RNA Editing pp 229-251 | Cite as

Proteome Diversification by RNA Editing

  • Eli EisenbergEmail author
Part of the Methods in Molecular Biology book series (MIMB, volume 2181)


手机体育投注平台RNA editing is an RNA modification that alters the RNA sequence relative to its genomic blueprint. The most common type of RNA editing is A-to-I editing by double-stranded RNA-specific adenosine deaminase (ADAR) enzymes. Editing of a protein-coding region within the RNA molecule may result in non-synonymous substitutions, leading to a modified protein product. These editing sites, also known as “recoding” sites, contribute to the complexity and diversification of the proteome. Recent computational transcriptomic studies have identified thousands of recoding sites in multiple species, many of which are conserved within (but not usually across) lineages and have functional and evolutionary importance. In this chapter we describe the recoding phenomenon across species, consider its potential utility for diversity and adaptation, and discuss its evolution.

Key words

RNA editing ADAR Recoding 


  1. 1.
    Bass BL (2002) RNA editing by adenosine deaminases that act on RNA. Annu Rev Biochem 71:817–846.  
  2. 2.
    Nishikura K (2016) A-to-I editing of coding and non-coding RNAs by ADARs. Nat Rev Mol Cell Biol 17:83–96.  
  3. 3.
    Eisenberg E, Levanon EY (2018) A-to-I RNA editing—immune protector and transcriptome diversifier. Nat Rev Genet 19:473–490.  
  4. 4.
    Lonsdale J, Thomas J, Salvatore M et al (2013) The genotype-tissue expression (GTEx) project. Nat Genet 45:580–585.  
  5. 5.
    Bass BL, Weintraub H (1988) An unwinding activity that covalently modifies its double-stranded RNA substrate. Cell 55:1089–1098.  
  6. 6.
    Rebagliati MR, Melton DA (1987) Antisense RNA injections in fertilized frog eggs reveal an RNA duplex unwinding activity. Cell 48:599–605
  7. 7.
    Pestal K, Funk CC, Snyder JM et al (2015) Isoforms of RNA-editing enzyme ADAR1 independently control nucleic acid sensor MDA5-driven autoimmunity and multi-organ development. Immunity 43:933–944.  
  8. 8.
    Liddicoat BJ, Piskol R, Chalk AM et al (2015) RNA editing by ADAR1 prevents MDA5 sensing of endogenous dsRNA as nonself. Science 349:1115–1120.  
  9. 9.
    Mannion NM, Greenwood SM, Young R et al (2014) The RNA-editing enzyme ADAR1 controls innate immune responses to RNA. Cell Rep 9:1482–1494.  
  10. 10.
    Porath HT, Knisbacher BA, Eisenberg E, Levanon EY (2017) Massive A-to-I RNA editing is common across the Metazoa and correlates with dsRNA abundance. Genome Biol 18:185.  
  11. 11.
    Porath HT, Schaffer A, Kaniewska P et al (2017) A-to-I RNA editing in the earliest-diverging eumetazoan phyla. Mol Biol Evol 34(8):1890–1901.  
  12. 12.
    Neeman Y, Levanon EY, Jantsch MF, Eisenberg E (2006) RNA editing level in the mouse is determined by the genomic repeat repertoire. RNA 12:1802–1809
  13. 13.
    Pinto Y, Buchumenski I, Levanon EY, Eisenberg E (2017) Human cancer tissues exhibit reduced A-to-I editing of miRNAs coupled with elevated editing of their targets. Nucleic Acids Res 46(1):71–82.  
  14. 14.
    Kawahara Y, Zinshteyn B, Sethupathy P et al (2007) Redirection of silencing targets by adenosine-to-inosine editing of miRNAs. Science 315:1137–1140.  
  15. 15.
    Wang Y, Xu X, Yu S et al (2017) Systematic characterization of A-to-I RNA editing hotspots in microRNAs across human cancers. Genome Res 27:1112–1125.  
  16. 16.
    Vesely C, Tauber S, Sedlazeck FJ et al (2012) Adenosine deaminases that act on RNA induce reproducible changes in abundance and sequence of embryonic miRNAs. Genome Res 22:1468–1476
  17. 17.
    Alon S, Mor E, Vigneault F (2012) Systematic identification of edited microRNAs in the human brain systematic identification of edited microRNAs in the human. Genome Res 22:1533–1540.  
  18. 18.
    Ivanov A, Memczak S, Wyler E et al (2014) Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals. Cell Rep 10:170–177.  
  19. 19.
    Basilio C, Wahba AJ, Lengyel P et al (1962) Synthetic polynucleotides and the amino acid code. Proc Natl Acad Sci U S A 48:613–616
  20. 20.
    Licht K, Hartl M, Amman F et al (2019) Inosine induces context-dependent recoding and translational stalling. Nucleic Acids Res 47:3–14.  
  21. 21.
    Rueter SM, Dawson TR, Emeson RB (1999) Regulation of alternative splicing by RNA editing. Nature 399:75–80.  
  22. 22.
    Lev-Maor G, Sorek R, Levanon EY et al (2007) RNA-editing-mediated exon evolution. Genome Biol 8:R29.  
  23. 23.
    Tan MH, Li Q, Shanmugam R et al (2017) Dynamic landscape and regulation of RNA editing in mammals. Nature 550:249–254.  
  24. 24.
    Benne R, Van den Burg J, Brakenhoff JP et al (1986) Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell 46:819–826
  25. 25.
    Estévez AM, Simpson L (1999) Uridine insertion/deletion RNA editing in trypanosome mitochondria—a review. Gene 240:247–260
  26. 26.
    Covello PS, Gray MW (1989) RNA editing in plant mitochondria. Nature 341:662–666.  
  27. 27.
    Gualberto JM, Lamattina L, Bonnard G et al (1989) RNA editing in wheat mitochondria results in the conservation of protein sequences. Nature 341:660–662.  
  28. 28.
    Hiesel R, Wissinger B, Schuster W, Brennicke A (1989) RNA editing in plant mitochondria. Science 246:1632–1634
  29. 29.
    Takenaka M, Verbitskiy D, Zehrmann A et al (2014) RNA editing in plant mitochondria—connecting RNA target sequences and acting proteins. Mitochondrion 19:191–197.  
  30. 30.
    Chen SH, Habib G, Yang CY et al (1987) Apolipoprotein B-48 is the product of a messenger RNA with an organ-specific in-frame stop codon. Science 238:363–366
  31. 31.
    Rosenberg BR, Hamilton CE, Mwangi MM et al (2011) Transcriptome-wide sequencing reveals numerous APOBEC1 mRNA-editing targets in transcript 3′ UTRs. Nat Struct Mol Biol 18:230–236.  
  32. 32.
    Schrider DR, Gout J-F, Hahn MW (2011) Very few RNA and DNA sequence differences in the human transcriptome. PLoS One 6:e25842.  
  33. 33.
    Kleinman CL, Majewski J (2012) Comment on “Widespread RNA and DNA sequence differences in the human transcriptome”. Science 335:1302.  ; author reply 1302. 335/6074/1302-c [pii]
  34. 34.
    Eisenberg E, Li JB, Levanon EY (2010) Sequence based identification of RNA editing sites. RNA Biol 7:248–252.  
  35. 35.
    Pickrell JK, Gilad Y, Pritchard JK (2012) Comment on “Widespread RNA and DNA sequence differences in the human transcriptome”. Science 335:1302–1302.  
  36. 36.
    Lin W, Piskol R, Tan MH, Li JB (2012) Comment on “Widespread RNA and DNA sequence differences in the human transcriptome”. Science 335:1302–1302.  
  37. 37.
    Piskol R, Peng Z, Wang J, Li JB (2013) Lack of evidence for existence of noncanonical RNA editing. Nat Biotechnol 31:19–20.  
  38. 38.
    Diroma MA, Ciaccia L, Pesole G, Picardi E (2017) Elucidating the editome: bioinformatics approaches for RNA editing detection. Brief Bioinform 20(2):436–447.  
  39. 39.
    Levanon EY, Eisenberg E (2006) Algorithmic approaches for identification of RNA editing sites. Brief Funct Genom Proteom 5:43–45.  
  40. 40.
    Eisenberg E (2012) Bioinformatic approaches for identification of A-to-I editing sites. Curr Top Microbiol Immunol 353:145–162.  
  41. 41.
    Ramaswami G, Li JB (2016) Identification of human RNA editing sites: a historical perspective. Methods 107:42–47.  
  42. 42.
    Ramaswami G, Li JB (2014) RADAR: a rigorously annotated database of A-to-I RNA editing. Nucleic Acids Res 42:D109–D113.  
  43. 43.
    Picardi E, D’Erchia AM, Lo Giudice C, Pesole G (2017) REDIportal: a comprehensive database of A-to-I RNA editing events in humans. Nucleic Acids Res 45:D750–D757.  
  44. 44.
    Bazak L, Haviv A, Barak M et al (2014) A-to-I RNA editing occurs at over a hundred million genomic sites, located in a majority of human genes. Genome Res 24:365–376.  
  45. 45.
    Pinto Y, Cohen HY, Levanon EY (2014) Mammalian conserved ADAR targets comprise only a small fragment of the human editosome. Genome Biol 15:R5.  
  46. 46.
    Hoopengardner B, Bhalla T, Staber C, Reenan R (2003) Nervous system targets of RNA editing identified by comparative genomics. Science 301:832–836.  
  47. 47.
    Levanon EY, Hallegger M, Kinar Y et al (2005) Evolutionarily conserved human targets of adenosine to inosine RNA editing. Nucleic Acids Res 33:1162–1168.  
  48. 48.
    Sommer B, Kohler M, Sprengel R, Seeburg PH (1991) RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67:11–19. 0092-8674(91)90568-J [pii]
  49. 49.
    Lomeli H, Mosbacher J, Melcher T et al (1994) Control of kinetic properties of AMPA receptor channels by nuclear RNA editing. Science 266:1709–1713.  
  50. 50.
    Burns CM, Chu H, Rueter SM et al (1997) Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature 387:303–308.  
  51. 51.
    Higuchi M, Single FN, Köhler M et al (1993) RNA editing of AMPA receptor subunit GluR-B: a base-paired intron-exon structure determines position and efficiency. Cell 75:1361–1370.  
  52. 52.
    Seeburg PH, Hartner J (2003) Regulation of ion channel/neurotransmitter receptor function by RNA editing. Curr Opin Neurobiol 13:279–283
  53. 53.
    Kwak S, Kawahara Y (2005) Deficient RNA editing of GluR2 and neuronal death in amyotrophic lateral sclerosis. J Mol Med 83:110–120.  
  54. 54.
    Maas S, Patt S, Schrey M, Rich A (2001) Underediting of glutamate receptor GluR-B mRNA in malignant gliomas. Proc Natl Acad Sci U S A 98:14687–14692.  
  55. 55.
    Kawahara Y, Ito K, Sun H et al (2004) Glutamate receptors: RNA editing and death of motor neurons. Nature 427:801.  
  56. 56.
    Higuchi M, Maas S, Single FN et al (2000) Point mutation in an AMPA receptor gene rescues lethality in mice deficient in the RNA-editing enzyme ADAR2. Nature 406:78–81.  
  57. 57.
    Horsch M, Seeburg PH, Adler T et al (2011) Requirement of the RNA-editing enzyme ADAR2 for normal physiology in mice. J Biol Chem 286:18614–18622.  
  58. 58.
    Marion S, Weiner DM, Caron MG (2004) RNA editing induces variation in desensitization and trafficking of 5-hydroxytryptamine 2c receptor isoforms. J Biol Chem 279:2945–2954.  
  59. 59.
    Wang Q, Khillan J, Gadue P, Nishikura K (2000) Requirement of the RNA editing deaminase ADAR1 gene for embryonic erythropoiesis. Science 290:1765–1768.  
  60. 60.
    Wahlstedt H, Daniel C, Ensterö M, Öhman M (2009) Large-scale mRNA sequencing determines global regulation of RNA editing during brain development. Genome Res 19(6):978–986.  
  61. 61.
    Khermesh K, Erchia AMD, Barak M et al (2016) Reduced levels of protein recoding by A-to-I RNA editing in Alzheimer’s disease. RNA 22:1–13.  
  62. 62.
    Zaidan H, Ramaswami G, Golumbic YN et al (2018) A-to-I RNA editing in the rat brain is age-dependent, region-specific and sensitive to environmental stress across generations. BMC Genomics 19:28.  
  63. 63.
    Niswender CM, Copeland SC, Herrick-Davis K et al (1999) RNA editing of the human serotonin 5-hydroxytryptamine 2C receptor silences constitutive activity. J Biol Chem 274:9472–9478.  
  64. 64.
    Price RD, Weiner DM, Chang MS, Sanders-Bush E (2001) RNA editing of the human serotonin 5-HT2C receptor alters receptor-mediated activation of G13 protein. J Biol Chem 276:44663–44668.  
  65. 65.
    Kawahara Y, Grimberg A, Teegarden S et al (2008) Dysregulated editing of serotonin 2C receptor mRNAs results in energy dissipation and loss of fat mass. J Neurosci 28:12834–12844. 28/48/12834 [pii]\r10.1523/JNEUROSCI.3896-08.2008
  66. 66.
    Englander MT, Dulawa SC, Bhansali P, Schmauss C (2005) How stress and fluoxetine modulate serotonin 2C receptor pre-mRNA editing. J Neurosci 25:648–651.  
  67. 67.
    Iwamoto K, Bundo M, Kato T (2009) Serotonin receptor 2C and mental disorders: genetic, expression and RNA editing studies. RNA Biol 6:248–253
  68. 68.
    Clutterbuck DR, Leroy A, O’Connell MA, Semple CAM (2005) A bioinformatic screen for novel A-I RNA editing sites reveals recoding editing in BC10. Bioinformatics 21:2590–2595.  
  69. 69.
    Kiran A, Baranov PV (2010) DARNED: a DAtabase of RNa EDiting in humans. Bioinformatics 26:1772–1776.  
  70. 70.
    Riedmann EM, Schopoff S, Hartner JC et al (2008) Specificity of ADAR-mediated RNA editing in newly identified targets specificity of ADAR-mediated RNA editing in newly identified targets. RNA 14:1110–1118.  
  71. 71.
    Chen L, Li Y, Lin CH et al (2013) Recoding RNA editing of AZIN1 predisposes to hepatocellular carcinoma. Nat Med 19:209–216.  
  72. 72.
    Yeo J, Goodman RA, Schirle NT et al (2010) RNA editing changes the lesion specificity for the DNA repair enzyme NEIL1. Proc Natl Acad Sci U S A 107:20715–20719.  
  73. 73.
    Bhalla T, Rosenthal JJC, Holmgren M, Reenan R (2004) Control of human potassium channel inactivation by editing of a small mRNA hairpin. Nat Struct Mol Biol 11:950–956.  
  74. 74.
    Daniel C, Wahlstedt H, Ohlson J et al (2011) Adenosine-to-inosine RNA editing affects trafficking of the gamma-aminobutyric acid type A (GABA(A)) receptor. J Biol Chem 286:2031–2040.  
  75. 75.
    Egebjerg J, Heinemann SF (1993) Ca2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6. Proc Natl Acad Sci U S A 90:755–759
  76. 76.
    Sailer A, Swanson GT, Pérez-Otaño I et al (1999) Generation and analysis of GluR5(Q636R) kainate receptor mutant mice. J Neurosci 19:8757–8764
  77. 77.
    Miyake K, Ohta T, Nakayama H et al (2016) CAPS1 RNA editing promotes dense Core vesicle exocytosis. Cell Rep 17:2004–2014.  
  78. 78.
    Jain M, Mann TD, Stulić M et al (2018) RNA editing of Filamin A pre-mRNA regulates vascular contraction and diastolic blood pressure. EMBO J 37:e94813.  
  79. 79.
    Xu G, Zhang J (2014) Human coding RNA editing is generally nonadaptive. Proc Natl Acad Sci U S A 111:3769–3774.  
  80. 80.
    St Laurent G, Tackett MR, Nechkin S et al (2013) Genome-wide analysis of A-to-I RNA editing by single-molecule sequencing in Drosophila. Nat Struct Mol Biol 20:1333–1339.  
  81. 81.
    Yu Y, Zhou H, Kong Y et al (2016) The landscape of A-to-I RNA editome is shaped by both positive and purifying selection. PLoS Genet 12:e1006191.  
  82. 82.
    Duan Y, Dou S, Luo S et al (2017) Adaptation of A-to-I RNA editing in Drosophila. PLoS Genet 13:e1006648.  
  83. 83.
    Zhang R, Deng P, Jacobson D, Li JB (2017) Evolutionary analysis reveals regulatory and functional landscape of coding and non-coding RNA editing. PLoS Genet 13:e1006563.  
  84. 84.
    Keegan LP, McGurk L, Palavicini JP et al (2011) Functional conservation in human and Drosophila of Metazoan ADAR2 involved in RNA editing: loss of ADAR1 in insects. Nucleic Acids Res 39:7249–7262.  
  85. 85.
    Palladino MJ, Keegan LP, O’Connell MA, Reenan RA (2000) A-to-I pre-mRNA editing in Drosophila is primarily involved in adult nervous system function and integrity. Cell 102:437–449.  
  86. 86.
    Palladino MJ, Keegan LP, O’Connell MA, Reenan RA (2000) dADAR, a Drosophila double-stranded RNA-specific adenosine deaminase is highly developmentally regulated and is itself a target for RNA editing [In Process Citation]. RNA 6:1004–1018.  
  87. 87.
    Alon S, Garrett SC, Levanon EY et al (2015) The majority of transcripts in the squid nervous system are extensively recoded by A-to-I RNA editing. Elife 4:e05198
  88. 88.
    Liscovitch-Brauer N, Alon S, Porath HT et al (2017) Trade-off between transcriptome plasticity and genome evolution in cephalopods. Cell 169:191–202.e11.  
  89. 89.
    Li I-C, Chen Y-C, Wang Y-Y et al (2014) Zebrafish Adar2 edits the Q/R site of AMPA receptor subunit gria2α transcript to ensure normal development of nervous system and cranial neural crest cells. PLoS One 9:e97133.  
  90. 90.
    Pozo P, Hoopengardner B (2012) Identification and characterization of two novel RNA editing sites in grin1b transcripts of embryonic Danio rerio. Neural Plast 2012:1–7.  
  91. 91.
    Sie CP, Maas S (2009) Conserved recoding RNA editing of vertebrate C1q-related factor C1QL1. FEBS Lett 583:1171–1174.  
  92. 92.
    Shamay-Ramot A, Khermesh K, Porath HT et al (2015) Fmrp interacts with Adar and regulates RNA editing, synaptic density and locomotor activity in zebrafish. PLoS Genet 11:e1005702.  
  93. 93.
    Li Q, Wang Z, Lian J et al (2014) Caste-specific RNA editomes in the leaf-cutting ant Acromyrmex echinatior. Nat Commun 5:4943.  
  94. 94.
    Porath HT, Hazan E, Shpigler H et al (2019) RNA editing is abundant and correlates with task performance in a social bumblebee. Nat Commun 10:1605.  
  95. 95.
    Gommans WM, Mullen SP, Maas S (2009) RNA editing: a driving force for adaptive evolution? BioEssays 31:1137–1145.  
  96. 96.
    Terajima H, Yoshitane H, Ozaki H et al (2016) ADARB1 catalyzes circadian A-to-I editing and regulates RNA rhythm. Nat Genet 49:146–151.  
  97. 97.
    Robinson JE, Paluch J, Dickman DK, Joiner WJ (2016) ADAR-mediated RNA editing suppresses sleep by acting as a brake on glutamatergic synaptic plasticity. Nat Commun 7:10512.  
  98. 98.
    Gallo A, Vukic D, Michalík D et al (2017) ADAR RNA editing in human disease; more to it than meets the I. Hum Genet 136:1265–1278.  
  99. 99.
    Garrett S, Rosenthal JJC (2012) RNA editing underlies temperature adaptation in K+ channels from polar octopuses. Science 335:848–851.  
  100. 100.
    Yablonovitch AL, Fu J, Li K et al (2017) Regulation of gene expression and RNA editing in Drosophila adapting to divergent microclimates. Nat Commun 8:1570.  
  101. 101.
    Yablonovitch AL, Deng P, Jacobson D, Li JB (2017) The evolution and adaptation of A-to-I RNA editing. PLoS Genet 13:e1007064.  
  102. 102.
    Greenberger S, Levanon EY, Paz-Yaacov N et al (2010) Consistent levels of A-to-I RNA editing across individuals in coding sequences and non-conserved Alu repeats. BMC Genomics 11:608.  
  103. 103.
    Picardi E, Manzari C, Mastropasqua F et al (2015) Profiling RNA editing in human tissues: towards the inosinome Atlas. Sci Rep 5:14941.  
  104. 104.
    Oakes E, Anderson A, Cohen-Gadol A, Hundley HA (2017) Adenosine deaminase that acts on RNA 3 (ADAR3) binding to glutamate receptor subunit B pre-mRNA inhibits RNA editing in glioblastoma. J Biol Chem 292:4326–4335.  
  105. 105.
    Marcucci R, Brindle J, Paro S et al (2011) Pin1 and WWP2 regulate GluR2 Q/R site RNA editing by ADAR2 with opposing effects. EMBO J 30:4211–4222.  
  106. 106.
    Behm M, Wahlstedt H, Widmark A et al (2017) Accumulation of nuclear ADAR2 regulates adenosine-to-inosine RNA editing during neuronal development. J Cell Sci 130:745–753.  
  107. 107.
    Garncarz W, Tariq A, Handl C et al (2013) A high-throughput screen to identify enhancers of ADAR-mediated RNA-editing. RNA Biol 10:192–204.  
  108. 108.
    Savva YA, Jepson JEC, Sahin A et al (2012) Auto-regulatory RNA editing fine-tunes mRNA re-coding and complex behaviour in Drosophila. Nat Commun 3:790.  
  109. 109.
    Rieder LE, Savva YA, Reyna MA et al (2015) Dynamic response of RNA editing to temperature in Drosophila. BMC Biol 13:1.  
  110. 110.
    Buchumenski I, Bartok O, Ashwal-Fluss R et al (2017) Dynamic hyper-editing underlies temperature adaptation in Drosophila. PLoS Genet 13:e1006931.  
  111. 111.
    Garrett SC, Rosenthal JJC (2012) A role for A-to-I RNA editing in temperature adaptation. Physiology 27:362–369.  
  112. 112.
    Riemondy KA, Gillen AE, White EA et al (2018) Dynamic temperature-sensitive A-to-I RNA editing in the brain of a heterothermic mammal during hibernation. RNA 24:1481–1495.  
  113. 113.
    Reenan RA (2005) Molecular determinants and guided evolution of species-specific RNA editing. Nature 434:409–413.  
  114. 114.
    Rieder LE, Staber CJ, Hoopengardner B, Reenan RA (2013) Tertiary structural elements determine the extent and specificity of messenger RNA editing. Nat Commun 4:2232.  
  115. 115.
    Gal-Mark N, Shallev L, Sweetat S et al (2017) Abnormalities in A-to-I RNA editing patterns in CNS injuries correlate with dynamic changes in cell type composition. Sci Rep 7:43421.  
  116. 116.
    Picardi E, Horner DS, Pesole G (2017) Single-cell transcriptomics reveals specific RNA editing signatures in the human brain. RNA 23:860–865.  
  117. 117.
    Daniel C, Silberberg G, Behm M, Ohman M (2014) Alu elements shape the primate transcriptome by cis-regulation of RNA editing. Genome Biol 15:R28.  
  118. 118.
    Sapiro AL, Deng P, Zhang R, Li JB (2015) Cis regulatory effects on A-to-I RNA editing in related drosophila species. Cell Rep 11:697–703.  
  119. 119.
    Kung SS, Chen YC, Lin WH et al (2001) Q/R RNA editing of the AMPA receptor subunit 2 (GRIA2) transcript evolves no later than the appearance of cartilaginous fishes. FEBS Lett 509:277–281
  120. 120.
    Sorek R, Lev-Maor G, Reznik M et al (2004) Minimal conditions for exonization of intronic sequences: 5′ splice site formation in Alu exons. Mol Cell 14:221–231.  
  121. 121.
    Bazak L, Levanon EY, Eisenberg E (2014) Genome-wide analysis of Alu editability. Nucleic Acids Res 42:6876–6884.  
  122. 122.
    Dagan T, Sorek R, Sharon E et al (2004) AluGene: a database of Alu elements incorporated within protein-coding genes. Nucleic Acids Res 32:D489–D492.  
  123. 123.
    Ramaswami G, Deng P, Zhang R et al (2015) Genetic mapping uncovers cis-regulatory landscape of RNA editing. Nat Commun 6:8194.  
  124. 124.
    Daniel C, Widmark A, Rigardt D, Öhman M (2017) Editing inducer elements increases A-to-I editing efficiency in the mammalian transcriptome. Genome Biol 18:195.  
  125. 125.
    Daniel C, Venø MT, Ekdahl Y et al (2012) A distant cis acting intronic element induces site-selective RNA editing. Nucleic Acids Res 40:9876–9886.  
  126. 126.
    Morgantini C, Jager J, Li X et al (2019) Liver macrophages regulate systemic metabolism through non-inflammatory factors. Nat Metab 1:445–459.  
  127. 127.
    Tian N, Wu X, Zhang Y, Jin Y (2008) A-to-I editing sites are a genomically encoded G: implications for the evolutionary significance and identification of novel editing sites. RNA 14:211–216.  
  128. 128.
    Ohlson J, Pedersen JS, Haussler D, Ohman M (2007) Editing modifies the GABA(A) receptor subunit alpha3. RNA 13:698–703.  

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Authors and Affiliations

  1. 1.Raymond and Beverly Sackler School of Physics and Astronomy and Sagol School of NeuroscienceTel Aviv UniversityTel AvivIsrael

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