; PMID:9047361; http://dx.doi.org/10.1006/jmbi.1996.0737
  • Schaefer M, Pollex T, Hanna K, Lyko F. RNA cytosine methylation analysis by bisulfite sequencing. Nucleic Acids Res 2009; 37:e12; PMID:19059995; http://dx.doi.org/10.1093/nar/gkn954
  • 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 NSun2 promotes tRNA stability and protein synthesis. Nat Struct Mol Biol 2012; 19:900-5; PMID:22885326; http://dx.doi.org/10.1038/nsmb.2357
  • Gigova A, Duggimpudi S, Pollex T, Schaefer M, Koš M. A cluster of methylations in the domain IV of 25S rRNA is required for ribosome stability. RNA 2014; 20:1632-44; PMID:25125595; http://dx.doi.org/10.1261/rna.043398.113
  • Bourgeois G, Ney M, Gaspar I, Aigueperse C, Schaefer M, Kellner S, Helm M, Motorin Y. Eukaryotic rRNA modification by yeast 5-methylcytosine-methyltransferases and human proliferation-associated antigen p120. PLoS One 2015; 10:e0133321; PMID:26196125; http://dx.doi.org/10.1371/journal.pone.0133321
  • Maden BE. Mapping 2′-O-methyl groups in ribosomal RNA. Methods 2001; 25:374-82; PMID:11860292; http://dx.doi.org/10.1006/meth.2001.1250
  • Jorjani H, Kehr S, Jedlinski DJ, Gumienny R, Hertel J, Stadler PF, Zavolan M, Gruber AR. An updated human snoRNAome. Nucleic Acids Res 2016; 44:5068-82; PMID:27174936; http://dx.doi.org/10.1093/nar/gkw386
  • Incarnato D, Anselmi F, Morandi E, Neri F, Maldotti M, Rapelli S, Parlato C, Basile G, Oliviero S. High-throughput single-base resolution mapping of RNA 2′-O-methylated residues. Nucleic Acids Res [ Internet] 2016; Available from: http://nar.oxfordjournals.org/content/early/2016/09/09/nar.gkw810.abstract; PMID:27614074
  • Sakurai M, Yano T, Kawabata H, Ueda H, Suzuki T. Inosine cyanoethylation identifies A-to-I RNA editing sites in the human transcriptome. Nat Chem Biol 2010; 6:733-40; PMID:20835228; http://dx.doi.org/10.1038/nchembio.434
  • Suzuki T, Ueda H, Okada S, Sakurai M. Transcriptome-wide identification of adenosine-to-inosine editing using the ICE-seq method. Nat Protoc 2015; 10:715-32; PMID:25855956; http://dx.doi.org/10.1038/nprot.2015.037
  • Sakurai M, Ueda H, Yano T, Okada S, Terajima H, Mitsuyama T, Toyoda A, Fujiyama A, Kawabata H, Suzuki T. A biochemical landscape of A-to-I RNA editing in the human brain transcriptome. Genome Res 2014; 24:522-34; PMID:24407955; http://dx.doi.org/10.1101/gr.162537.113
  • Linder B, Grozhik AV, Olarerin-George AO, Meydan C, Mason CE, Jaffrey SR. Single-nucleotide-resolution mapping of m6A and m6Am throughout the transcriptome. Nat Methods [ Internet] 2015; 12:767-72; PMID:26121403; http://dx.doi.org/10.1038/nmeth.3453
  • Chen K, Lu Z, Wang X, Fu Y, Luo GZ, Liu N, Han D, Dominissini D, Dai Q, Pan T, et al. High-resolution N(6) -methyladenosine (m(6) A) map using photo-crosslinking-assisted m(6) A sequencing. Angew Chem Int Ed Engl 2015; 54:1587-90; PMID:25491922; http://dx.doi.org/10.1002/anie.201410647
  • Uren PJ, Bahrami-Samani E, Burns SC, Qiao M, Karginov FV, Hodges E, Hannon GJ, Sanford JR, Penalva LOF, Smith AD. Site identification in high-throughput RNA–protein interaction data. Bioinformatics 2012; 28:3013-20; PMID:23024010; http://dx.doi.org/10.1093/bioinformatics/bts569
  • Corcoran DL, Georgiev S, Mukherjee N, Gottwein E, Skalsky RL, Keene JD, Ohler U. PARalyzer: definition of RNA binding sites from PAR-CLIP short-read sequence data. Genome Biol 2011; 12:R79; PMID:21851591; http://dx.doi.org/10.1186/gb-2011-12-8-r79
  • Sievers C, Schlumpf T, Sawarkar R, Comoglio F, Paro R. Mixture models and wavelet transforms reveal high confidence RNA-protein interaction sites in MOV10 PAR-CLIP data. Nucleic Acids Res 2012; 40:e160; PMID:22844102; http://dx.doi.org/10.1093/nar/gks697
  • Li B, Tambe A, Aviran S, Pachter L. Prober: A general toolkit for analyzing sequencing-based “toeprinting” assays [Internet]. 2016. Available from: http://biorxiv.org/lookup/doi/10.1101/063107
  • Cui X, Meng J, Zhang S, Chen Y, Huang Y. A novel algorithm for calling mRNA m6A peaks by modeling biological variances in MeRIP-seq data. Bioinformatics 2016; 32:i378-85; PMID:27307641; http://dx.doi.org/10.1093/bioinformatics/btw281
  • Molinie B, Wang J, Lim KS, Hillebrand R, Lu ZX, Van Wittenberghe N, Howard BD, Daneshvar K, Mullen AC, Dedon P, et al. m(6)A-LAIC-seq reveals the census and complexity of the m(6)A epitranscriptome. Nat Methods 2016; 13:692-8; PMID:27376769; http://dx.doi.org/10.1038/nmeth.3898
  • Li M, Wang IX, Li Y, Bruzel A, Richards AL, Toung JM, Cheung VG. Widespread RNA and DNA sequence differences in the human transcriptome. Science 2011; 333:53-8; PMID:21596952; http://dx.doi.org/10.1126/science.1207018
  • Pickrell JK, Gilad Y, Pritchard JK. Comment on “Widespread RNA and DNA sequence differences in the human transcriptome.” Science 2012; 335:1302; author reply 1302; PMID:22422963; http://dx.doi.org/10.1126/science.1210484
  • Kleinman CL, Majewski J. Comment on “Widespread RNA and DNA sequence differences in the human transcriptome.” Science 2012; 335:1302; author reply 1302; PMID:22422962; http://dx.doi.org/10.1126/science.1209658
  • Lin W, Piskol R, Tan MH, Li JB. Comment on “Widespread RNA and DNA sequence differences in the human transcriptome.” Science 2012; 335:1302; author reply 1302; PMID:22422964; http://dx.doi.org/10.1126/science.1210624