Mapping the epigenetic modifications of DNA and RNA

Lin-Yong Zhao, Jinghui Song, Yibin Liu, Chun-Xiao Song, Chengqi Yi

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Protein Cell ›› 2020, Vol. 11 ›› Issue (11) : 792-808. DOI: 10.1007/s13238-020-00733-7
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Mapping the epigenetic modifications of DNA and RNA

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Abstract

Over 17 and 160 types of chemical modifications have been identified in DNA and RNA, respectively. The interest in understanding the various biological functions of DNA and RNA modifications has lead to the cutting-edged fields of epigenomics and epitranscriptomics. Developing chemical and biological tools to detect specific modifications in the genome or transcriptome has greatly facilitated their study. Here, we review the recent technological advances in this rapidly evolving field. We focus on high-throughput detection methods and biological findings for these modifications, and discuss questions to be addressed as well. We also summarize third-generation sequencing methods, which enable long-read and single-molecule sequencing of DNA and RNA modification.

Keywords

DNA modification / DNA methylation / RNA modification / epitranscriptomics / epigenetics / long read sequencing

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Lin-Yong Zhao, Jinghui Song, Yibin Liu, Chun-Xiao Song, Chengqi Yi. Mapping the epigenetic modifications of DNA and RNA. Protein Cell, 2020, 11(11): 792‒808 https://doi.org/10.1007/s13238-020-00733-7

References

[1]
Adey A, Shendure J (2012) Ultra-low-input, tagmentation-based whole-genome bisulfite sequencing. Genome Res 22:1139–1143
CrossRef Google scholar
[2]
Akichika S, Hirano S, Shichino Y, Suzuki T, Nishimasu H, Ishitani R, Sugita A, Hirose Y, Iwasaki S, Nureki O (2019) Cap-specific terminal N (6)-methylation of RNA by an RNA polymerase IIassociated methyltransferase. Science (New York, NY).https://doi.org/10.1126/science.aav0080
CrossRef Google scholar
[3]
Alarcon CR, Goodarzi H, Lee H, Liu X, Tavazoie S,Tavazoie SF (2015) HNRNPA2B1 is a mediator of m(6)A-dependent nuclear RNA processing events. Cell 162:1299–1308
CrossRef Google scholar
[4]
Arango D,Sturgill D, Alhusaini N, Dillman AA, Sweet TJ, Hanson G, Hosogane M, Sinclair WR, Nanan KK, Mandler MD (2018) Acetylation of cytidine in mRNA promotes translation efficiency. Cell 175:1872–1886.e1824
CrossRef Google scholar
[5]
Ardui S, Ameur A, Vermeesch JR, Hestand MS (2018) Single molecule real-time (SMRT) sequencing comes of age: applications and utilities for medical diagnostics. Nucleic Acids Res 46:2159–2168
CrossRef Google scholar
[6]
Bartosovic M, Molares HC, Gregorova P, Hrossova D, Kudla G, Vanacova S (2017) N6-methyladenosine demethylase FTO targets pre-mRNAs and regulates alternative splicing and 3′-end processing. Nucleic Acids Res 45:11356–11370
CrossRef Google scholar
[7]
Boccaletto P, Machnicka MA, Purta E, Piatkowski P, Baginski B, Wirecki TK, de Crecy-Lagard V,Ross R, Limbach PA, Kotter A (2018) MODOMICS: a database of RNA modification pathways. 2017 update. Nucleic Acids Res 46:D303–d307
CrossRef Google scholar
[8]
Bokar JA, Rath-Shambaugh ME, Ludwiczak R, Narayan P, Rottman F (1994) Characterization and partial purification of mRNA N6-adenosine methyltransferase from HeLa cell nuclei. Internal mRNA methylation requires a multisubunit complex. J Biol Chem 269:17697–17704
[9]
Booth MJ, Branco MR, Ficz G, Oxley D, Krueger F, Reik W,Balasubramanian S (2012) Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution. Science (New York, NY) 336:934–937
CrossRef Google scholar
[10]
Booth MJ, Ost TW, Beraldi D, Bell NM, Branco MR, Reik W, Balasubramanian S (2013) Oxidative bisulfite sequencing of 5-methylcytosine and 5-hydroxymethylcytosine. Nat Protoc 8:1841–1851
CrossRef Google scholar
[11]
Booth MJ, Marsico G, Bachman M, Beraldi D, Balasubramanian S (2014) Quantitative sequencing of 5-formylcytosine in DNA at single-base resolution. Nat Chem 6:435–440
CrossRef Google scholar
[12]
Booth MJ, Raiber EA, Balasubramanian S (2015) Chemical methods for decoding cytosine modifications in DNA. Chem Rev 115:2240–2254
CrossRef Google scholar
[13]
Boulias K, Toczydlowska-Socha D,Hawley BR, Liberman N, Takashima K, Zaccara S, Guez T, Vasseur JJ, Debart F, Aravind L (2019) Identification of the m(6)Am methyltransferase PCIF1 reveals the location and functions of m(6)Am in the transcriptome. Mol Cell 75(3):631.e8–643.e8
CrossRef Google scholar
[14]
Cao G, Li HB (2016) Recent advances in dynamic m6A RNA modification. Open Biol 6:160003
CrossRef Google scholar
[15]
Carlile TM, Rojas-Duran MF, Zinshteyn B, Shin H, Bartoli KM, Gilbert WV (2014) Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells. Nature 515:143–146
CrossRef Google scholar
[16]
Chen K, Lu Z, Wang X, Fu Y, Luo GZ, Liu N, Han D, Dominissini D, Dai Q, Pan T(2015) High-resolution N(6) -methyladenosine (m(6) A) map using photo-crosslinking-assisted m(6) A sequencing. Angew Chem Int Ed Engl 54:1587–1590
CrossRef Google scholar
[17]
Chen X, Li A, Sun BF, Yang Y, Han YN, Yuan X, Chen RX, Wei WS, Liu Y, Gao CC(2019) 5-methylcytosine promotes pathogenesis of bladder cancer through stabilizing mRNAs. Nat Cell Biol 21(8):978–990
CrossRef Google scholar
[18]
Chu JM, Ye TT, Ma CJ, Lan MD, Liu T, Yuan BF, Feng YQ (2018) Existence of Internal N7-methylguanosine modification in mRNA determined by differential enzyme treatment coupled with mass spectrometry analysis. ACS Chem Biol 13:3243–3250
CrossRef Google scholar
[19]
Clark SJ, Smallwood SA, Lee HJ, Krueger F, Reik W, Kelsey G (2017) Genome-wide base-resolution mapping of DNA methylation in single cells using single-cell bisulfite sequencing (scBS-seq). Nat Protoc 12:534–547
CrossRef Google scholar
[20]
Clarke J, Wu HC, Jayasinghe L,Patel A, Reid S, Bayley H (2009) Continuous base identification for single-molecule nanopore DNA sequencing. Nat Nanotechnol 4:265–270
CrossRef Google scholar
[21]
Courtney DG, Kennedy EM, Dumm RE, Bogerd HP, Tsai K, Heaton NS, Cullen BR (2017) Epitranscriptomic enhancement of influenza A virus gene expression and replication. Cell Host Microbe 22:377–386.e375
CrossRef Google scholar
[22]
Cui Q, Shi H, Ye P,Li L, Qu Q, Sun G,Sun G, Lu Z, Huang Y, Yang CG (2017a) m(6)A RNA methylation regulates the selfrenewal and tumorigenesis of glioblastoma stem cells. Cell Rep 18:2622–2634
CrossRef Google scholar
[23]
Cui X, Liang Z, Shen L, Zhang Q, Bao S,Geng Y,Zhang B, Leo V, Vardy LA, Lu T (2017b) 5-Methylcytosine RNA methylation in Arabidopsis thaliana. Molecular plant 10:1387–1399
CrossRef Google scholar
[24]
Delatte B, Wang F, Ngoc LV, Collignon E, Bonvin E, Deplus R, Calonne E, Hassabi B, Putmans P, Awe S (2016) RNA biochemistry. Transcriptome-wide distribution and function of RNA hydroxymethylcytosine. Science (New York, NY) 351:282–285
CrossRef Google scholar
[25]
Dominissini D, Moshitch-Moshkovitz S, Schwartz S, Salmon-Divon M, Ungar L, Osenberg S, Cesarkas K, Jacob-Hirsch J, Amariglio N, Kupiec M (2012) Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 485:201–206
CrossRef Google scholar
[26]
Dominissini D, Nachtergaele S, Moshitch-Moshkovitz S, Peer E, Kol N, Ben-Haim MS, Dai Q, Di Segni A, Salmon-Divon M, Clark WC (2016) The dynamic N(1)-methyladenosine methylome in eukaryotic messenger RNA. Nature 530:441–446
CrossRef Google scholar
[27]
Dong C, Niu L, Song W, Xiong X, Zhang X, Zhang Z, Yang Y, Yi F, Zhan J, Zhang H (2016) tRNA modification profiles of the fast-proliferating cancer cells. Biochem Biophys Res Commun 476:340–345
CrossRef Google scholar
[28]
Douvlataniotis K, Bensberg M, Lentini A, Gylemo B, Nestor CE (2020) No evidence for DNA N (6)-methyladenine in mammals. Sci Adv 6:eaay3335
CrossRef Google scholar
[29]
Dubin DT, Taylor RH (1975) The methylation state of poly A-containing messenger RNA from cultured hamster cells. Nucleic Acids Res 2:1653–1668
CrossRef Google scholar
[30]
Edelheit S, Schwartz S, Mumbach MR, Wurtzel O, Sorek R (2013) Transcriptome-wide mapping of 5-methylcytidine RNA modifications in bacteria, archaea, and yeast reveals m5C within archaeal mRNAs. PLoS Genet 9:e1003602
CrossRef Google scholar
[31]
Ficz G, Branco MR, Seisenberger S, Santos F, Krueger F, Hore TA, Marques CJ, Andrews S, Reik W (2011) Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 473:398–402
CrossRef Google scholar
[32]
Flusberg BA, Webster DR, Lee JH, Travers KJ, Olivares EC, Clark TA, Korlach J, Turner SW (2010) Direct detection of DNA methylation during single-molecule, real-time sequencing. Nat Methods 7:461–465
CrossRef Google scholar
[33]
Frye M, Jaffrey SR, Pan T, Rechavi G,Suzuki T (2016) RNA modifications: what have we learned and where are we headed? Nat Rev Genet 17:365–372
CrossRef Google scholar
[34]
Fu Y, Jia G, Pang X, Wang RN, Wang X, Li CJ, Smemo S, Dai Q, Bailey KA, Nobrega MA (2013) FTO-mediated formation of N6-hydroxymethyladenosine and N6-formyladenosine in mammalian RNA. Nat Commun 4:1798
CrossRef Google scholar
[35]
Fu L, Guerrero CR, Zhong N, Amato NJ, Liu Y, Liu S, Cai Q, Ji D, Jin SG, Niedernhofer LJ (2014) Tet-mediated formation of 5-hydroxymethylcytosine in RNA. J Am Chem Soc 136:11582–11585
CrossRef Google scholar
[36]
Fu Y, Luo GZ, Chen K, Deng X, Yu M, Han D, Hao Z, Liu J, Lu X, Dore LC (2015) N6-methyldeoxyadenosine marks active transcription start sites in Chlamydomonas. Cell 161:879–892
CrossRef Google scholar
[37]
Garalde DR, Snell EA, Jachimowicz D, Sipos B, Lloyd JH, Bruce M, Pantic N, Admassu T, James P, Warland A (2018) Highly parallel direct RNA sequencing on an array of nanopores. Nat Methods 15:201–206
CrossRef Google scholar
[38]
Garcia-Campos MA, Edelheit S, Toth U, Safra M, Shachar R, Viukov S, Winkler R, Nir R, Lasman L, Brandis A (2019) Deciphering the “m(6)A code” via antibody-independent quantitative profiling. Cell 178:731–747.e716
CrossRef Google scholar
[39]
Geula S, Moshitch-Moshkovitz S, Dominissini D, Mansour AA, Kol N, Salmon-Divon M, Hershkovitz V, Peer E, Mor N, Manor YS (2015) Stem cells. m6A mRNA methylation facilitates resolution of naive pluripotency toward differentiation. Science (New York, NY) 347:1002–1006
CrossRef Google scholar
[40]
Gilbert WV, Bell TA, Schaening C (2016) Messenger RNA modifications: form, distribution, and function. Science (New York, NY) 352:1408–1412
CrossRef Google scholar
[41]
Gokhale NS, McIntyre AB, McFadden MJ, Roder AE, Kennedy EM, Gandara JA, Hopcraft SE, Quicke KM, Vazquez C, Willer J (2016) N6-methyladenosine in flaviviridae viral RNA genomes regulates infection. Cell Host Microbe 20:654–665
CrossRef Google scholar
[42]
Greenberg MVC, Bourc’his D (2019) The diverse roles of DNA methylation in mammalian development and disease. Nat Rev Mol Cell Biol 20:590–607
CrossRef Google scholar
[43]
Greer EL, Blanco MA, Gu L, Sendinc E, Liu J, Aristizabal-Corrales D, Hsu CH, Aravind L, He C, Shi Y (2015) DNA methylation on N6-adenine in C. elegans. Cell 161:868–878
CrossRef Google scholar
[44]
Guo F, Li X, Liang D, Li T, Zhu P, Guo H, Wu X, Wen L,Gu TP, Hu B (2014) Active and passive demethylation of male and female pronuclear DNA in the mammalian zygote. Cell Stem Cell 15:447–459
CrossRef Google scholar
[45]
Hao Z, Wu T, Cui X, Zhu P, Tan C, Dou X, Hsu KW, Lin YT, Peng PH, Zhang LS (2020) N(6)-deoxyadenosine methylation in mammalian mitochondrial DNA. Mol Cell 78(3):382–395.e8
CrossRef Google scholar
[46]
Harper JE, Miceli SM, Roberts RJ, Manley JL (1990) Sequence specificity of the human mRNA N6-adenosine methylase in vitro. Nucleic Acids Res 18:5735–5741
CrossRef Google scholar
[47]
He C (2010) Grand challenge commentary: RNA epigenetics? Nat Chem Biol 6:863–865
CrossRef Google scholar
[48]
He YF, Li BZ, Li Z, Liu P, Wang Y, Tang Q, Ding J, Jia Y, Chen Z, Li L (2011) Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333:1303–1307
CrossRef Google scholar
[49]
Hussain S, Aleksic J, Blanco S, Dietmann S, Frye M (2013a) Characterizing 5-methylcytosine in the mammalian epitranscriptome. Genome Biol 14:215
CrossRef Google scholar
[50]
Hussain S, Sajini AA, Blanco S, Dietmann S, Lombard P, Sugimoto Y, Paramor M, Gleeson JG, Odom DT, Ule J (2013b) NSun2-mediated cytosine-5 methylation of vault noncoding RNA determines its processing into regulatory small RNAs. Cell Rep 4:255–261
CrossRef Google scholar
[51]
Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y (2011) Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science (New York, NY) 333:1300–1303
CrossRef Google scholar
[52]
Jain M, Olsen HE, Paten B, Akeson M (2016) The Oxford Nanopore MinION: delivery of nanopore sequencing to the genomics community. Genome Biol 17:239
CrossRef Google scholar
[53]
Jain M, Koren S, Miga KH, Quick J, Rand AC, Sasani TA, Tyson JR, Beggs AD, Dilthey AT, Fiddes IT (2018) Nanopore sequencing and assembly of a human genome with ultra-long reads. Nat Biotechnol 36:338–345
CrossRef Google scholar
[54]
Jia G, Fu Y, Zhao X, Dai Q, Zheng G, Yang Y, Yi C, Lindahl T, Pan T, Yang YG (2011) N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nat Chem Biol 7:885–887
CrossRef Google scholar
[55]
Karijolich J, Yi C, Yu YT (2015) Transcriptome-wide dynamics of RNA pseudouridylation. Nat Rev Mol Cell Biol 16:581–585
CrossRef Google scholar
[56]
Ke S, Alemu EA, Mertens C, Gantman EC, Fak JJ, Mele A, Haripal B, Zucker-Scharff I, Moore MJ, Park CY (2015) A majority of m6A residues are in the last exons, allowing the potential for 3’ UTR regulation. Genes Dev 29:2037–2053
CrossRef Google scholar
[57]
Ke S, Pandya-Jones A, Saito Y, Fak JJ, Vagbo CB, Geula S, Hanna JH, Black DL, Darnell JE Jr, Darnell RB (2017) m(6)A mRNA modifications are deposited in nascent pre-mRNA and are not required for splicing but do specify cytoplasmic turnover. Genes Dev 31:990–1006
CrossRef Google scholar
[58]
Kennedy EM, Bogerd HP, Kornepati AV, Kang D, Ghoshal D, Marshall JB, Poling BC, Tsai K, Gokhale NS, Horner SM (2016) Posttranscriptional m(6)A editing of HIV-1 mRNAs enhances viral gene expression. Cell Host Microbe 19:675–685
CrossRef Google scholar
[59]
Khoddami V, Cairns BR (2013) Identification of direct targets and modified bases of RNA cytosine methyltransferases. Nat Biotechnol 31:458–464
CrossRef Google scholar
[60]
Khoddami V, Yerra A, Mosbruger TL, Fleming AM, Burrows CJ, Cairns BR (2019) Transcriptome-wide profiling of multiple RNA modifications simultaneously at single-base resolution. Proc Natl Acad Sci USA 116:6784–6789
CrossRef Google scholar
[61]
Kobayashi H, Kono T (2012) DNA methylation analysis of germ cells by using bisulfite-based sequencing methods. Methods Mol Biol (Clifton, NJ) 825:223–235
CrossRef Google scholar
[62]
Kobayashi H, Sakurai T, Miura F,Imai M, Mochiduki K, Yanagisawa E,Sakashita A, Wakai T, Suzuki Y, Ito T (2013) Highresolution DNA methylome analysis of primordial germ cells identifies gender-specific reprogramming in mice. Genome Res 23:616–627
CrossRef Google scholar
[63]
Koch A, Joosten SC, Feng Z, de Ruijter TC, Draht MX, Melotte V, Smits KM, Veeck J, Herman JG, Van Neste L (2018) Author correction: analysis of DNA methylation in cancer: location revisited. Nat Rev Clin Oncol 15:467
CrossRef Google scholar
[64]
Kriaucionis S, Heintz N (2009) The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324:929–930
CrossRef Google scholar
[65]
Lei Z, Yi C (2017) A radiolabeling-free, qPCR-based method for locus-specific pseudouridine detection. Angew Chem Int Ed Engl 56:14878–14882
CrossRef Google scholar
[66]
Lentini A, Lagerwall C, Vikingsson S, Mjoseng HK, Douvlataniotis K, Vogt H, Green H, Meehan RR, Benson M, Nestor CE (2018) A reassessment of DNA-immunoprecipitation-based genomic profiling. Nat Methods 15:499–504
CrossRef Google scholar
[67]
Li E, Zhang Y (2014) DNA methylation in mammals. Cold Spring Harb Perspect Biol 6:a019133
CrossRef Google scholar
[68]
Li WW, Gong L, Bayley H (2013) Single-molecule detection of 5-hydroxymethylcytosine in DNA through chemical modification and nanopore analysis. Angew Chem Int Ed Engl 52:4350–4355
CrossRef Google scholar
[69]
Li X, Zhu P, Ma S, Song J, Bai J, Sun F, Yi C (2015) Chemical pulldown reveals dynamic pseudouridylation of the mammalian transcriptome. Nat Chem Biol 11:592–597
CrossRef Google scholar
[70]
Li X, Xiong X, Wang K, Wang L, Shu X, Ma S, Yi C (2016a) Transcriptome-wide mapping reveals reversible and dynamic N (1)-methyladenosine methylome. Nat Chem Biol 12:311–316
CrossRef Google scholar
[71]
Li X, Xiong X, Yi C (2016b) Epitranscriptome sequencing technologies: decoding RNA modifications. Nat Methods 14:23–31
CrossRef Google scholar
[72]
Li W, Zhang X, Lu X, You L, Song Y, Luo Z, Zhang J, Nie J, Zheng W, Xu D (2017a) 5-Hydroxymethylcytosine signatures in circulating cell-free DNA as diagnostic biomarkers for human cancers. Cell Res 27:1243–1257
CrossRef Google scholar
[73]
Li X, Xiong X, Zhang M, Wang K, Chen Y, Zhou J, Mao Y, Lv J, Yi D, Chen XW(2017b) Base-resolution mapping reveals distinct m(1)A methylome in nuclear- and mitochondrial-encoded transcripts. Mol Cell 68:993–1005.e1009
CrossRef Google scholar
[74]
Li Z, Weng H, Su R, Weng X, Zuo Z,Li C, Huang H, Nachtergaele S, Dong L, Hu C (2017c) FTO plays an oncogenic role in acute myeloid leukemia as a N(6)-methyladenosine RNA demethylase. Cancer Cell 31:127–141
CrossRef Google scholar
[75]
Li QY, Xie NB, Xiong J, Yuan BF, Feng YQ (2018) Single-nucleotide resolution analysis of 5-hydroxymethylcytosine in DNA by enzyme-mediated deamination in combination with sequencing. Anal Chem 90:14622–14628
CrossRef Google scholar
[76]
Lichinchi G, Gao S, Saletore Y, Gonzalez GM (2016a) Dynamics of the human and viral m(6)A RNA methylomes during HIV-1 infection of T cells. Nat Microbiol 1:16011
CrossRef Google scholar
[77]
Lichinchi G, Zhao BS, Wu Y, Lu Z, Qin Y, He C, Rana TM (2016b) Dynamics of human and viral RNA methylation during Zika virus infection. Cell Host Microbe 20:666–673
CrossRef Google scholar
[78]
Lin S, Liu Q, Lelyveld VS, Choe J, Szostak JW, Gregory RI (2018) Mettl1/Wdr4-mediated m(7)G tRNA methylome is required for normal mRNA translation and embryonic stem cell self-renewal and differentiation. Mol Cell 71:244–255.e245
CrossRef Google scholar
[79]
Linder B, Grozhik AV, Olarerin-George AO, Meydan C, Mason CE, Jaffrey SR (2015) Single-nucleotide-resolution mapping of m6A and m6Am throughout the transcriptome. Nat Methods 12:767–772
CrossRef Google scholar
[80]
Liu J, Yue Y, Han D, Wang X, Fu Y, Zhang L, Jia G, Yu M, Lu Z, Deng X (2014) A METTL3-METTL14 complex mediates mammalian nuclear RNA N6-adenosine methylation. Nat Chem Biol 10:93–95
CrossRef Google scholar
[81]
Liu N, Dai Q, Zheng G, He C, Parisien M, Pan T (2015) N(6)-methyladenosine-dependent RNA structural switches regulate RNA-protein interactions. Nature 518:560–564
CrossRef Google scholar
[82]
Liu F, Clark W, Luo G, Wang X, Fu Y,Wei J,Wang X, Hao Z, Dai Q, Zheng G (2016) ALKBH1-mediated tRNA demethylation regulates translation. Cell 167(3):816–828
CrossRef Google scholar
[83]
Liu N, Zhou KI, Parisien M, Dai Q, Diatchenko L, Pan T (2017) N6-methyladenosine alters RNA structure to regulate binding of a low-complexity protein. Nucleic Acids Res 45:6051–6063
CrossRef Google scholar
[84]
Liu H, Begik O, Lucas MC, Ramirez JM, Mason CE, Wiener D, Schwartz S, Mattick JS, Smith MA, Novoa EM (2019a) Accurate detection of m6A RNA modifications in native RNA sequences. Nat Commun 10:4079
CrossRef Google scholar
[85]
Liu J, Harada BT, He C (2019b) Regulation of gene expression by N (6)-methyladenosine in cancer. Trends Cell Biol 29(6):487–489
CrossRef Google scholar
[86]
Liu J, Li K, Cai J, Zhang M, Zhang X, Xiong X, Meng H, Xu X, Huang Z, Peng J(2019c) Landscape and regulation of m(6)A and m (6)Am methylome across human and mouse tissues. Mol Cell 77 (2):426.e6–440.e6
CrossRef Google scholar
[87]
Liu Y, You Y, Lu Z, Yang J, Li P,Liu L, Xu H, Niu Y, Cao X (2019d) N (6)-methyladenosine RNA modification-mediated cellular metabolism rewiring inhibits viral replication. Science (New York, NY) 365:1171–1176
CrossRef Google scholar
[88]
Liu Y, Cheng J, Siejka-Zielinska P, Weldon C, Roberts H, Lopopolo M, Magri A, D’Arienzo V, Harris JM, McKeating JA (2020) Accurate targeted long-read DNA methylation and hydroxymethylation sequencing with TAPS. Genome Biol 21:54
CrossRef Google scholar
[89]
Louloupi A, Ntini E, Conrad T, Orom UAV (2018) Transient N-6-methyladenosine transcriptome sequencing reveals a regulatory role of m6A in splicing efficiency. Cell Rep 23:3429–3437
CrossRef Google scholar
[90]
Lovejoy AF, Riordan DP, Brown PO (2014) Transcriptome-wide mapping of pseudouridines: pseudouridine synthases modify specific mRNAs in S. cerevisiae. PLoS ONE 9:e110799
CrossRef Google scholar
[91]
Lu X, Song CX, Szulwach K, Wang Z, Weidenbacher P, Jin P, He C (2013) Chemical modification-assisted bisulfite sequencing (CAB-Seq) for 5-carboxylcytosine detection in DNA. J Am Chem Soc 135:9315–9317
CrossRef Google scholar
[92]
Lu X, Han D, Zhao BS, Song CX, Zhang LS, Dore LC, He C(2015) Base-resolution maps of 5-formylcytosine and 5-carboxylcytosine reveal genome-wide DNA demethylation dynamics. Cell Res 25:386–389
CrossRef Google scholar
[93]
Lu W, Tirumuru N, St Gelais C, Koneru PC, Liu C, Kvaratskhelia M, He C, Wu L (2018) N(6)-methyladenosine-binding proteins suppress HIV-1 infectivity and viral production. J Biol Chem 293:12992–13005
CrossRef Google scholar
[94]
Malbec L, Zhang T, Chen YS, Zhang Y, Sun BF, Shi BY, Zhao YL, Yang Y,Yang YG (2019) Dynamic methylome of internal mRNA N (7)-methylguanosine and its regulatory role in translation. Cell Res.https://doi.org/10.1016/j.molp.2019.12.007
CrossRef Google scholar
[95]
Mauer J, Luo X, Blanjoie A, Jiao X, Grozhik AV, Patil DP, Linder B, Pickering BF, Vasseur JJ, Chen Q (2017) Reversible methylation of m(6)Am in the 5′ cap controls mRNA stability. Nature 541:371–375
CrossRef Google scholar
[96]
Meyer KD (2019) DART-seq: an antibody-free method for global m (6)A detection. Nat Methods 16:1275–1280
CrossRef Google scholar
[97]
Meyer KD, Saletore Y, Zumbo P, Elemento O, Mason CE, Jaffrey SR (2012) Comprehensive analysis of mRNA methylation reveals enrichment in 3’ UTRs and near stop codons. Cell 149:1635–1646
CrossRef Google scholar
[98]
Molinie B, Wang J, Lim KS, Hillebrand R, Lu ZX (2016) m(6)A-LAICseq reveals the census and complexity of the m(6)A epitranscriptome. Nat Methods 13:692–698
CrossRef Google scholar
[99]
Musheev MU, Baumgärtner A, Krebs L, Niehrs C (2020) The origin of genomic N6-methyl-deoxyadenosine in mammalian cells. Nat Chem Biol.https://doi.org/10.1038/s41589-020-0504-2
CrossRef Google scholar
[100]
Neri F,Incarnato D, Krepelova A, Rapelli S, Anselmi F,Parlato C, Medana C, Dal Bello F, Oliviero S (2015) Single-base resolution analysis of 5-formyl and 5-carboxyl cytosine reveals promoter DNA methylation dynamics. Cell Rep 10:674–683
CrossRef Google scholar
[101]
O’Brown ZK, Boulias K, Wang J, Wang SY, O’Brown NM, Hao Z, Shibuya H, Fady PE, Shi Y, He C (2019) Sources of artifact in measurements of 6mA and 4mC abundance in eukaryotic genomic DNA. BMC Genom 20:445
CrossRef Google scholar
[102]
Patil DP, Chen CK, Pickering BF, Chow A, Jackson C, Guttman M, Jaffrey SR (2016) m(6)A RNA methylation promotes XISTmediated transcriptional repression. Nature 537:369–373
CrossRef Google scholar
[103]
Pendleton KE, Chen B, Liu K, Hunter OV, Xie Y, Tu BP, Conrad NK (2017) The U6 snRNA m(6)A methyltransferase METTL16 regulates SAM synthetase intron retention. Cell 169:824–835. e814
CrossRef Google scholar
[104]
Pfaffeneder T, Hackner B, Truss M, Munzel M, Muller M, Deiml CA, Hagemeier C, Carell T (2011) The discovery of 5-formylcytosine in embryonic stem cell DNA. Angew Chem 50:7008–7012
CrossRef Google scholar
[105]
Ping XL, Sun BF, Wang L, Xiao W, Yang X,Wang WJ, Adhikari S, Shi Y, Lv Y, Chen YS (2014) Mammalian WTAP is a regulatory subunit of the RNA N6-methyladenosine methyltransferase. Cell Res 24:177–189
CrossRef Google scholar
[106]
Raiber E-A, Hardisty R, van Delft P,Balasubramanian S (2017) Mapping and elucidating the function of modified bases in DNA. Nat Rev Chem 1:0069
CrossRef Google scholar
[107]
Rand AC, Jain M, Eizenga JM, Musselman-Brown A, Olsen HE, Akeson M, Paten B (2017) Mapping DNA methylation with highthroughput nanopore sequencing. Nat Methods 14:411–413
CrossRef Google scholar
[108]
Roundtree IA, Evans ME, Pan T,He C (2017) Dynamic RNA modifications in gene expression regulation. Cell 169:1187–1200
CrossRef Google scholar
[109]
Safra M, Sas-Chen A, Nir R, Winkler R, Nachshon A, Bar-Yaacov D, Erlacher M, Rossmanith W, Stern-Ginossar N, Schwartz S (2017) The m1A landscape on cytosolic and mitochondrial mRNA at single-base resolution. Nature 551:251–255
CrossRef Google scholar
[110]
Schaefer M, Pollex T, Hanna K, Lyko F (2009) RNA cytosine methylation analysis by bisulfite sequencing. Nucleic Acids Res 37:e12
CrossRef Google scholar
[111]
Schutsky EK, DeNizio JE, Hu P, Liu MY, Nabel CS, Fabyanic EB, Hwang Y, Bushman FD, Wu H, Kohli RM (2018) Nondestructive, base-resolution sequencing of 5-hydroxymethylcytosine using a DNA deaminase. Nat Biotechnol.https://doi.org/10.1038/nbt.4204
CrossRef Google scholar
[112]
Schwartz S, Agarwala SD, Mumbach MR, Jovanovic M, Mertins P, Shishkin A, Tabach Y,Mikkelsen TS, Satija R, Ruvkun G (2013) High-resolution mapping reveals a conserved, widespread, dynamic mRNA methylation program in yeast meiosis. Cell 155:1409–1421
CrossRef Google scholar
[113]
Schwartz S, Bernstein DA, Mumbach MR, Jovanovic M, Herbst RH, Leon-Ricardo BX, Engreitz JM, Guttman M, Satija R, Lander ES (2014a) Transcriptome-wide mapping reveals widespread dynamic-regulated pseudouridylation of ncRNA and mRNA. Cell 159:148–162
CrossRef Google scholar
[114]
Schwartz S, Mumbach Maxwell R, Jovanovic M, Wang T, Maciag K, Bushkin GG, Mertins P, Ter-Ovanesyan D, Habib N, Cacchiarelli D (2014b) Perturbation of m6A writers reveals two distinct classes of mRNA methylation at internal and 5′ sites. Cell Rep 8:284–296
CrossRef Google scholar
[115]
Sendinc E, Valle-Garcia D, Dhall A, Chen H, Henriques T, Navarrete-Perea J, Sheng W, Gygi SP, Adelman K, Shi Y (2019) PCIF1 catalyzes m6Am mRNA methylation to regulate gene expression. Mol Cell 75(3):620.e9–630.e9
CrossRef Google scholar
[116]
Shafik A, Schumann U, Evers M, Sibbritt T, Preiss T (2016) The emerging epitranscriptomics of long noncoding RNAs. Biochim Biophys Acta 1859:59–70
CrossRef Google scholar
[117]
Shen L, Wu H, Diep D, Yamaguchi S, D’Alessio AC, Fung HL, Zhang K, Zhang Y (2013) Genome-wide analysis reveals TET- and TDG-dependent 5-methylcytosine oxidation dynamics. Cell 153:692–706
CrossRef Google scholar
[118]
Shen Q, Zhang Q, Shi Y,Shi Q, Jiang Y, Gu Y, Li Z, Li X, Zhao K, Wang C (2018) Tet2 promotes pathogen infection-induced myelopoiesis through mRNA oxidation. Nature 554:123–127
CrossRef Google scholar
[119]
Shirane K, Toh H, Kobayashi H, Miura F, Chiba H, Ito T, Kono T, Sasaki H (2013) Mouse oocyte methylomes at base resolution reveal genome-wide accumulation of non-CpG methylation and role of DNA methyltransferases. PLoS Genet 9:e1003439
CrossRef Google scholar
[120]
Shu X, Cao J, Cheng M, Xiang S, Gao M, Li T, Ying X, Wang F, Yue Y, Lu Z (2020) A metabolic labeling method detects m6A transcriptome-wide at single base resolution. Nat Chem Biol. https://doi.org/10.1038/s41589-020-0526-9
CrossRef Google scholar
[121]
Simpson JT, Workman RE, Zuzarte PC, David M, Dursi LJ, Timp W (2017) Detecting DNA cytosine methylation using nanopore sequencing. Nat Methods 14:407–410
CrossRef Google scholar
[122]
Smallwood SA, Lee HJ, Angermueller C,Krueger F, Saadeh H, Peat J, Andrews SR, Stegle O, Reik W, Kelsey G (2014) Single-cell genome-wide bisulfite sequencing for assessing epigenetic heterogeneity. Nat Methods 11:817–820
CrossRef Google scholar
[123]
Smith AM, Jain M, Mulroney L, Garalde DR, Akeson M (2019) Reading canonical and modified nucleobases in 16S ribosomal RNA using nanopore native RNA sequencing. PLoS ONE 14: e0216709
CrossRef Google scholar
[124]
Song J, Yi C (2019) Reading chemical modifications in the transcriptome. J Mol Biol.https://doi.org/10.1016/j.jmb.2019.10.006
CrossRef Google scholar
[125]
Song CX, Clark TA, Lu XY, Kislyuk A, Dai Q, Turner SW, He C, Korlach J (2011a) Sensitive and specific single-molecule sequencing of 5-hydroxymethylcytosine. Nat Methods 9:75–77
CrossRef Google scholar
[126]
Song CX, Szulwach KE, Fu Y, Dai Q, Yi C, Li X, Li Y, Chen CH, Zhang W, Jian X (2011b) Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine. Nat Biotechnol 29:68–72
CrossRef Google scholar
[127]
Song CX, Szulwach KE, Dai Q, Fu Y, Mao SQ, Lin L, Street C, Li Y, Poidevin M, Wu H (2013) Genome-wide profiling of 5-formylcytosine reveals its roles in epigenetic priming. Cell 153:678–691
CrossRef Google scholar
[128]
Song CX, Yin S, Ma L, Wheeler A, Chen Y, Zhang Y, Liu B, Xiong J, Zhang W, Hu J (2017) 5-Hydroxymethylcytosine signatures in cell-free DNA provide information about tumor types and stages. Cell Res 27:1231–1242
CrossRef Google scholar
[129]
Song J, Zhuang Y, Zhu C,Meng H, Lu B, Xie B, Peng J, Li M, Yi C (2019) Differential roles of human PUS10 in miRNA processing and tRNA pseudouridylation. Nat Chem Biol 16(2):160–169
CrossRef Google scholar
[130]
Squires JE, Patel HR, Nousch M, Sibbritt T, Humphreys DT, Parker BJ, Suter CM, Preiss T (2012) Widespread occurrence of 5-methylcytosine in human coding and non-coding RNA. Nucleic Acids Res 40:5023–5033
CrossRef Google scholar
[131]
Stroud H, Feng S, Morey Kinney S, Pradhan S, Jacobsen SE (2011) 5-Hydroxymethylcytosine is associated with enhancers and gene bodies in human embryonic stem cells. Genome Biol 12:R54
CrossRef Google scholar
[132]
Su R, Dong L, Li C, Nachtergaele S,Wunderlich M, Qing Y, Deng X, Wang Y, Weng X, Hu C (2018) R-2HG exhibits anti-tumor activity by targeting FTO/m(6)A/MYC/CEBPA signaling. Cell 172:90–105.e123
CrossRef Google scholar
[133]
Sun H, Zhang M, Li K, Bai D, Yi C (2019) Cap-specific, terminal N(6)-methylation by a mammalian m(6)Am methyltransferase. Cell Res 29:80–82
CrossRef Google scholar
[134]
Tahiliani M, Koh KP, Shen Y,Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324:930–935
CrossRef Google scholar
[135]
Tanaka K, Okamoto A (2007) Degradation of DNA by bisulfite treatment. Bioorg Med Chem Lett 17:1912–1915
CrossRef Google scholar
[136]
Tirumuru N, Zhao BS, Lu W, Lu Z, He C, Wu L (2016) N(6)-methyladenosine of HIV-1 RNA regulates viral infection and HIV-1 Gag protein expression. Elife 5:e15528
CrossRef Google scholar
[137]
Tsai K, Courtney DG, Cullen BR (2018) Addition of m6A to SV40 late mRNAs enhances viral structural gene expression and replication. PLoS Pathog 14:e1006919
CrossRef Google scholar
[138]
Ueda Y, Ooshio I, Fusamae Y, Kitae K, Kawaguchi M, Jingushi K, Hase H, Harada K, Hirata K, Tsujikawa K (2017) AlkB homolog 3-mediated tRNA demethylation promotes protein synthesis in cancer cells. Sci Rep 7:42271
CrossRef Google scholar
[139]
Unnikrishnan A, Freeman WM, Jackson J, Wren JD, Porter H, Richardson A (2019) The role of DNA methylation in epigenetics of aging. Pharmacol Therapeut 195:172–185
CrossRef Google scholar
[140]
Vaisvila R, Ponnaluri VKC, Sun Z, Langhorst BW, Saleh L, Guan S, Dai N, Campbell MA, Sexton B, Marks K (2019) EM-seq: detection of DNA methylation at single base resolution from picograms of DNA. BioRxiv Dec 23:2019. https://doi.org/10.1101/2019.12.20.884692
CrossRef Google scholar
[141]
Venkatesan BM, Bashir R (2011) Nanopore sensors for nucleic acid analysis. Nat Nanotechnol 6:615–624
CrossRef Google scholar
[142]
Viehweger A, Krautwurst S, Lamkiewicz K, Madhugiri R, Ziebuhr J, Holzer M, Marz M (2019) Direct RNA nanopore sequencing of full-length coronavirus genomes provides novel insights into structural variants and enables modification analysis. Genome Res 29:1545–1554
CrossRef Google scholar
[143]
Vilfan ID, Tsai YC, Clark TA, Wegener J, Dai Q, Yi C, Pan T, Turner SW, Korlach J (2013) Analysis of RNA base modification and structural rearrangement by single-molecule real-time detection of reverse transcription. J Nanobiotechnol 11:8
CrossRef Google scholar
[144]
Wang Y, Li Y, Toth JI, Petroski MD, Zhang Z, Zhao JC (2014) N6- methyladenosine modification destabilizes developmental regulators in embryonic stem cells. Nat Cell Biol 16:191–198
CrossRef Google scholar
[145]
Wang L, Wen M, Cao X (2019) Nuclear hnRNPA2B1 initiates and amplifies the innate immune response to DNA viruses. Science. https://doi.org/10.1126/science.aav0758
CrossRef Google scholar
[146]
Wang Y, Xiao Y, Dong S,Yu Q,Jia G (2020) Antibody-free enzymeassisted chemical approach for detection of N6-methyladenosine. Nat Chem Biol.https://doi.org/10.1038/s41589-020-0525-x
CrossRef Google scholar
[147]
Weber M, Davies JJ, Wittig D, Oakeley EJ, Haase M, Lam WL, Schubeler D (2005) Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat Genet 37:853–862
CrossRef Google scholar
[148]
Wei J, Liu F, Lu Z, Fei Q, Ai Y, He PC, Shi H,Cui X, Su R, Klungland A (2018) Differential m(6)A, m(6)Am, and m(1)A demethylation mediated by FTO in the cell nucleus and cytoplasm. Mol Cell 71:973–985.e975
CrossRef Google scholar
[149]
Wen J, Lv R, Ma H, Shen H, He C, Wang J, Jiao F,Liu H, Yang P, Tan L (2018) Zc3h13 regulates nuclear RNA m(6)A methylation and mouse embryonic stem cell self-renewal. Mol Cell 69:1028–1038.e1026
CrossRef Google scholar
[150]
Wenger AM, Peluso P, Rowell WJ, Chang PC, Hall RJ, Concepcion GT, Ebler J, Fungtammasan A, Kolesnikov A, Olson ND (2019) Accurate circular consensus long-read sequencing improves variant detection and assembly of a human genome. Nat Biotechnol 37:1155–1162
CrossRef Google scholar
[151]
Wongsurawat T, Jenjaroenpun P, Wassenaar TM, Wadley TD, Wanchai V, Akel NS, Franco AT, Jennings ML, Ussery DW, Nookaew I (2018) Decoding the epitranscriptional landscape from native RNA sequences. bioRxiv. https://doi.org/10.1101/487819
CrossRef Google scholar
[152]
Workman RE, Tang AD, Tang PS, Jain M, Tyson JR, Razaghi R, Zuzarte PC, Gilpatrick T, Payne A,Quick J (2019) Nanopore native RNA sequencing of a human poly(A) transcriptome. Nat Methods 16:1297–1305
CrossRef Google scholar
[153]
Wu H, Wu X, Shen L, Zhang Y (2014) Single-base resolution analysis of active DNA demethylation using methylase-assisted bisulfite sequencing. Nat Biotechnol 32:1231–1240
CrossRef Google scholar
[154]
Wu H, Wu X, Zhang Y (2016) Base-resolution profiling of active DNA demethylation using MAB-seq and caMAB-seq. Nat Protoc 11:1081–1100
CrossRef Google scholar
[155]
Xia B, Han D, Lu X, Sun Z, Zhou A, Yin Q, Zeng H, Liu M, Jiang X, Xie W (2015) Bisulfite-free, base-resolution analysis of 5-formylcytosine at the genome scale. Nat Methods 12:1047–1050
CrossRef Google scholar
[156]
Xiang Y, Laurent B, Hsu CH, Nachtergaele S, Lu Z, Sheng W, Xu C, Chen H, Ouyang J, Wang S (2017) RNA m(6)A methylation regulates the ultraviolet-induced DNA damage response. Nature 543:573–576
CrossRef Google scholar
[157]
Xiao W, Adhikari S, Dahal U, Chen YS, Hao YJ, Sun BF, Sun HY, Li A, Ping XL, Lai WY (2016) Nuclear m(6)A reader YTHDC1 regulates mRNA splicing. Mol Cell 61:507–519
CrossRef Google scholar
[158]
Xiao S, Cao S, Huang Q, Xia L, Deng M, Yang M, Jia G, Liu X, Shi J, Wang W (2019) The RNA N(6)-methyladenosine modification landscape of human fetal tissues. Nat Cell Biol 21:651–661
CrossRef Google scholar
[159]
Xiong X, Li X, Wang K, Yi C (2018) Perspectives on topology of the human m(1)A methylome at single nucleotide resolution. RNA (New York, NY) 24:1437–1442
CrossRef Google scholar
[160]
Xu L, Liu X, Sheng N, Oo KS, Liang J, Chionh YH, Xu J, Ye F, Gao YG, Dedon PC(2017) Three distinct 3-methylcytidine (m(3) C) methyltransferases modify tRNA and mRNA in mice and humans. J Biol Chem 292:14695–14703
CrossRef Google scholar
[161]
Yamaguchi S, Hong K, Liu R, Shen L, Inoue A, Diep D, Zhang K, Zhang Y (2012) Tet1 controls meiosis by regulating meiotic gene expression. Nature 492:443–447
CrossRef Google scholar
[162]
Yang X, Yang Y, Sun BF, Chen YS, Xu JW, Lai WY, Li A, Wang X, Bhattarai DP, Xiao W (2017) 5-methylcytosine promotes mRNA export- NSUN2 as the methyltransferase and ALYREF as an m(5)C reader. Cell Res 27:606–625
CrossRef Google scholar
[163]
Yang Y, Wang L, Han X, Yang WL, Zhang M, Ma HL, Sun BF, Li A, Xia J, Chen J (2019) RNA 5-methylcytosine facilitates the maternal-to-zygotic transition by preventing maternal mRNA decay. Mol Cell 75:1188–1202.e1111
CrossRef Google scholar
[164]
Yu M, Hon GC, Szulwach KE, Song CX, Jin P, Ren B, He C (2012a) Tet-assisted bisulfite sequencing of 5-hydroxymethylcytosine. Nat Protoc 7:2159–2170
CrossRef Google scholar
[165]
Yu M, Hon GC, Szulwach KE, Song CX, Zhang L, Kim A, Li X, Dai Q, Shen Y, Park B(2012b) Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell 149:1368–1380
CrossRef Google scholar
[166]
Yu J, Chen M, Huang H, Zhu J, Song H, Zhu J, Park J, Ji SJ (2018) Dynamic m6A modification regulates local translation of mRNA in axons. Nucleic Acids Res 46:1412–1423
CrossRef Google scholar
[167]
Yuan F, Bi Y, Siejka-Zielinska P, Zhou YL, Zhang XX, Song CX (2019) Bisulfite-free and base-resolution analysis of 5-methylcytidine and 5-hydroxymethylcytidine in RNA with peroxotungstate. Chem Commun (Camb) 55:2328–2331
CrossRef Google scholar
[168]
Yue Y, Liu J, Cui X, Cao J, Luo G, Zhang Z, Cheng T, Gao M, Shu X, Ma H (2018) VIRMA mediates preferential m(6)A mRNA methylation in 3’UTR and near stop codon and associates with alternative polyadenylation. Cell Discov 4:10
CrossRef Google scholar
[169]
Zaringhalam M, Papavasiliou FN (2016) Pseudouridylation meets next-generation sequencing. Methods (San Diego, Calif) 107:63–72
CrossRef Google scholar
[170]
Zeng H, He B, Xia B, Bai D, Lu X, Cai J, Chen L, Zhou A, Zhu C, Meng H (2018) Bisulfite-free, nanoscale analysis of 5-hydroxymethylcytosine at single base resolution. J Am Chem Soc 140:13190–13194
CrossRef Google scholar
[171]
Zhang G, Huang H, Liu D, Cheng Y, Liu X, Zhang W, Yin R, Zhang D, Zhang P,Liu J(2015) N6-methyladenine DNA modification in Drosophila. Cell 161:893–906
CrossRef Google scholar
[172]
Zhang LS, Liu C, Ma H, Dai Q, Sun HL, Luo G, Zhang Z, Zhang L, Hu L, Dong X (2019a) Transcriptome-wide mapping of internal N(7)-methylguanosine methylome in mammalian mRNA. Mol Cell 4(6):1304.e8–1316.e8
CrossRef Google scholar
[173]
Zhang Z, Chen LQ, Zhao YL, Yang CG, Roundtree IA, Zhang Z, Ren J, Xie W, He C, Luo GZ (2019b) Single-base mapping of m(6)A by an antibody-independent method. Sci Adv 5:250
CrossRef Google scholar
[174]
Zhao X, Yang Y, Sun BF, Shi Y, Yang X, Xiao W, Hao YJ, Ping XL, Chen YS, Wang WJ (2014) FTO-dependent demethylation of N6-methyladenosine regulates mRNA splicing and is required for adipogenesis. Cell Res 24:1403–1419
CrossRef Google scholar
[175]
Zheng G, Dahl JA, Niu Y, Fedorcsak P, Huang CM, Li CJ, Vagbo CB, Shi Y, Wang WL, Song SH (2013) ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Mol Cell 49:18–29
CrossRef Google scholar
[176]
Zhou J, Wan J, Gao X, Zhang X, Jaffrey SR, Qian SB (2015) Dynamic m(6)A mRNA methylation directs translational control of heat shock response. Nature 526:591–594
CrossRef Google scholar
[177]
Zhou J, Wan J, Shu XE, Mao Y, Liu XM, Yuan X, Zhang X, Hess ME, Bruning JC, Qian SB (2018) N(6)-methyladenosine guides mRNA alternative translation during integrated stress response. Mol Cell 69:636–647.e637
CrossRef Google scholar
[178]
Zhou H, Rauch S, Dai Q, Cui X, Zhang Z, Nachtergaele S, Sepich C, He C, Dickinson BC (2019) Evolution of a reverse transcriptase to map N(1)-methyladenosine in human messenger RNA. Nat Methods 16:1281–1288
CrossRef Google scholar
[179]
Zhu C, Gao Y, Guo H, Xia B, Song J, Wu X, Zeng H, Kee K, Tang F, Yi C (2017) Single-Cell 5-formylcytosine landscapes of mammalian early embryos and ESCs at single-base resolution. Cell Stem Cell 20:720–731.e725
CrossRef Google scholar

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