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RNA Modifications in Hematologic Malignancies

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Epigenetics in Oncology

Part of the book series: Cancer Treatment and Research ((CTAR,volume 190))

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Abstract

Chemical modifications on macromolecules such as DNA, RNA and proteins play important roles in almost all biological processes. The revival of RNA modification research began with the discovery of RNA modification machineries, and with the development of better techniques for characterizing and profiling these modifications at the transcriptome-wide level. Hematopoietic system is maintained by hematopoietic stem cells that possess efficient self-renewal capacity and the potential of differentiation into all lineages of blood cells, and the imbalance of this homeostasis frequently causes hematologic malignancies such as leukemia. Recent studies reveal that dysregulated RNA modifications play essential roles in hematologic malignancies. Herein, we summarize recent advances in some major RNA modifications, the detection methods, roles and mechanisms of these RNA modifications in hematologic malignancies.

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References

  1. Cohn WE (1960) Pseudouridine, a carbon-carbon linked ribonucleoside in ribonucleic acids: isolation, structure, and chemical characteristics. J Biol Chem 235:1488–1498

    Article  CAS  PubMed  Google Scholar 

  2. Davis FF, Allen FW (1957) Ribonucleic acids from yeast which contain a fifth nucleotide. J Biol Chem 227:907–915

    Article  CAS  PubMed  Google Scholar 

  3. Ma J, Zhang L, Chen S, Liu H (2022) A brief review of RNA modification related database resources. Methods 203:342–353. https://doi.org/10.1016/j.ymeth.2021.03.003

    Article  CAS  PubMed  Google Scholar 

  4. Jia G, Fu Y, Zhao X, Dai Q, Zheng G, Yang Y, Yi C, Lindahl T, Pan T, Yang YG, He C (2011) N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nat Chem Biol 7:885–887. https://doi.org/10.1038/nchembio.687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. 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 (2012) Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 485:201–206. https://doi.org/10.1038/nature11112

    Article  CAS  PubMed  Google Scholar 

  6. 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. https://doi.org/10.1016/j.cell.2012.05.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Orkin SH, Zon LI (2008) Hematopoiesis: an evolving paradigm for stem cell biology. Cell 132:631–644. https://doi.org/10.1016/j.cell.2008.01.025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Wilkinson AC, Igarashi KJ, Nakauchi H (2020) Haematopoietic stem cell self-renewal in vivo and ex vivo. Nat Rev Genet 21:541–554. https://doi.org/10.1038/s41576-020-0241-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Olson OC, Kang YA, Passegue E (2020) Normal hematopoiesis is a balancing act of self-renewal and regeneration. Cold Spring Harb Perspect Med.https://doi.org/10.1101/cshperspect.a035519

  10. Dohner H, Weisdorf DJ, Bloomfield CD (2015) Acute Myeloid Leukemia. N Engl J Med 373:1136–1152. https://doi.org/10.1056/NEJMra1406184

    Article  CAS  PubMed  Google Scholar 

  11. Vu LP, Cheng Y, Kharas MG (2019) The Biology of m(6)A RNA methylation in normal and malignant hematopoiesis. Cancer Discov 9:25–33. https://doi.org/10.1158/2159-8290.CD-18-0959

    Article  CAS  PubMed  Google Scholar 

  12. Wang J, Li Y, Wang P, Han G, Zhang T, Chang J, Yin R, Shan Y, Wen J, Xie X et al (2020) Leukemogenic chromatin alterations promote AML Leukemia stem cells via a KDM4C-ALKBH5-AXL signaling axis. Cell Stem Cell 27(81–97):e88. https://doi.org/10.1016/j.stem.2020.04.001

    Article  CAS  Google Scholar 

  13. 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. https://doi.org/10.1038/nchembio.1836

    Article  CAS  PubMed  Google Scholar 

  14. Borchardt EK, Martinez NM, Gilbert WV (2020) Regulation and function of RNA pseudouridylation in human cells. Annu Rev Genet 54:309–336. https://doi.org/10.1146/annurev-genet-112618-043830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Karijolich J, Yi C, Yu YT (2015) Transcriptome-wide dynamics of RNA pseudouridylation. Nat Rev Mol Cell Biol 16:581–585. https://doi.org/10.1038/nrm4040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Penzo M, Guerrieri AN, Zacchini F, Trere D, Montanaro L (2017) RNA Pseudouridylation in physiology and medicine: for better and for worse. Genes 8.https://doi.org/10.3390/genes8110301

  17. Cerneckis J, Cui Q, He C, Yi C, Shi Y (2022) Decoding pseudouridine: an emerging target for therapeutic development. Trends Pharmacol Sci 43:522–535. https://doi.org/10.1016/j.tips.2022.03.008

    Article  CAS  PubMed  Google Scholar 

  18. Jobert L, Skjeldam HK, Dalhus B, Galashevskaya A, Vagbo CB, Bjoras M, Nilsen H (2013) The human base excision repair enzyme SMUG1 directly interacts with DKC1 and contributes to RNA quality control. Mol Cell 49:339–345. https://doi.org/10.1016/j.molcel.2012.11.010

    Article  CAS  PubMed  Google Scholar 

  19. Jack K, Bellodi C, Landry DM, Niederer RO, Meskauskas A, Musalgaonkar S, Kopmar N, Krasnykh O, Dean AM, Thompson SR et al (2011) RRNA pseudouridylation defects affect ribosomal ligand binding and translational fidelity from yeast to human cells. Mol Cell 44:660–666. https://doi.org/10.1016/j.molcel.2011.09.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Lorenz C, Lünse CE, Mörl M (2017) tRNA Modifications: impact on structure and thermal adaptation. Biomolecules 7.https://doi.org/10.3390/biom7020035

  21. Martinez NM, Su A, Burns MC, Nussbacher JK, Schaening C, Sathe S, Yeo GW, Gilbert WV (2022) Pseudouridine synthases modify human pre-mRNA co-transcriptionally and affect pre-mRNA processing. Mol Cell 82:645-659.e649. https://doi.org/10.1016/j.molcel.2021.12.023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Kariko K, Buckstein M, Ni H, Weissman D (2005) Suppression of RNA recognition by Toll-like receptors: the impact of nucleoside modification and the evolutionary origin of RNA. Immunity 23:165–175. https://doi.org/10.1016/j.immuni.2005.06.008

    Article  CAS  PubMed  Google Scholar 

  23. Desrosiers RC, Friderici KH, Rottman FM (1975) Characterization of Novikoff hepatoma mRNA methylation and heterogeneity in the methylated 5’ terminus. Biochemistry 14:4367–4374

    Article  CAS  PubMed  Google Scholar 

  24. Batista PJ, Molinie B, Wang J, Qu K, Zhang J, Li L, Bouley DM, Lujan E, Haddad B, Daneshvar K et al (2014) M(6)A RNA modification controls cell fate transition in mammalian embryonic stem cells. Cell Stem Cell 15:707–719. https://doi.org/10.1016/j.stem.2014.09.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Liu J, Yue Y, Han D, Wang X, Fu Y, Zhang L, Jia G, Yu M, Lu Z, Deng X et al (2014) A METTL3-METTL14 complex mediates mammalian nuclear RNA N6-adenosine methylation. Nat Chem Biol 10:93–95. https://doi.org/10.1038/nchembio.1432

    Article  CAS  PubMed  Google Scholar 

  26. Ping XL, Sun BF, Wang L, Xiao W, Yang X, Wang WJ, Adhikari S, Shi Y, Lv Y, Chen YS et al (2014) Mammalian WTAP is a regulatory subunit of the RNA N6-methyladenosine methyltransferase. Cell Res 24:177–189. https://doi.org/10.1038/cr.2014.3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Hu Y, Ouyang Z, Sui X, Qi M, Li M, He Y, Cao Y, Cao Q, Lu Q, Zhou S et al (2020) Oocyte competence is maintained by m(6)A methyltransferase KIAA1429-mediated RNA metabolism during mouse follicular development. Cell Death Differ 27:2468–2483. https://doi.org/10.1038/s41418-020-0516-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Knuckles P, Lence T, Haussmann IU, Jacob D, Kreim N, Carl SH, Masiello I, Hares T, Villasenor R, Hess D et al (2018) 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. Genes Dev 32:415–429. https://doi.org/10.1101/gad.309146.117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Wen J, Lv R, Ma H, Shen H, He C, Wang J, Jiao F, Liu H, Yang P, Tan L et al (2018) Zc3h13 regulates nuclear RNA m(6)A methylation and mouse embryonic stem cell self-renewal. Mol Cell 69(1028–1038):e1026. https://doi.org/10.1016/j.molcel.2018.02.015

    Article  CAS  Google Scholar 

  30. Zheng G, Dahl JA, Niu Y, Fedorcsak P, Huang CM, Li CJ, Vagbo CB, Shi Y, Wang WL, Song SH et al (2013) ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Mol Cell 49:18–29. https://doi.org/10.1016/j.molcel.2012.10.015

    Article  CAS  PubMed  Google Scholar 

  31. Xiao W, Adhikari S, Dahal U, Chen YS, Hao YJ, Sun BF, Sun HY, Li A, Ping XL, Lai WY et al (2016) Nuclear m(6)A reader YTHDC1 regulates mRNA splicing. Mol Cell 61:507–519. https://doi.org/10.1016/j.molcel.2016.01.012

    Article  CAS  PubMed  Google Scholar 

  32. Hsu PJ, Zhu Y, Ma H, Guo Y, Shi X, Liu Y, Qi M, Lu Z, Shi H, Wang J et al (2017) Ythdc2 is an N(6)-methyladenosine binding protein that regulates mammalian spermatogenesis. Cell Res 27:1115–1127. https://doi.org/10.1038/cr.2017.99

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Theler D, Dominguez C, Blatter M, Boudet J, Allain FH (2014) Solution structure of the YTH domain in complex with N6-methyladenosine RNA: a reader of methylated RNA. Nucleic Acids Res 42:13911–13919. https://doi.org/10.1093/nar/gku1116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Huang H, Weng H, Sun W, Qin X, Shi H, Wu H, Zhao BS, Mesquita A, Liu C, Yuan CL et al (2018) Recognition of RNA N(6)-methyladenosine by IGF2BP proteins enhances mRNA stability and translation. Nat Cell Biol 20:285–295. https://doi.org/10.1038/s41556-018-0045-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Feng M, Xie X, Han G, Zhang T, Li Y, Li Y, Yin R, Wang Q, Zhang T, Wang P et al (2021) YBX1 is required for maintaining myeloid leukemia cell survival by regulating BCL2 stability in an m6A-dependent manner. Blood 138:71–85. https://doi.org/10.1182/blood.2020009676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Wang P, Doxtader KA, Nam Y (2016) Structural basis for cooperative function of Mettl3 and Mettl14 Methyltransferases. Mol Cell 63:306–317. https://doi.org/10.1016/j.molcel.2016.05.041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Wang X, Feng J, Xue Y, Guan Z, Zhang D, Liu Z, Gong Z, Wang Q, Huang J, Tang C et al (2016) Structural basis of N(6)-adenosine methylation by the METTL3-METTL14 complex. Nature 534:575–578. https://doi.org/10.1038/nature18298

    Article  CAS  PubMed  Google Scholar 

  38. Huang J, Dong X, Gong Z, Qin LY, Yang S, Zhu YL, Wang X, Zhang D, Zou T, Yin P, Tang C (2019) Solution structure of the RNA recognition domain of METTL3-METTL14 N(6)-methyladenosine methyltransferase. Protein Cell 10:272–284. https://doi.org/10.1007/s13238-018-0518-7

    Article  CAS  PubMed  Google Scholar 

  39. Patil DP, Chen C-K, Pickering BF, Chow A, Jackson C, Guttman M, Jaffrey SR (2016) M(6)A RNA methylation promotes XIST-mediated transcriptional repression. Nature 537:369–373. https://doi.org/10.1038/nature19342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Yue Y, Liu J, Cui X, Cao J, Luo G, Zhang Z, Cheng T, Gao M, Shu X, Ma H et al (2018) VIRMA mediates preferential mA mRNA methylation in 3’UTR and near stop codon and associates with alternative polyadenylation. Cell Discov 4:10. https://doi.org/10.1038/s41421-018-0019-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Wei J, Liu F, Lu Z, Fei Q, Ai Y, He PC, Shi H, Cui X, Su R, Klungland A et al (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. https://doi.org/10.1016/j.molcel.2018.08.011

    Article  CAS  Google Scholar 

  42. Shen C, Sheng Y, Zhu AC, Robinson S, Jiang X, Dong L, Chen H, Su R, Yin Z, Li W et al (2020) RNA demethylase ALKBH5 selectively promotes tumorigenesis and cancer stem cell self-renewal in acute myeloid leukemia. Cell Stem Cell 27(64–80):e69. https://doi.org/10.1016/j.stem.2020.04.009

    Article  CAS  Google Scholar 

  43. Shi H, Wang X, Lu Z, Zhao BS, Ma H, Hsu PJ, Liu C, He C (2017) YTHDF3 facilitates translation and decay of N-methyladenosine-modified RNA. Cell Res 27:315–328. https://doi.org/10.1038/cr.2017.15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Du H, Zhao Y, He J, Zhang Y, Xi H, Liu M, Ma J, Wu L (2016) YTHDF2 destabilizes m(6)A-containing RNA through direct recruitment of the CCR4-NOT deadenylase complex. Nat Commun 7:12626. https://doi.org/10.1038/ncomms12626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Xu C, Wang X, Liu K, Roundtree IA, Tempel W, Li Y, Lu Z, He C, Min J (2014) Structural basis for selective binding of m6A RNA by the YTHDC1 YTH domain. Nat Chem Biol 10:927–929. https://doi.org/10.1038/nchembio.1654

    Article  CAS  PubMed  Google Scholar 

  46. Zhang Z, Theler D, Kaminska KH, Hiller M, de la Grange P, Pudimat R, Rafalska I, Heinrich B, Bujnicki JM, Allain FHT, Stamm S (2010) The YTH domain is a novel RNA binding domain. J Biol Chem 285:14701–14710. https://doi.org/10.1074/jbc.M110.104711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Roundtree IA, Luo G-Z, Zhang Z, Wang X, Zhou T, Cui Y, Sha J, Huang X, Guerrero L, Xie P et al (2017) YTHDC1 mediates nuclear export of N-methyladenosine methylated mRNAs. Elife 6.https://doi.org/10.7554/eLife.31311

  48. Kretschmer J, Rao H, Hackert P, Sloan KE, Höbartner C, Bohnsack MT (2018) The mA reader protein YTHDC2 interacts with the small ribosomal subunit and the 5′-3′ exoribonuclease XRN1. RNA 24:1339–1350. https://doi.org/10.1261/rna.064238.117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Xu C, Liu K, Ahmed H, Loppnau P, Schapira M, Min J (2015) Structural basis for the discriminative recognition of N6-Methyladenosine RNA by the human YT521-B homology domain family of proteins. J Biol Chem 290:24902–24913. https://doi.org/10.1074/jbc.M115.680389

    Article  CAS  PubMed  Google Scholar 

  50. Wojtas MN, Pandey RR, Mendel M, Homolka D, Sachidanandam R, Pillai RS (2017) Regulation of mA Transcripts by the 3′′→5’ RNA Helicase YTHDC2 Is essential for a successful meiotic program in the mammalian germline. Molecular Cell 68.https://doi.org/10.1016/j.molcel.2017.09.021

  51. Feng M, Xie X, Han G, Zhang T, Li Y, Li Y, Yin R, Wang Q, Zhang T, Wang P et al (2021) YBX1 is required for maintaining myeloid leukemia cell survival by regulating BCL2 stability in an m6A-dependent manner. Blood.https://doi.org/10.1182/blood.2020009676

  52. Alarcón 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. https://doi.org/10.1016/j.cell.2015.08.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Amos H, Korn M (1958) 5-Methyl cytosine in the RNA of Escherichia coli. Biochim Biophys Acta 29:444–445. https://doi.org/10.1016/0006-3002(58)90214-2

    Article  CAS  PubMed  Google Scholar 

  54. Schosserer M, Minois N, Angerer TB, Amring M, Dellago H, Harreither E, Calle-Perez A, Pircher A, Gerstl MP, Pfeifenberger S et al (2015) Methylation of ribosomal RNA by NSUN5 is a conserved mechanism modulating organismal lifespan. Nat Commun 6:6158. https://doi.org/10.1038/ncomms7158

    Article  CAS  PubMed  Google Scholar 

  55. Yang X, Yang Y, Sun BF, Chen YS, Xu JW, Lai WY, Li A, Wang X, Bhattarai DP, Xiao W et al (2017) 5-methylcytosine promotes mRNA export—NSUN2 as the methyltransferase and ALYREF as an m(5)C reader. Cell Res 27:606–625. https://doi.org/10.1038/cr.2017.55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Song H, Zhang J, Liu B, Xu J, Cai B, Yang H, Straube J, Yu X, Ma T (2022) Biological roles of RNA m(5)C modification and its implications in Cancer immunotherapy. Biomark Res 10:15. https://doi.org/10.1186/s40364-022-00362-8

    Article  PubMed  PubMed Central  Google Scholar 

  57. Bohnsack KE, Hobartner C, Bohnsack MT (2019) Eukaryotic 5-methylcytosine (m(5)C) RNA Methyltransferases: mechanisms, cellular functions, and links to disease. Genes 10.https://doi.org/10.3390/genes10020102

  58. Liu J, Huang T, Zhang Y, Zhao T, Zhao X, Chen W, Zhang R (2021) Sequence- and structure-selective mRNA m(5)C methylation by NSUN6 in animals. Natl Sci Rev 8, nwaa273. https://doi.org/10.1093/nsr/nwaa273.

  59. Selmi T, Hussain S, Dietmann S, Heiss M, Borland K, Flad S, Carter JM, Dennison R, Huang YL, Kellner S et al (2021) Sequence- and structure-specific cytosine-5 mRNA methylation by NSUN6. Nucleic Acids Res 49:1006–1022. https://doi.org/10.1093/nar/gkaa1193

    Article  CAS  PubMed  Google Scholar 

  60. Delatte B, Wang F, Ngoc LV, Collignon E, Bonvin E, Deplus R, Calonne E, Hassabi B, Putmans P, Awe S et al (2016) RNA biochemistry. Transcriptome-wide distribution and function of RNA hydroxymethylcytosine. Science 351:282–285. https://doi.org/10.1126/science.aac5253

    Article  CAS  PubMed  Google Scholar 

  61. Shen Q, Zhang Q, Shi Y, Shi Q, Jiang Y, Gu Y, Li Z, Li X, Zhao K, Wang C et al (2018) Tet2 promotes pathogen infection-induced myelopoiesis through mRNA oxidation. Nature 554:123–127. https://doi.org/10.1038/nature25434

    Article  CAS  PubMed  Google Scholar 

  62. Shen H, Ontiveros RJ, Owens MC, Liu MY, Ghanty U, Kohli RM, Liu KF (2021) TET-mediated 5-methylcytosine oxidation in tRNA promotes translation. J Biol Chem 296:100087. https://doi.org/10.1074/jbc.RA120.014226

    Article  CAS  PubMed  Google Scholar 

  63. Kawarada L, Suzuki T, Ohira T, Hirata S, Miyauchi K, Suzuki T (2017) ALKBH1 is an RNA dioxygenase responsible for cytoplasmic and mitochondrial tRNA modifications. Nucleic Acids Res 45:7401–7415. https://doi.org/10.1093/nar/gkx354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Chen X, Li A, Sun BF, Yang Y, Han YN, Yuan X, Chen RX, Wei WS, Liu Y, Gao CC et al (2019) 5-methylcytosine promotes pathogenesis of bladder cancer through stabilizing mRNAs. Nat Cell Biol 21:978–990. https://doi.org/10.1038/s41556-019-0361-y

    Article  CAS  PubMed  Google Scholar 

  65. Yang Y, Wang L, Han X, Yang WL, Zhang M, Ma HL, Sun BF, Li A, Xia J, Chen J et al (2019) RNA 5-methylcytosine facilitates the maternal-to-zygotic transition by preventing maternal mRNA decay. Mol Cell 75(1188–1202):e1111. https://doi.org/10.1016/j.molcel.2019.06.033

    Article  CAS  Google Scholar 

  66. Dunn DB (1961) The occurrence of 1-methyladenine in ribonucleic acid. Biochim Biophys Acta 46:198–200

    Article  CAS  PubMed  Google Scholar 

  67. Hall RH (1963) Isolation of 2’-O-Methylribonucleosides from the Rna of Mammalian Tissues and from E. Coli. Biochem Biophys Res Commun 12:429–431. https://doi.org/10.1016/0006-291x(63)90309-7

    Article  CAS  PubMed  Google Scholar 

  68. Sharma S, Watzinger P, Kotter P, Entian KD (2013) Identification of a novel methyltransferase, Bmt2, responsible for the N-1-methyl-adenosine base modification of 25S rRNA in Saccharomyces cerevisiae. Nucleic Acids Res 41:5428–5443. https://doi.org/10.1093/nar/gkt195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. El Yacoubi B, Bailly M, de Crecy-Lagard V (2012) Biosynthesis and function of posttranscriptional modifications of transfer RNAs. Annu Rev Genet 46:69–95. https://doi.org/10.1146/annurev-genet-110711-155641

    Article  CAS  PubMed  Google Scholar 

  70. Engel JD (1975) Mechanism of the Dimroth rearrangement in adenosine. Biochem Biophys Res Commun 64:581–586. https://doi.org/10.1016/0006-291x(75)90361-7

    Article  CAS  PubMed  Google Scholar 

  71. 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 (2016) The dynamic N(1)-methyladenosine methylome in eukaryotic messenger RNA. Nature 530:441–446. https://doi.org/10.1038/nature16998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Li X, Xiong X, Zhang M, Wang K, Chen Y, Zhou J, Mao Y, Lv J, Yi D, Chen XW et al (2017) Base-resolution mapping reveals distinct m(1)A Methylome in nuclear- and mitochondrial-encoded transcripts. Mol Cell 68(993–1005):e1009. https://doi.org/10.1016/j.molcel.2017.10.019

    Article  CAS  Google Scholar 

  73. Li X, Xiong X, Wang K, Wang L, Shu X, Ma S, Yi C (2016) Transcriptome-wide mapping reveals reversible and dynamic N(1)-methyladenosine methylome. Nat Chem Biol 12:311–316. https://doi.org/10.1038/nchembio.2040

    Article  CAS  PubMed  Google Scholar 

  74. 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. https://doi.org/10.1038/nature24456

    Article  CAS  PubMed  Google Scholar 

  75. Bar-Yaacov D, Frumkin I, Yashiro Y, Chujo T, Ishigami Y, Chemla Y, Blumberg A, Schlesinger O, Bieri P, Greber B et al (2016) Mitochondrial 16S rRNA is methylated by tRNA methyltransferase TRMT61B in all vertebrates. PLoS Biol 14:e1002557. https://doi.org/10.1371/journal.pbio.1002557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Chujo T, Suzuki T (2012) Trmt61B is a methyltransferase responsible for 1-methyladenosine at position 58 of human mitochondrial tRNAs. RNA 18:2269–2276. https://doi.org/10.1261/rna.035600.112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Vilardo E, Nachbagauer C, Buzet A, Taschner A, Holzmann J, Rossmanith W (2012) A subcomplex of human mitochondrial RNase P is a bifunctional methyltransferase–extensive moonlighting in mitochondrial tRNA biogenesis. Nucleic Acids Res 40:11583–11593. https://doi.org/10.1093/nar/gks910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Dai X, Wang T, Gonzalez G, Wang Y (2018) Identification of YTH domain-containing proteins as the readers for N1-methyladenosine in RNA. Anal Chem 90:6380–6384. https://doi.org/10.1021/acs.analchem.8b01703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Duncan T, Trewick SC, Koivisto P, Bates PA, Lindahl T, Sedgwick B (2002) Reversal of DNA alkylation damage by two human dioxygenases. Proc Natl Acad Sci U S A 99:16660–16665. https://doi.org/10.1073/pnas.262589799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Aas PA, Otterlei M, Falnes PO, Vagbo CB, Skorpen F, Akbari M, Sundheim O, Bjoras M, Slupphaug G, Seeberg E, Krokan HE (2003) Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA. Nature 421:859–863. https://doi.org/10.1038/nature01363

    Article  CAS  PubMed  Google Scholar 

  81. Liu F, Clark W, Luo G, Wang X, Fu Y, Wei J, Wang X, Hao Z, Dai Q, Zheng G et al (2016) ALKBH1-mediated tRNA demethylation regulates translation. Cell 167(816–828):e816. https://doi.org/10.1016/j.cell.2016.09.038

    Article  CAS  Google Scholar 

  82. 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. https://doi.org/10.1038/nmeth.3453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Molinie B, Wang J, Lim KS, Hillebrand R, Lu ZX, Van Wittenberghe N, Howard BD, Daneshvar K, Mullen AC, Dedon P et al (2016) M(6)A-LAIC-seq reveals the census and complexity of the m(6)A epitranscriptome. Nat Methods 13:692–698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Dierks D, Garcia-Campos MA, Uzonyi A, Safra M, Edelheit S, Rossi A, Sideri T, Varier RA, Brandis A, Stelzer Y et al (2021) Multiplexed profiling facilitates robust m6A quantification at site, gene and sample resolution. Nat Methods 18:1060–1067. https://doi.org/10.1038/s41592-021-01242-z

    Article  CAS  PubMed  Google Scholar 

  85. Yin R, Chang J, Li Y, Gao Z, Qiu Q, Wang Q, Han G, Chai J, Feng M, Wang P et al (2022) Differential m(6)A RNA landscapes across hematopoiesis reveal a role for IGF2BP2 in preserving hematopoietic stem cell function. Cell Stem Cell 29(149–159):e147. https://doi.org/10.1016/j.stem.2021.09.014

    Article  CAS  Google Scholar 

  86. Garcia-Campos MA, Edelheit S, Toth U, Safra M, Shachar R, Viukov S, Winkler R, Nir R, Lasman L, Brandis A et al (2019) Deciphering the “m(6)A Code” via antibody-independent quantitative profiling. Cell 178(731–747):e716. https://doi.org/10.1016/j.cell.2019.06.013

    Article  CAS  Google Scholar 

  87. Meyer KD (2019) DART-seq: an antibody-free method for global m(6)A detection. Nat Methods 16:1275–1280. https://doi.org/10.1038/s41592-019-0570-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Wang Y, Xiao Y, Dong S, Yu Q, Jia G (2020) Antibody-free enzyme-assisted chemical approach for detection of N(6)-methyladenosine. Nat Chem Biol 16:896–903. https://doi.org/10.1038/s41589-020-0525-x

    Article  CAS  PubMed  Google Scholar 

  89. Shu X, Cao J, Cheng M, Xiang S, Gao M, Li T, Ying X, Wang F, Yue Y, Lu Z et al (2020) A metabolic labeling method detects m(6)A transcriptome-wide at single base resolution. Nat Chem Biol 16:887–895. https://doi.org/10.1038/s41589-020-0526-9

    Article  CAS  PubMed  Google Scholar 

  90. Hu L, Liu S, Peng Y, Ge R, Su R, Senevirathne C, Harada BT, Dai Q, Wei J, Zhang L et al (2022) M(6)A RNA modifications are measured at single-base resolution across the mammalian transcriptome. Nat Biotechnol 40:1210–1219. https://doi.org/10.1038/s41587-022-01243-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. 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. https://doi.org/10.1038/s41592-019-0550-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. 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. https://doi.org/10.1093/nar/gks144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Khoddami V, Cairns BR (2013) Identification of direct targets and modified bases of RNA cytosine methyltransferases. Nat Biotechnol 31:458–464. https://doi.org/10.1038/nbt.2566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Hussain S, Sajini AA, Blanco S, Dietmann S, Lombard P, Sugimoto Y, Paramor M, Gleeson JG, Odom DT, Ule J, Frye M (2013) NSun2-mediated cytosine-5 methylation of vault noncoding RNA determines its processing into regulatory small RNAs. Cell Rep 4:255–261. https://doi.org/10.1016/j.celrep.2013.06.029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. 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. https://doi.org/10.1038/nature13802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Schwartz S, Bernstein DA, Mumbach MR, Jovanovic M, Herbst RH, Leon-Ricardo BX, Engreitz JM, Guttman M, Satija R, Lander ES et al (2014) Transcriptome-wide mapping reveals widespread dynamic-regulated pseudouridylation of ncRNA and mRNA. Cell 159:148–162. https://doi.org/10.1016/j.cell.2014.08.028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Zhang Z, Chen LQ, Zhao YL, Yang CG, Roundtree IA, Zhang Z, Ren J, Xie W, He C, Luo GZ (2019) Single-base mapping of m(6)A by an antibody-independent method. Science advances 5, eaax0250. https://doi.org/10.1126/sciadv.aax0250.

  98. Li X, Xiong X, Zhang M, Wang K, Chen Y, Zhou J, Mao Y, Lv J, Yi D, Chen XW et al (2017) Base-resolution mapping reveals distinct m(1)A Methylome in nuclear- and mitochondrial-encoded transcripts. Mol Cell 68:993-1005.e1009. https://doi.org/10.1016/j.molcel.2017.10.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Xiong X, Li X, Yi C (2018) N(1)-methyladenosine methylome in messenger RNA and non-coding RNA. Curr Opin Chem Biol 45:179–186. https://doi.org/10.1016/j.cbpa.2018.06.017

    Article  CAS  PubMed  Google Scholar 

  100. 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. https://doi.org/10.1371/journal.pgen.1003602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Zhang C, Chen Y, Sun B, Wang L, Yang Y, Ma D, Lv J, Heng J, Ding Y, Xue Y et al (2017) M(6)A modulates haematopoietic stem and progenitor cell specification. Nature 549:273–276. https://doi.org/10.1038/nature23883

    Article  CAS  PubMed  Google Scholar 

  102. Jiang X, Liu B, Nie Z, Duan L, Xiong Q, Jin Z, Yang C, Chen Y (2021) The role of m6A modification in the biological functions and diseases. Signal Transduct Target Ther 6:74. https://doi.org/10.1038/s41392-020-00450-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Gao Y, Vasic R, Song Y, Teng R, Liu C, Gbyli R, Biancon G, Nelakanti R, Lobben K, Kudo E et al (2020) M(6)A Modification prevents formation of endogenous double-stranded RNAs and deleterious innate immune responses during hematopoietic development. Immunity 52(1007–1021):e1008. https://doi.org/10.1016/j.immuni.2020.05.003

    Article  CAS  Google Scholar 

  104. Lee H, Bao S, Qian Y, Geula S, Leslie J, Zhang C, Hanna JH, Ding L (2019) Stage-specific requirement for Mettl3-dependent m(6)A mRNA methylation during haematopoietic stem cell differentiation. Nat Cell Biol 21:700–709. https://doi.org/10.1038/s41556-019-0318-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Cheng Y, Luo H, Izzo F, Pickering BF, Nguyen D, Myers R, Schurer A, Gourkanti S, Bruning JC, Vu LP et al (2019) M(6)A RNA methylation maintains hematopoietic stem cell identity and symmetric commitment. Cell Rep 28(1703–1716):e1706. https://doi.org/10.1016/j.celrep.2019.07.032

    Article  CAS  Google Scholar 

  106. Yao QJ, Sang L, Lin M, Yin X, Dong W, Gong Y, Zhou BO (2018) Mettl3-Mettl14 methyltransferase complex regulates the quiescence of adult hematopoietic stem cells. Cell Res 28:952–954. https://doi.org/10.1038/s41422-018-0062-2

    Article  PubMed  PubMed Central  Google Scholar 

  107. Martin GH, Park CY (2018) Meddling with METTLs in normal and leukemia stem cells. Cell Stem Cell 22:139–141. https://doi.org/10.1016/j.stem.2018.01.013

    Article  CAS  PubMed  Google Scholar 

  108. Vu LP, Pickering BF, Cheng Y, Zaccara S, Nguyen D, Minuesa G, Chou T, Chow A, Saletore Y, MacKay M et al (2017) The N(6)-methyladenosine (m(6)A)-forming enzyme METTL3 controls myeloid differentiation of normal hematopoietic and leukemia cells. Nat Med 23:1369–1376. https://doi.org/10.1038/nm.4416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Barbieri I, Tzelepis K, Pandolfini L, Shi J, Millan-Zambrano G, Robson SC, Aspris D, Migliori V, Bannister AJ, Han N et al (2017) Promoter-bound METTL3 maintains myeloid leukaemia by m(6)A-dependent translation control. Nature 552:126–131. https://doi.org/10.1038/nature24678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Li Z, Weng H, Su R, Weng X, Zuo Z, Li C, Huang H, Nachtergaele S, Dong L, Hu C et al (2017) FTO plays an oncogenic role in acute myeloid leukemia as a N(6)-Methyladenosine RNA demethylase. Cancer Cell 31:127–141. https://doi.org/10.1016/j.ccell.2016.11.017

    Article  CAS  PubMed  Google Scholar 

  111. Su R, Dong L, Li C, Nachtergaele S, Wunderlich M, Qing Y, Deng X, Wang Y, Weng X, Hu C et al (2018) R-2HG exhibits anti-tumor activity by targeting FTO/m(6)A/MYC/CEBPA signaling. Cell 172(90–105):e123. https://doi.org/10.1016/j.cell.2017.11.031

    Article  CAS  Google Scholar 

  112. Guirguis AA, Liddicoat BJ, Dawson MA (2020) The old and the new: DNA and RNA methylation in normal and malignant hematopoiesis. Exp Hematol 90:1–11. https://doi.org/10.1016/j.exphem.2020.09.193

    Article  CAS  PubMed  Google Scholar 

  113. Weng H, Huang H, Wu H, Qin X, Zhao BS, Dong L, Shi H, Skibbe J, Shen C, Hu C et al (2018) METTL14 inhibits hematopoietic stem/progenitor differentiation and promotes leukemogenesis via mRNA m(6)A modification. Cell Stem Cell 22(191–205):e199. https://doi.org/10.1016/j.stem.2017.11.016

    Article  CAS  Google Scholar 

  114. Park IK, Mundy-Bosse B, Whitman SP, Zhang X, Warner SL, Bearss DJ, Blum W, Marcucci G, Caligiuri MA (2015) Receptor tyrosine kinase Axl is required for resistance of leukemic cells to FLT3-targeted therapy in acute myeloid leukemia. Leukemia 29:2382–2389. https://doi.org/10.1038/leu.2015.147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Cheng Y, Luo H, Kharas MG (2020) Rubbing out leukemia stem cells by erasing the eraser. Cell Stem Cell 27:3–5. https://doi.org/10.1016/j.stem.2020.06.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Sheng Y, Wei J, Yu F, Xu H, Yu C, Wu Q, Liu Y, Li L, Cui XL, Gu X et al (2021) A critical role of nuclear m6A reader YTHDC1 in leukemogenesis by regulating MCM complex-mediated DNA replication. Blood 138:2838–2852. https://doi.org/10.1182/blood.2021011707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Mapperley C, van de Lagemaat LN, Lawson H, Tavosanis A, Paris J, Campos J, Wotherspoon D, Durko J, Sarapuu A, Choe J et al (2021) The mRNA m6A reader YTHDF2 suppresses proinflammatory pathways and sustains hematopoietic stem cell function. J Exp Med 218.https://doi.org/10.1084/jem.20200829

  118. Li Z, Qian P, Shao W, Shi H, He XC, Gogol M, Yu Z, Wang Y, Qi M, Zhu Y et al (2018) Suppression of m(6)A reader Ythdf2 promotes hematopoietic stem cell expansion. Cell Res 28:904–917. https://doi.org/10.1038/s41422-018-0072-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Paris J, Morgan M, Campos J, Spencer GJ, Shmakova A, Ivanova I, Mapperley C, Lawson H, Wotherspoon DA, Sepulveda C et al (2019) Targeting the RNA m(6)A reader YTHDF2 selectively compromises cancer stem cells in acute myeloid leukemia. Cell Stem Cell 25(137–148):e136. https://doi.org/10.1016/j.stem.2019.03.021

    Article  CAS  Google Scholar 

  120. Elcheva IA, Wood T, Chiarolanzio K, Chim B, Wong M, Singh V, Gowda CP, Lu Q, Hafner M, Dovat S et al (2020) RNA-binding protein IGF2BP1 maintains leukemia stem cell properties by regulating HOXB4, MYB, and ALDH1A1. Leukemia 34:1354–1363. https://doi.org/10.1038/s41375-019-0656-9

    Article  CAS  PubMed  Google Scholar 

  121. Tran TM, Philipp J, Bassi JS, Nibber N, Draper JM, Lin TL, Palanichamy JK, Jaiswal AK, Silva O, Paing M et al (2022) The RNA-binding protein IGF2BP3 is critical for MLL-AF4-mediated leukemogenesis. Leukemia 36:68–79. https://doi.org/10.1038/s41375-021-01346-7

    Article  CAS  PubMed  Google Scholar 

  122. Zhang N, Shen Y, Li H, Chen Y, Zhang P, Lou S, Deng J (2022) The m6A reader IGF2BP3 promotes acute myeloid leukemia progression by enhancing RCC2 stability. Exp Mol Med 54:194–205. https://doi.org/10.1038/s12276-022-00735-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Weng H, Huang F, Yu Z, Chen Z, Prince E, Kang Y, Zhou K, Li W, Hu J, Fu C et al (2022) The m(6)A reader IGF2BP2 regulates glutamine metabolism and represents a therapeutic target in acute myeloid leukemia. Cancer Cell 40(1566–1582):e1510. https://doi.org/10.1016/j.ccell.2022.10.004

    Article  CAS  Google Scholar 

  124. Cheng Y, Gao Z, Zhang T, Wang Y, Xie X, Han G, Li Y, Yin R, Chen Y, Wang P et al (2022) Decoding m(6)A RNA methylome identifies PRMT6-regulated lipid transport promoting AML stem cell maintenance. Cell Stem Cell.https://doi.org/10.1016/j.stem.2022.12.003

  125. Yankova E, Blackaby W, Albertella M, Rak J, De Braekeleer E, Tsagkogeorga G, Pilka ES, Aspris D, Leggate D, Hendrick AG (2021) Small-molecule inhibition of METTL3 as a strategy against myeloid leukaemia. Nature 593:597–601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Huang Y, Su R, Sheng Y, Dong L, Dong Z, Xu H, Ni T, Zhang ZS, Zhang T, Li C et al (2019) Small-molecule targeting of oncogenic FTO demethylase in acute myeloid leukemia. Cancer Cell 35(677–691):e610. https://doi.org/10.1016/j.ccell.2019.03.006

    Article  CAS  Google Scholar 

  127. Su R, Dong L, Li Y, Gao M, Han L, Wunderlich M, Deng X, Li H, Huang Y, Gao L et al (2020) Targeting FTO suppresses cancer stem cell maintenance and immune evasion. Cancer Cell 38(79–96):e11. https://doi.org/10.1016/j.ccell.2020.04.017

    Article  CAS  Google Scholar 

  128. Cheng JX, Chen L, Li Y, Cloe A, Yue M, Wei J, Watanabe KA, Shammo JM, Anastasi J, Shen QJ et al (2018) RNA cytosine methylation and methyltransferases mediate chromatin organization and 5-azacytidine response and resistance in leukaemia. Nat Commun 9:1163. https://doi.org/10.1038/s41467-018-03513-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Guzzi N, Muthukumar S, Ciesla M, Todisco G, Ngoc PCT, Madej M, Munita R, Fazio S, Ekstrom S, Mortera-Blanco T et al (2022) Pseudouridine-modified tRNA fragments repress aberrant protein synthesis and predict leukaemic progression in myelodysplastic syndrome. Nat Cell Biol 24:299–306. https://doi.org/10.1038/s41556-022-00852-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. He H, Wang Y, Wang J (2020) ALKBH3 is dispensable in maintaining hematopoietic stem cells but forced ALKBH3 rectified the differentiation skewing of aged hematopoietic stem cells. Blood Sci 2:137–143. https://doi.org/10.1097/BS9.0000000000000057

    Article  PubMed  PubMed Central  Google Scholar 

  131. Esteve-Puig R, Climent F, Pineyro D, Domingo-Domenech E, Davalos V, Encuentra M, Rea A, Espejo-Herrera N, Soler M, Lopez M et al (2021) Epigenetic loss of m1A RNA demethylase ALKBH3 in Hodgkin lymphoma targets collagen, conferring poor clinical outcome. Blood 137:994–999. https://doi.org/10.1182/blood.2020005823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Zhang Z, Chen T, Chen HX, Xie YY, Chen LQ, Zhao YL, Liu BD, Jin L, Zhang W, Liu C et al (2021) Systematic calibration of epitranscriptomic maps using a synthetic modification-free RNA library. Nat Methods 18:1213–1222. https://doi.org/10.1038/s41592-021-01280-7

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We acknowledge the members of our laboratory for helpful discussion. This work is supported by grants to H.Z. from the National Natural Science Foundation of China (82230007), and the Medical Science Advancement Program (Basic Medical Sciences) of Wuhan University (TFJC2018005).

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  1. State Key Laboratory of Oral & Maxillofacial Reconstruction and Regeneration, Key Laboratory of Oral Biomedicine Ministry of Education, Hubei Key Laboratory of Stomatology, School and Hospital of Stomatology, Wuhan University, Wuhan, China

    Yashu Li, Wen Tian & Haojian Zhang

  2. Frontier Science Center for Immunology and Metabolism, Medical Research Institute, Wuhan University, No.185, East Lake Road, Wuchang District, Wuhan, Hubei, 430071, P. R. China

    Yashu Li, Wen Tian & Haojian Zhang

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  1. Yashu Li
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  2. Wen Tian
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  1. Department of Systems Biology, City of Hope National Medical Center, Duarte, CA, USA

    Jianjun Chen

  2. Department of Pharmacology and Cancer Biology, Duke University School of Medicine, Chapel Hill, NC, USA

    G. Greg Wang

  3. Stem Cell Center, Yale University School of Medicine, New Haven, CT, USA

    Jun Lu

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Li, Y., Tian, W., Zhang, H. (2023). RNA Modifications in Hematologic Malignancies. In: Chen, J., Wang, G.G., Lu, J. (eds) Epigenetics in Oncology . Cancer Treatment and Research, vol 190. Springer, Cham. https://doi.org/10.1007/978-3-031-45654-1_6

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