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PMID: 28855326 Published · ppublish English Journal Article Review Research Support, Non-U.S. Gov't

The RNA modification landscape in human disease.

RNA (New York, N.Y.) ·Vol. 23 ·No. 12 ·2017-00-00 ·Pages 1754-1769

Jonkhout N, Tran J, Smith MA, Schonrock N, Mattick JS, Novoa EM

Abstract

RNA modifications have been historically considered as fine-tuning chemo-structural features of infrastructural RNAs, such as rRNAs, tRNAs, and snoRNAs. This view has changed dramatically in recent years, to a large extent as a result of systematic efforts to map and quantify various RNA modifications in a transcriptome-wide manner, revealing that RNA modifications are reversible, dynamically regulated, far more widespread than originally thought, and involved in major biological processes, including cell differentiation, sex determination, and stress responses. Here we summarize the state of knowledge and provide a catalog of RNA modifications and their links to neurological disorders, cancers, and other diseases. With the advent of direct RNA-sequencing technologies, we expect that this catalog will help prioritize those RNA modifications for transcriptome-wide maps.

Keywords
RNA modification detection methods direct RNA sequencing disease epitranscriptome
MeSH Terms
Animals Disease/genetics Humans RNA/chemistry RNA Processing, Post-Transcriptional
Chemicals
RNA
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Jonkhout Nicky
Garvan Institute of Medical Research, Darlinghurst, 2010 NSW, Australia. | St. Vincent's Clinical School, Faculty of Medicine, University of New South Wales, Kensington NSW 2052, Australia.
Tran Julia
Garvan Institute of Medical Research, Darlinghurst, 2010 NSW, Australia.
Smith Martin A
Garvan Institute of Medical Research, Darlinghurst, 2010 NSW, Australia. | St. Vincent's Clinical School, Faculty of Medicine, University of New South Wales, Kensington NSW 2052, Australia.
Schonrock Nicole
Garvan Institute of Medical Research, Darlinghurst, 2010 NSW, Australia. | Genome.One, Darlinghurst, 2010 NSW, Australia.
Mattick John S
Garvan Institute of Medical Research, Darlinghurst, 2010 NSW, Australia. | St. Vincent's Clinical School, Faculty of Medicine, University of New South Wales, Kensington NSW 2052, Australia.
Novoa Eva Maria
Garvan Institute of Medical Research, Darlinghurst, 2010 NSW, Australia. | St. Vincent's Clinical School, Faculty of Medicine, University of New South Wales, Kensington NSW 2052, Australia. | Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA. | Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02139, USA.
References (139)
139 references, click to expand
  1. A third member of the RNA-specific adenosine deaminase gene family, ADAR3, contains both single- and double-stranded RNA binding domains.
    RNA. 2000 May;6(5):755-67 PMID: 10836796
  2. Reverse transcriptase adds nontemplated nucleotides to cDNAs during 5'-RACE and primer extension.
    Biotechniques. 2001 Mar;30(3):574-80, 582 PMID: 11252793
  3. Characterization of two novel genes, WBSCR20 and WBSCR22, deleted in Williams-Beuren syndrome.
    Cytogenet Cell Genet. 2001;95(1-2):20-7 PMID: 11978965
  4. Detection and quantitation of RNA base modifications.
    RNA. 2004 Jun;10(6):996-1002 PMID: 15146083
  5. Mutations in the FTSJ1 gene coding for a novel S-adenosylmethionine-binding protein cause nonsyndromic X-linked mental retardation.
    Am J Hum Genet. 2004 Aug;75(2):305-9 PMID: 15162322
  6. Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G.
    PLoS Biol. 2004 Sep;2(9):E275 PMID: 15269786
  7. Determination of the 'critical region' for cat-like cry of Cri-du-chat syndrome and analysis of candidate genes by quantitative PCR.
    Eur J Hum Genet. 2005 Apr;13(4):475-85 PMID: 15657623
  8. Chromosome 8 BAC array comparative genomic hybridization and expression analysis identify amplification and overexpression of TRMT12 in breast cancer.
    Genes Chromosomes Cancer. 2007 Jul;46(7):694-707 PMID: 17440925
  9. Identification of modified residues in RNAs by reverse transcription-based methods.
    Methods Enzymol. 2007;425:21-53 PMID: 17673078
  10. Use of DNAzymes for site-specific analysis of ribonucleotide modifications.
    RNA. 2008 Jan;14(1):180-7 PMID: 17998290
  11. RNA editing, DNA recoding and the evolution of human cognition.
    Trends Neurosci. 2008 May;31(5):227-33 PMID: 18395806
  12. RNA cytosine methylation analysis by bisulfite sequencing.
    Nucleic Acids Res. 2009 Feb;37(2):e12 PMID: 19059995
  13. An association study of 45 folate-related genes in spina bifida: Involvement of cubilin (CUBN) and tRNA aspartic acid methyltransferase 1 (TRDMT1).
    Birth Defects Res A Clin Mol Teratol. 2009 Mar;85(3):216-26 PMID: 19161160
  14. Mutation of a gene essential for ribosome biogenesis, EMG1, causes Bowen-Conradi syndrome.
    Am J Hum Genet. 2009 Jun;84(6):728-39 PMID: 19463982
  15. Spliceosomal snRNA modifications and their function.
    RNA Biol. 2010 Mar-Apr;7(2):192-204 PMID: 20215871
  16. RNA metabolism and the pathogenesis of motor neuron diseases.
    Trends Neurosci. 2010 May;33(5):249-58 PMID: 20227117
  17. Long non-coding RNAs in nervous system function and disease.
    Brain Res. 2010 Jun 18;1338:20-35 PMID: 20380817
  18. RNA as the substrate for epigenome-environment interactions: RNA guidance of epigenetic processes and the expansion of RNA editing in animals underpins development, phenotypic plasticity, learning, and cognition.
    Bioessays. 2010 Jul;32(7):548-52 PMID: 20544741
  19. Adenosine-to-inosine RNA editing shapes transcriptome diversity in primates.
    Proc Natl Acad Sci U S A. 2010 Jul 6;107(27):12174-9 PMID: 20566853
  20. iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution.
    Nat Struct Mol Biol. 2010 Jul;17(7):909-15 PMID: 20601959
  21. The RNA Modification Database, RNAMDB: 2011 update.
    Nucleic Acids Res. 2011 Jan;39(Database issue):D195-201 PMID: 21071406
  22. Grand challenge commentary: RNA epigenetics?
    Nat Chem Biol. 2010 Dec;6(12):863-5 PMID: 21079590
  23. A quantitative systems approach reveals dynamic control of tRNA modifications during cellular stress.
    PLoS Genet. 2010 Dec 16;6(12):e1001247 PMID: 21187895
  24. The central role of RNA in human development and cognition.
    FEBS Lett. 2011 Jun 6;585(11):1600-16 PMID: 21557942
  25. DETECTING LOW-LEVEL SYNTHESIS IMPURITIES IN MODIFIED PHOSPHOROTHIOATE OLIGONUCLEOTIDES USING LIQUID CHROMATOGRAPHY - HIGH RESOLUTION MASS SPECTROMETRY.
    Int J Mass Spectrom. 2011 Jul 1;304(2-3):98-104 PMID: 21811394
  26. Deep sequencing reveals 50 novel genes for recessive cognitive disorders.
    Nature. 2011 Sep 21;478(7367):57-63 PMID: 21937992
  27. Mass spectrometry-based quantification of pseudouridine in RNA.
    J Am Soc Mass Spectrom. 2011 Aug;22(8):1363-72 PMID: 21953190
  28. N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO.
    Nat Chem Biol. 2011 Oct 16;7(12):885-7 PMID: 22002720
  29. When Does ALS Start? ADAR2-GluA2 Hypothesis for the Etiology of Sporadic ALS.
    Front Mol Neurosci. 2011 Nov 02;4:33 PMID: 22102833
  30. Profound downregulation of the RNA editing enzyme ADAR2 in ALS spinal motor neurons.
    Neurobiol Dis. 2012 Mar;45(3):1121-8 PMID: 22226999
  31. Widespread occurrence of 5-methylcytosine in human coding and non-coding RNA.
    Nucleic Acids Res. 2012 Jun;40(11):5023-33 PMID: 22344696
  32. Mutations in NSUN2 cause autosomal-recessive intellectual disability.
    Am J Hum Genet. 2012 May 4;90(5):847-55 PMID: 22541559
  33. Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq.
    Nature. 2012 Apr 29;485(7397):201-6 PMID: 22575960
  34. Whole exome sequencing identifies a splicing mutation in NSUN2 as a cause of a Dubowitz-like syndrome.
    J Med Genet. 2012 Jun;49(6):380-5 PMID: 22577224
  35. Comprehensive analysis of mRNA methylation reveals enrichment in 3' UTRs and near stop codons.
    Cell. 2012 Jun 22;149(7):1635-46 PMID: 22608085
  36. Translational infidelity-induced protein stress results from a deficiency in Trm9-catalyzed tRNA modifications.
    RNA Biol. 2012 Jul;9(7):990-1001 PMID: 22832247
  37. RNA cytosine methylation by Dnmt2 and NSun2 promotes tRNA stability and protein synthesis.
    Nat Struct Mol Biol. 2012 Sep;19(9):900-5 PMID: 22885326
  38. Landscape of transcription in human cells.
    Nature. 2012 Sep 6;489(7414):101-8 PMID: 22955620
  39. Method for comparative analysis of ribonucleic acids using isotope labeling and mass spectrometry.
    Anal Chem. 2012 Oct 16;84(20):8607-13 PMID: 22985222
  40. The birth of the Epitranscriptome: deciphering the function of RNA modifications.
    Genome Biol. 2012 Oct 31;13(10):175 PMID: 23113984
  41. MODOMICS: a database of RNA modification pathways--2013 update.
    Nucleic Acids Res. 2013 Jan;41(Database issue):D262-7 PMID: 23118484
  42. ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility.
    Mol Cell. 2013 Jan 10;49(1):18-29 PMID: 23177736
  43. Transcriptome-wide identification of A > I RNA editing sites by inosine specific cleavage.
    RNA. 2013 Feb;19(2):257-70 PMID: 23264566
  44. Identifying RNA editing sites using RNA sequencing data alone.
    Nat Methods. 2013 Feb;10(2):128-32 PMID: 23291724
  45. A human tRNA methyltransferase 9-like protein prevents tumour growth by regulating LIN9 and HIF1-α.
    EMBO Mol Med. 2013 Mar;5(3):366-83 PMID: 23381944
  46. Structure and function of long noncoding RNAs in epigenetic regulation.
    Nat Struct Mol Biol. 2013 Mar;20(3):300-7 PMID: 23463315
  47. Identification of direct targets and modified bases of RNA cytosine methyltransferases.
    Nat Biotechnol. 2013 May;31(5):458-64 PMID: 23604283
  48. Expression of NOL1/NOP2/sun domain (Nsun) RNA methyltransferase family genes in early mouse embryogenesis.
    Gene Expr Patterns. 2013 Dec;13(8):319-27 PMID: 23816522
  49. The fat mass and obesity associated gene (Fto) regulates activity of the dopaminergic midbrain circuitry.
    Nat Neurosci. 2013 Aug;16(8):1042-8 PMID: 23817550
  50. Loss of a conserved tRNA anticodon modification perturbs cellular signaling.
    PLoS Genet. 2013;9(8):e1003675 PMID: 23935536
  51. DNA methylation regulates associative reward learning.
    Nat Neurosci. 2013 Oct;16(10):1445-52 PMID: 23974711
  52. Whole exome sequencing unravels disease-causing genes in consanguineous families in Qatar.
    Clin Genet. 2014 Aug;86(2):134-41 PMID: 24102521
  53. HAMR: high-throughput annotation of modified ribonucleotides.
    RNA. 2013 Dec;19(12):1684-92 PMID: 24149843
  54. RNA-methylation-dependent RNA processing controls the speed of the circadian clock.
    Cell. 2013 Nov 7;155(4):793-806 PMID: 24209618
  55. A high-throughput quantitative approach reveals more small RNA modifications in mouse liver and their correlation with diabetes.
    Anal Chem. 2013 Dec 17;85(24):12173-81 PMID: 24261999
  56. High-resolution mapping reveals a conserved, widespread, dynamic mRNA methylation program in yeast meiosis.
    Cell. 2013 Dec 5;155(6):1409-21 PMID: 24269006
  57. Characterizing 5-methylcytosine in the mammalian epitranscriptome.
    Genome Biol. 2013 Nov 29;14(11):215 PMID: 24286375
  58. Posttranscriptional RNA Modifications: playing metabolic games in a cell's chemical Legoland.
    Chem Biol. 2014 Feb 20;21(2):174-85 PMID: 24315934
  59. N6-methyladenosine modification destabilizes developmental regulators in embryonic stem cells.
    Nat Cell Biol. 2014 Feb;16(2):191-8 PMID: 24394384
  60. A system of RNA modifications and biased codon use controls cellular stress response at the level of translation.
    Chem Res Toxicol. 2014 Mar 17;27(3):330-7 PMID: 24422464
  61. Role of tRNA modifications in human diseases.
    Trends Mol Med. 2014 Jun;20(6):306-14 PMID: 24581449
  62. Quantitative analysis of ribonucleoside modifications in tRNA by HPLC-coupled mass spectrometry.
    Nat Protoc. 2014 Apr;9(4):828-41 PMID: 24625781
  63. Contribution of CDKAL1 rs7756992 and IGF2BP2 rs4402960 polymorphisms in type 2 diabetes, diabetic complications, obesity risk and hypertension in the Tunisian population.
    J Diabetes. 2015 Jan;7(1):102-13 PMID: 24636221
  64. Hippocampus-specific deficiency in RNA editing of GluA2 in Alzheimer's disease.
    Neurobiol Aging. 2014 Aug;35(8):1785-91 PMID: 24679603
  65. The rise of regulatory RNA.
    Nat Rev Genet. 2014 Jun;15(6):423-37 PMID: 24776770
  66. Chemical inhibition of NAT10 corrects defects of laminopathic cells.
    Science. 2014 May 2;344(6183):527-32 PMID: 24786082
  67. The pivotal regulatory landscape of RNA modifications.
    Annu Rev Genomics Hum Genet. 2014;15:127-50 PMID: 24898039
  68. Association analysis of IGF2BP2, KCNJ11, and CDKAL1 polymorphisms with type 2 diabetes mellitus in a Moroccan population: a case-control study and meta-analysis.
    Biochem Genet. 2014 Oct;52(9-10):430-42 PMID: 24898818
  69. Perturbation of m6A writers reveals two distinct classes of mRNA methylation at internal and 5' sites.
    Cell Rep. 2014 Jul 10;8(1):284-96 PMID: 24981863
  70. Dynamic RNA modifications in disease.
    Curr Opin Genet Dev. 2014 Jun;26:47-52 PMID: 25005745
  71. Aberrant methylation of tRNAs links cellular stress to neuro-developmental disorders.
    EMBO J. 2014 Sep 17;33(18):2020-39 PMID: 25063673
  72. Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells.
    Nature. 2014 Nov 6;515(7525):143-6 PMID: 25192136
  73. Transcriptome-wide mapping reveals widespread dynamic-regulated pseudouridylation of ncRNA and mRNA.
    Cell. 2014 Sep 25;159(1):148-162 PMID: 25219674
  74. Dynamic RNA modifications in posttranscriptional regulation.
    Mol Cell. 2014 Oct 2;56(1):5-12 PMID: 25280100
  75. Rational experiment design for sequencing-based RNA structure mapping.
    RNA. 2014 Dec;20(12):1864-77 PMID: 25332375
  76. m(6)A RNA modification controls cell fate transition in mammalian embryonic stem cells.
    Cell Stem Cell. 2014 Dec 4;15(6):707-19 PMID: 25456834
  77. Functional importance of Ψ38 and Ψ39 in distinct tRNAs, amplified for tRNAGln(UUG) by unexpected temperature sensitivity of the s2U modification in yeast.
    RNA. 2015 Feb;21(2):188-201 PMID: 25505024
  78. An evolutionary approach uncovers a diverse response of tRNA 2-thiolation to elevated temperatures in yeast.
    RNA. 2015 Feb;21(2):202-12 PMID: 25505025
  79. Modulation of microRNA editing, expression and processing by ADAR2 deaminase in glioblastoma.
    Genome Biol. 2015 Jan 13;16:5 PMID: 25582055
  80. The origin of the ADAR gene family and animal RNA editing.
    BMC Evol Biol. 2015 Jan 29;15:4 PMID: 25630791
  81. A cautionary tale: the non-causal association between type 2 diabetes risk SNP, rs7756992, and levels of non-coding RNA, CDKAL1-v1.
    Diabetologia. 2015 Apr;58(4):745-8 PMID: 25634229
  82. Improved data analysis for the MinION nanopore sequencer.
    Nat Methods. 2015 Apr;12(4):351-6 PMID: 25686389
  83. Modify or die?--RNA modification defects in metazoans.
    RNA Biol. 2014;11(12):1555-67 PMID: 25692999
  84. RNA modification: the Golden Period 1995-2015.
    RNA. 2015 Apr;21(4):625-6 PMID: 25780166
  85. Successful test launch for nanopore sequencing.
    Nat Methods. 2015 Apr;12(4):303-4 PMID: 25825834
  86. Autophagy in spinal motor neurons of conditional ADAR2-knockout mice: An implication for a role of calcium in increased autophagy flux in ALS.
    Neurosci Lett. 2015 Jun 26;598:79-84 PMID: 25980994
  87. N(6)-methyladenosine Modulates Messenger RNA Translation Efficiency.
    Cell. 2015 Jun 4;161(6):1388-99 PMID: 26046440
  88. An association study of the m6A genes with major depressive disorder in Chinese Han population.
    J Affect Disord. 2015 Sep 1;183:279-86 PMID: 26047305
  89. Optimization of Codon Translation Rates via tRNA Modifications Maintains Proteome Integrity.
    Cell. 2015 Jun 18;161(7):1606-18 PMID: 26052047
  90. A complete bacterial genome assembled de novo using only nanopore sequencing data.
    Nat Methods. 2015 Aug;12(8):733-5 PMID: 26076426
  91. Single-nucleotide-resolution mapping of m6A and m6Am throughout the transcriptome.
    Nat Methods. 2015 Aug;12(8):767-72 PMID: 26121403
  92. FTO Obesity Variant Circuitry and Adipocyte Browning in Humans.
    N Engl J Med. 2015 Sep 3;373(10):895-907 PMID: 26287746
  93. The Role of a Novel TRMT1 Gene Mutation and Rare GRM1 Gene Defect in Intellectual Disability in Two Azeri Families.
    PLoS One. 2015 Aug 26;10(8):e0129631 PMID: 26308914
  94. The reverse transcription signature of N-1-methyladenosine in RNA-Seq is sequence dependent.
    Nucleic Acids Res. 2015 Nov 16;43(20):9950-64 PMID: 26365242
  95. Mutation in WDR4 impairs tRNA m(7)G46 methylation and causes a distinct form of microcephalic primordial dwarfism.
    Genome Biol. 2015 Sep 28;16:210 PMID: 26416026
  96. Profiling RNA editing in human tissues: towards the inosinome Atlas.
    Sci Rep. 2015 Oct 09;5:14941 PMID: 26449202
  97. The emerging epitranscriptomics of long noncoding RNAs.
    Biochim Biophys Acta. 2016 Jan;1859(1):59-70 PMID: 26541084
  98. PacBio Sequencing and Its Applications.
    Genomics Proteomics Bioinformatics. 2015 Oct;13(5):278-89 PMID: 26542840
  99. The epitranscriptome in modulating spatiotemporal RNA translation in neuronal post-synaptic function.
    Front Cell Neurosci. 2015 Oct 31;9:420 PMID: 26582006
  100. Trm9-Catalyzed tRNA Modifications Regulate Global Protein Expression by Codon-Biased Translation.
    PLoS Genet. 2015 Dec 15;11(12):e1005706 PMID: 26670883
  101. Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder.
    Science. 2016 Jan 22;351(6271):397-400 PMID: 26721680
  102. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals.
    Science. 2016 Jan 22;351(6271):391-396 PMID: 26721685
  103. Assessing the performance of the Oxford Nanopore Technologies MinION.
    Biomol Detect Quantif. 2015 Mar;3:1-8 PMID: 26753127
  104. Cracking the epitranscriptome.
    RNA. 2016 Feb;22(2):169-74 PMID: 26787305
  105. RNA Editing: A Contributor to Neuronal Dynamics in the Mammalian Brain.
    Trends Genet. 2016 Mar;32(3):165-175 PMID: 26803450
  106. RNA biochemistry. Transcriptome-wide distribution and function of RNA hydroxymethylcytosine.
    Science. 2016 Jan 15;351(6270):282-5 PMID: 26816380
  107. Real-time, portable genome sequencing for Ebola surveillance.
    Nature. 2016 Feb 11;530(7589):228-232 PMID: 26840485
  108. The dynamic N(1)-methyladenosine methylome in eukaryotic messenger RNA.
    Nature. 2016 Feb 25;530(7591):441-6 PMID: 26863196
  109. RNA modifications: what have we learned and where are we headed?
    Nat Rev Genet. 2016 Jun;17(6):365-72 PMID: 27140282
  110. Messenger RNA modifications: Form, distribution, and function.
    Science. 2016 Jun 17;352(6292):1408-12 PMID: 27313037
  111. Overexpression of NSUN2 by DNA hypomethylation is associated with metastatic progression in human breast cancer.
    Oncotarget. 2017 Mar 28;8(13):20751-20765 PMID: 27447970
  112. tRNA anticodon loop modifications ensure protein homeostasis and cell morphogenesis in yeast.
    Nucleic Acids Res. 2016 Dec 15;44(22):10946-10959 PMID: 27496282
  113. Nanocall: an open source basecaller for Oxford Nanopore sequencing data.
    Bioinformatics. 2017 Jan 1;33(1):49-55 PMID: 27614348
  114. Oxford Nanopore MinION Sequencing and Genome Assembly.
    Genomics Proteomics Bioinformatics. 2016 Oct;14(5):265-279 PMID: 27646134
  115. Evolving insights into RNA modifications and their functional diversity in the brain.
    Nat Neurosci. 2016 Sep 27;19(10):1292-8 PMID: 27669990
  116. Post-transcriptional gene regulation by mRNA modifications.
    Nat Rev Mol Cell Biol. 2017 Jan;18(1):31-42 PMID: 27808276
  117. Elp3 links tRNA modification to IRES-dependent translation of LEF1 to sustain metastasis in breast cancer.
    J Exp Med. 2016 Oct 17;213(11):2503-2523 PMID: 27811057
  118. m6A modulates neuronal functions and sex determination in Drosophila.
    Nature. 2016 Dec 8;540(7632):242-247 PMID: 27919077
  119. m6A potentiates Sxl alternative pre-mRNA splicing for robust Drosophila sex determination.
    Nature. 2016 Dec 8;540(7632):301-304 PMID: 27919081
  120. ALKBH1-Mediated tRNA Demethylation Regulates Translation.
    Cell. 2016 Dec 15;167(7):1897 PMID: 27984735
  121. Reversible methylation of m6Am in the 5' cap controls mRNA stability.
    Nature. 2017 Jan 19;541(7637):371-375 PMID: 28002401
  122. Epitranscriptome sequencing technologies: decoding RNA modifications.
    Nat Methods. 2016 Dec 29;14(1):23-31 PMID: 28032622
  123. m6A-dependent maternal mRNA clearance facilitates zebrafish maternal-to-zygotic transition.
    Nature. 2017 Feb 23;542(7642):475-478 PMID: 28192787
  124. Detecting RNA modifications in the epitranscriptome: predict and validate.
    Nat Rev Genet. 2017 May;18(5):275-291 PMID: 28216634
  125. Mapping DNA methylation with high-throughput nanopore sequencing.
    Nat Methods. 2017 Apr;14(4):411-413 PMID: 28218897
  126. Detecting DNA cytosine methylation using nanopore sequencing.
    Nat Methods. 2017 Apr;14(4):407-410 PMID: 28218898
  127. Wobble uridine modifications-a reason to live, a reason to die?!
    RNA Biol. 2017 Sep 2;14(9):1209-1222 PMID: 28277930
  128. Charting the unknown epitranscriptome.
    Nat Rev Mol Cell Biol. 2017 Jun;18(6):339-340 PMID: 28488699
  129. Lost in Translation: Defects in Transfer RNA Modifications and Neurological Disorders.
    Front Mol Neurosci. 2017 May 09;10:135 PMID: 28536502
  130. Multiplex PCR method for MinION and Illumina sequencing of Zika and other virus genomes directly from clinical samples.
    Nat Protoc. 2017 Jun;12(6):1261-1276 PMID: 28538739
  131. DeepNano: Deep recurrent neural networks for base calling in MinION nanopore reads.
    PLoS One. 2017 Jun 5;12(6):e0178751 PMID: 28582401
  132. The Importance of Being Modified: The Role of RNA Modifications in Translational Fidelity.
    Enzymes. 2017;41:1-50 PMID: 28601219
  133. Rethinking m6A Readers, Writers, and Erasers.
    Annu Rev Cell Dev Biol. 2017 Oct 6;33:319-342 PMID: 28759256
  134. Mapping and phasing of structural variation in patient genomes using nanopore sequencing.
    Nat Commun. 2017 Nov 6;8(1):1326 PMID: 29109544
  135. Highly parallel direct RNA sequencing on an array of nanopores.
    Nat Methods. 2018 Mar;15(3):201-206 PMID: 29334379
  136. Nanopore sequencing and assembly of a human genome with ultra-long reads.
    Nat Biotechnol. 2018 Apr;36(4):338-345 PMID: 29431738
  137. Primary and secondary structure of U2 snRNA.
    Nucleic Acids Res. 1981 Nov 11;9(21):5645-58 PMID: 6796940
  138. Mobilities of modified ribonucleotides on two-dimensional cellulose thin-layer chromatography.
    Biochimie. 1995;77(1-2):142-4 PMID: 7599271
  139. Inosine exists in mRNA at tissue-specific levels and is most abundant in brain mRNA.
    EMBO J. 1998 Feb 16;17(4):1120-7 PMID: 9463389
Article Info
Journal
RNA (New York, N.Y.)
Abbr.
RNA
ISSN
1469-9001
DOI
10.1261/rna.063503.117
Published
2017-00-00
Epub
2017-00-30
Pages
1754-1769
Language
English
Region
United States
NLM ID
9509184
PMCID
PMC5688997
Subset
IM
External Links
PubMed source DOI: 10.1261/rna.063503.117 PMC Full Text View journal details
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