1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Animal Biosciences
  4. Volume 11, 2023
  5. Article

Annual Review of Animal Biosciences

Volume 11, 2023

Extensive Recoding of the Neural Proteome in Cephalopods by RNA Editing

Abstract

The coleoid cephalopods have the largest brains, and display the most complex behaviors, of all invertebrates. The molecular and cellular mechanisms that underlie these remarkable advancements remain largely unexplored. Early molecular cloning studies of squid ion channel transcripts uncovered an unusually large number of A→I RNA editing sites that recoded codons. Further cloning of other neural transcripts showed a similar pattern. The advent of deep-sequencing technologies and the associated bioinformatics allowed the mapping of RNA editing events across the entire neural transcriptomes of various cephalopods. The results were remarkable: They contained orders of magnitude more recoding editing sites than any other taxon. Although RNA editing sites are abundant in most multicellular metazoans, they rarely recode. In cephalopods, the majority of neural transcripts are recoded. Recent studies have focused on whether these events are adaptive, as well as other noncanonical aspects of cephalopod RNA editing.

Keyword(s): adaptation, ADAR, adenosine deaminase acting on RNA, cephalopods, RNA editing
Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-060322-114534
2023-02-15
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/animal/11/1/annurev-animal-060322-114534.html?itemId=/content/journals/10.1146/annurev-animal-060322-114534&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Boccaletto P, Machnicka MA, Purta E, Piatkowski P, Baginski B et al. 2018. MODOMICS: a database of RNA modification pathways. 2017 update. Nucleic Acids Res. 46:D303–7
     [Google Scholar]
  2. 2.
    Bass BL. 2002. RNA editing by adenosine deaminases that act on RNA. Annu. Rev. Biochem. 71:817–46
     [Google Scholar]
  3. 3.
    Nishikura K. 2010. Functions and regulation of RNA editing by ADAR deaminases. Annu. Rev. Biochem. 79:321–49
     [Google Scholar]
  4. 4.
    Nishikura K. 2016. A-to-I editing of coding and non-coding RNAs by ADARs. Nat. Rev. Mol. Cell Biol. 17:83–96
     [Google Scholar]
  5. 5.
    Savva YA, Rieder LE, Reenan RA. 2012. The ADAR protein family. Genome Biol. 13:252
     [Google Scholar]
  6. 6.
    Eisenberg E, Levanon EY. 2018. A-to-I RNA editing—immune protector and transcriptome diversifier. Nat. Rev. Genet. 19:473–90
     [Google Scholar]
  7. 7.
    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
     [Google Scholar]
  8. 8.
    Rieder LE, Reenan RA. 2012. The intricate relationship between RNA structure, editing, and splicing. Semin. Cell Dev. Biol. 23:281–88
     [Google Scholar]
  9. 9.
    Basilio C, Wahba AJ, Lengyel P, Speyer JF, Ochoa S. 1962. Synthetic polynucleotides and the amino acid code, V. PNAS 48:613–16
     [Google Scholar]
  10. 10.
    Licht K, Hartl M, Amman F, Anrather D, Janisiw MP, Jantsch MF. 2019. Inosine induces context-dependent recoding and translational stalling. Nucleic Acids Res. 47:3–14
     [Google Scholar]
  11. 11.
    Bass BL, Weintraub H. 1988. An unwinding activity that covalently modifies its double-stranded RNA substrate. Cell 55:1089–98
     [Google Scholar]
  12. 12.
    Polson AG, Crain PF, Pomerantz SC, McCloskey JA, Bass BL. 1991. The mechanism of adenosine to inosine conversion by the double-stranded RNA unwinding/modifying activity: a high-performance liquid chromatography-mass spectrometry analysis. Biochemistry 30:11507–14
     [Google Scholar]
  13. 13.
    Kim U, Wang Y, Sanford T, Zeng Y, Nishikura K. 1994. Molecular cloning of cDNA for double-stranded RNA adenosine deaminase, a candidate enzyme for nuclear RNA editing. PNAS 91:11457–61
     [Google Scholar]
  14. 14.
    O'Connell MA, Keller W. 1994. Purification and properties of double-stranded RNA-specific adenosine deaminase from calf thymus. PNAS 91:10596–600
     [Google Scholar]
  15. 15.
    O'Connell MA, Krause S, Higuchi M, Hsuan JJ, Totty NF et al. 1995. Cloning of cDNAs encoding mammalian double-stranded RNA-specific adenosine deaminase. Mol. Cell. Biol. 15:1389–97
     [Google Scholar]
  16. 16.
    Melcher T, Maas S, Herb A, Sprengel R, Seeburg PH, Higuchi M. 1996. A mammalian RNA editing enzyme. Nature 379:460–64
     [Google Scholar]
  17. 17.
    Higuchi M, Single FN, Köhler M, Sommer B, Sprengel R, Seeburg PH. 1993. RNA editing of AMPA receptor subunit GluR-B: a base-paired intron-exon structure determines position and efficiency. Cell 75:1361–70
     [Google Scholar]
  18. 18.
    Sommer B, Köhler M, Sprengel R, Seeburg PH. 1991. RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67:11–19
     [Google Scholar]
  19. 19.
    Brusa R, Zimmermann F, Koh DS, Feldmeyer D, Gass P et al. 1995. Early-onset epilepsy and postnatal lethality associated with an editing-deficient GluR-B allele in mice. Science 270:1677–80
     [Google Scholar]
  20. 20.
    Rosenthal JJC, Seeburg PH. 2012. A-to-I RNA editing: effects on proteins key to neural excitability. Neuron 74:432–39
     [Google Scholar]
  21. 21.
    Seeburg PH, Higuchi M, Sprengel R. 1998. RNA editing of brain glutamate receptor channels: mechanism and physiology. Brain Res. Rev. 26:217–29
     [Google Scholar]
  22. 22.
    Niswender CM, Copeland SC, Herrick-Davis K, Emeson RB, Sanders-Bush E. 1999. RNA editing of the human serotonin 5-hydroxytryptamine 2C receptor silences constitutive activity. J. Biol. Chem. 274:9472–78
     [Google Scholar]
  23. 23.
    Burns CM, Chu H, Rueter SM, Hutchinson LK, Canton H et al. 1997. Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature 387:303–8
     [Google Scholar]
  24. 24.
    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. 11:950–56
     [Google Scholar]
  25. 25.
    Young J. 1939. Fused neurons and synaptic contacts in the giant nerve fibres of cephalopods. Philos. Trans. R. Soc. Lond. 229:465–503
     [Google Scholar]
  26. 26.
    Bullock TH, Hagiwara S. 1957. Intracellular recording from the giant synapse of the squid. J. Gen. Physiol. 40:565–77
     [Google Scholar]
  27. 27.
    Hagiwara S, Tasaki I. 1958. A study on the mechanism of impulse transmission across the giant synapse of the squid. J. Physiol. 143:114–37
     [Google Scholar]
  28. 28.
    Katz B, Miledi R. 1967. A study of synaptic transmission in the absence of nerve impulses. J. Physiol. 192:407–36
     [Google Scholar]
  29. 29.
    Hodgkin AL, Huxley AF. 1952. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117:500–44
     [Google Scholar]
  30. 30.
    Noda M, Ikeda T, Suzuki H, Takeshima H, Takahashi T et al. 1986. Expression of functional sodium channels from cloned cDNA. Nature 322:826–28
     [Google Scholar]
  31. 31.
    Levinson SR, Duch DS, Urban BW, Recio-Pinto E. 1986. The sodium channel from Electrophorus electricusa. Ann. N.Y. Acad. Sci. 479:162–78
     [Google Scholar]
  32. 32.
    Papazian DM, Schwarz TL, Tempel BL, Jan YN, Jan LY 1987. Cloning of genomic and complementary DNA from Shaker, a putative potassium channel gene from Drosophila. Science 237:749–53
     [Google Scholar]
  33. 33.
    Tempel BL, Papazian DM, Schwarz TL, Jan YN, Jan LY 1987. Sequence of a probable potassium channel component encoded at Shaker locus of Drosophila. Science 237:770–75
     [Google Scholar]
  34. 34.
    Schwarz TL, Tempel BL, Papazian DM, Jan YN, Jan LY 1988. Multiple potassium-channel components are produced by alternative splicing at the Shaker locus in Drosophila. Nature 331:137–42
     [Google Scholar]
  35. 35.
    Rosenthal JJC, Gilly WF. 1993. Amino acid sequence of a putative sodium channel expressed in the giant axon of the squid Loligo opalescens. PNAS 90:10026–30
     [Google Scholar]
  36. 36.
    Rosenthal JJC, Vickery RG, Gilly WF. 1996. Molecular identification of SqKv1A: a candidate for the delayed rectifier K channel in squid giant axon. J. Gen. Physiol. 108:207–19
     [Google Scholar]
  37. 37.
    Rosenthal JJC, Liu TI, Gilly WF. 1997. A family of delayed rectifier Kv1 cDNAs showing cell type-specific expression in the squid stellate ganglion/giant fiber lobe complex. J. Neurosci. 17:5070–79
     [Google Scholar]
  38. 38.
    Liu TI, Lebaric ZN, Rosenthal JJC, Gilly WF. 2001. Natural substitutions at highly conserved T1-domain residues perturb processing and functional expression of squid Kv1 channels. J. Neurophysiol. 85:61–71
     [Google Scholar]
  39. 39.
    Patton DE, Silva T, Bezanilla F. 1997. RNA editing generates a diverse array of transcripts encoding squid Kv2 K+ channels with altered functional properties. Neuron 19:711–22. https:/doi.org/10.1016/S0896-6273(00)80383-9
    [Google Scholar]
  40. 40.
    Rosenthal JJC, Bezanilla F. 2002. Extensive editing of mRNAs for the squid delayed rectifier K+ channel regulates subunit tetramerization. Neuron 34:743–57
     [Google Scholar]
  41. 41.
    Garrett S, Rosenthal JJC. 2012. RNA editing underlies temperature adaptation in K+ channels from polar octopuses. Science 335:848–51
     [Google Scholar]
  42. 42.
    Alon S, Garrett SC, Levanon EY, Olson S, Graveley BR et al. 2015. The majority of transcripts in the squid nervous system are extensively recoded by A-to-I RNA editing. eLife 2015:e05198
     [Google Scholar]
  43. 43.
    Liscovitch-Brauer N, Alon S, Porath HT, Elstein B, Unger R et al. 2017. Trade-off between transcriptome plasticity and genome evolution in cephalopods. Cell 169:191–202.e11
     [Google Scholar]
  44. 44.
    Rueter SM, Dawson TR, Emeson RB. 1999. Regulation of alternative splicing by RNA editing. Nature 399:75–80
     [Google Scholar]
  45. 45.
    Daniel C, Wahlstedt H, Ohlson J, Björk P, Ohman M. 2011. Adenosine-to-inosine RNA editing affects trafficking of the γ-aminobutyric acid type A (GABAA) receptor. J. Biol. Chem. 286:2031–40
     [Google Scholar]
  46. 46.
    Daniel C, Ohman M. 2009. RNA editing and its impact on GABAA receptor function. Biochem. Soc. Trans. 37:1399–403
     [Google Scholar]
  47. 47.
    Egebjerg J, Heinemann SFF. 1993. Ca2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6. PNAS 90:755–59
     [Google Scholar]
  48. 48.
    Köhler M, Burnashev N, Sakmann B, Seeburg PH. 1993. Determinants of Ca2+ permeability in both TM1 and TM2 of high affinity kainate receptor channels: diversity by RNA editing. Neuron 10:491–500
     [Google Scholar]
  49. 49.
    Huang H, Tan BZ, Shen Y, Tao J, Jiang F et al. 2012. RNA editing of the IQ domain in Cav1.3 channels modulates their Ca2+-dependent inactivation. Neuron 73:304–16
     [Google Scholar]
  50. 50.
    Bazzazi H, Ben Johny M, Adams PJ, Soong TW, Yue DT 2013. Continuously tunable Ca2+ regulation of RNA-edited CaV1.3 channels. Cell Rep. 5:367–77
     [Google Scholar]
  51. 51.
    Colina C, Palavicini JP, Srikumar D, Holmgren M, Rosenthal JJCC. 2010. Regulation of Na+/K+ ATPase transport velocity by RNA editing. PLOS Biol. 8:e1000540
     [Google Scholar]
  52. 52.
    Vallecillo-Viejo IC, Liscovitch-Brauer N, Diaz Quiroz JF, Montiel-Gonzalez MF, Nemes SE et al. 2020. Spatially regulated editing of genetic information within a neuron. Nucleic Acids Res. 48:3999–4012
     [Google Scholar]
  53. 53.
    Schrider DR, Gout J-F, Hahn MW. 2011. Very few RNA and DNA sequence differences in the human transcriptome. PLOS ONE 6:e25842
     [Google Scholar]
  54. 54.
    Kleinman CL, Majewski J. 2012. Comment on “Widespread RNA and DNA sequence differences in the human transcriptome. .” Science 335:1302; author reply 1302
    [Google Scholar]
  55. 55.
    Eisenberg E, Li JB, Levanon EY. 2010. Sequence based identification of RNA editing sites. RNA Biol. 7:248–52
     [Google Scholar]
  56. 56.
    Pickrell JK, Gilad Y, Pritchard JK. 2012. Comment on “Widespread RNA and DNA sequence differences in the human transcriptome. .” Science 335:1302
     [Google Scholar]
  57. 57.
    Lin W, Piskol R, Tan MH, Li JB. 2012. Comment on “Widespread RNA and DNA sequence differences in the human transcriptome. .” Science 335:1302
     [Google Scholar]
  58. 58.
    Piskol R, Peng Z, Wang J, Li JB 2013. Lack of evidence for existence of noncanonical RNA editing. Nat. Biotechnol. 31:19–20
     [Google Scholar]
  59. 59.
    Diroma MA, Ciaccia L, Pesole G, Picardi E. 2017. Elucidating the editome: bioinformatics approaches for RNA editing detection. Brief. Bioinform. 20:436–47
     [Google Scholar]
  60. 60.
    Levanon EY, Eisenberg E. 2006. Algorithmic approaches for identification of RNA editing sites. Brief. Funct. Genomics 5:43–45
     [Google Scholar]
  61. 61.
    Eisenberg E. 2012. Bioinformatic approaches for identification of A-to-I editing sites. Curr. Top. Microbiol. Immunol. 353:145–62
     [Google Scholar]
  62. 62.
    Ramaswami G, Li JB. 2016. Identification of human RNA editing sites: a historical perspective. Methods 107:42–47
     [Google Scholar]
  63. 63.
    Ramaswami G, Li JB. 2014. RADAR: a rigorously annotated database of A-to-I RNA editing. Nucleic Acids Res. 42:D109–13
     [Google Scholar]
  64. 64.
    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:D750–57
     [Google Scholar]
  65. 65.
    Bazak L, Haviv A, Barak M, Jacob-Hirsch J, Deng P 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. 24:365–76
     [Google Scholar]
  66. 66.
    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
     [Google Scholar]
  67. 67.
    Porath HT, Schaffer AA, Kaniewska P, Alon S, Eisenberg E et al. 2017. A-to-I RNA editing in the earliest-diverging eumetazoan phyla. Mol. Biol. Evol. 34:1890–901
     [Google Scholar]
  68. 68.
    Neeman Y, Levanon EY, Jantsch MF, Eisenberg E. 2006. RNA editing level in the mouse is determined by the genomic repeat repertoire. RNA 12:1802–9
     [Google Scholar]
  69. 69.
    Kim DDY, Kim TTY, Walsh T, Kobayashi Y, Matise TC et al. 2004. Widespread RNA editing of embedded Alu elements in the human transcriptome. Genome Res. 14:1719–25
     [Google Scholar]
  70. 70.
    Blow M, Futreal AP, Wooster R, Stratton MR. 2004. A survey of RNA editing in human brain. Genome Res. 14:2379–87
     [Google Scholar]
  71. 71.
    Athanasiadis A, Rich A, Maas S. 2004. Widespread A-to-I RNA editing of Alu-containing mRNAs in the human transcriptome. PLOS Biol. 2:e391
     [Google Scholar]
  72. 72.
    Levanon EY, Eisenberg E, Yelin R, Nemzer S, Hallegger M et al. 2004. Systematic identification of abundant A-to-I editing sites in the human transcriptome. Nat. Biotechnol. 22:1001–5
     [Google Scholar]
  73. 73.
    Gabay O, Shoshan Y, Kopel E, Ben-Zvi U, Mann TD et al. 2022. Landscape of adenosine-to-inosine RNA recoding across human tissues. Nat. Commun. 13:1184
     [Google Scholar]
  74. 74.
    Buchumenski I, Holler K, Appelbaum L, Eisenberg E, Junker JP, Levanon EY. 2021. Systematic identification of A-to-I RNA editing in zebrafish development and adult organs. Nucleic Acids Res. 49:4325–37
     [Google Scholar]
  75. 75.
    Li Q, Wang Z, Lian J, Schiøtt, Jin L et al. 2014. Caste-specific RNA editomes in the leaf-cutting ant Acromyrmex echinatior. Nat. Commun. 5:4943
     [Google Scholar]
  76. 76.
    Porath HT, Hazan E, Shpigler H, Cohen M, Band M et al. 2019. RNA editing is abundant and correlates with task performance in a social bumblebee. Nat. Commun. 10:1605
     [Google Scholar]
  77. 77.
    Duan Y, Dou S, Porath HT, Huang J, Eisenberg E, Lu J. 2021. A-to-I RNA editing in honeybees shows signals of adaptation and convergent evolution. iScience 24:101983
     [Google Scholar]
  78. 78.
    Yu Y, Zhou H, Kong Y, Pan B, Chen L et al. 2016. The landscape of A-to-I RNA editome is shaped by both positive and purifying selection. PLOS Genet. 12:e1006191
     [Google Scholar]
  79. 79.
    Duan Y, Dou S, Luo S, Zhang H, Lu J. 2017. Adaptation of A-to-I RNA editing in Drosophila. PLOS Genet. 13:e1006648
     [Google Scholar]
  80. 80.
    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
     [Google Scholar]
  81. 81.
    Albertin CB, Simakov O, Mitros T, Wang ZY, Pungor JR et al. 2015. The octopus genome and the evolution of cephalopod neural and morphological novelties. Nature 524:220–24
     [Google Scholar]
  82. 82.
    Shoshan Y, Liscovitch-Brauer N, Rosenthal JJC, Eisenberg E. 2021. Adaptive proteome diversification by nonsynonymous A-to-I RNA editing in coleoid cephalopods. Mol. Biol. Evol. 38:3775–88
     [Google Scholar]
  83. 83.
    Hanlon RT, Messenger JB. 2018. Cephalopod Behaviour Cambridge, UK: Cambridge Univ. Press. , 2nd ed..
  84. 84.
    Albertin CB, Medina-Ruiz S, Mitros T, Schmidbaur H, Sanchez G et al. 2022. Genome and transcriptome mechanisms driving cephalopod evolution. Nat. Commun. 13:2427
     [Google Scholar]
  85. 85.
    Checa AG, Cartwright JHE, Sánchez-Almazo I, Andrade JP, Ruiz-Raya F. 2015. The cuttlefish Sepia officinalis (Sepiidae, Cephalopoda) constructs cuttlebone from a liquid-crystal precursor. Sci. Rep. 5:11513
     [Google Scholar]
  86. 86.
    Kröger B, Vinther J, Fuchs D. 2011. Cephalopod origin and evolution: a congruent picture emerging from fossils, development and molecules: Extant cephalopods are younger than previously realised and were under major selection to become agile, shell-less predators. BioEssays 33:602–13
     [Google Scholar]
  87. 87.
    Garrett SC, Rosenthal JJC. 2012. A role for A-to-I RNA editing in temperature adaptation. Physiology 27:362–69
     [Google Scholar]
  88. 88.
    Tan MH, Li Q, Shanmugam R, Piskol R, Kohler J et al. 2017. Dynamic landscape and regulation of RNA editing in mammals. Nature 550:249–54
     [Google Scholar]
  89. 89.
    Wahlstedt H, Daniel C, Ensterö M, Ohman M. 2009. Large-scale mRNA sequencing determines global regulation of RNA editing during brain development. Genome Res. 19:978–86
     [Google Scholar]
  90. 90.
    Moldovan M, Chervontseva Z, Bazykin G, Gelfand MS. 2020. Adaptive evolution at mRNA editing sites in soft-bodied cephalopods. PeerJ 8:e10456
     [Google Scholar]
  91. 91.
    Herb A, Higuchi M, Sprengel R, Seeburg PH. 1996. Q/R site editing in kainate receptor GluR5 and GluR6 pre-mRNAs requires distant intronic sequences. PNAS 93:1875–80
     [Google Scholar]
  92. 92.
    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 14:211–16
     [Google Scholar]
  93. 93.
    Zhang S-J, Liu C-J, Yu P, Zhong X, Chen J-Y et al. 2014. Evolutionary interrogation of human biology in well-annotated genomic framework of rhesus macaque. Mol. Biol. Evol. 31:1309–24
     [Google Scholar]
  94. 94.
    An NA, Ding W, Yang X-Z, Peng J, He BZ et al. 2019. Evolutionarily significant A-to-I RNA editing events originated through G-to-A mutations in primates. Genome Biol. 20:24
     [Google Scholar]
  95. 95.
    Jiang D, Zhang J. 2019. The preponderance of nonsynonymous A-to-I RNA editing in coleoids is nonadaptive. Nat. Commun. 10:5411
     [Google Scholar]
  96. 96.
    Rieder LE, Savva YA, Reyna MA, Chang Y-J, Dorsky JS et al. 2015. Dynamic response of RNA editing to temperature in Drosophila. BMC Biol. 13:1
     [Google Scholar]
  97. 97.
    Popitsch N, Huber CD, Buchumenski I, Eisenberg E, Jantsch M et al. 2020. A-to-I RNA editing uncovers hidden signals of adaptive genome evolution in animals. Genome Biol. Evol. 12:345–57
     [Google Scholar]
  98. 98.
    Duan Y, Dou S, Zhang H, Wu C, Wu M et al. 2018. Linkage of A-to-I RNA editing in metazoans and the impact on genome evolution. Mol. Biol. Evol. 35:132–48
     [Google Scholar]
  99. 99.
    Marion S, Weiner DM, Caron MG. 2004. RNA editing induces variation in desensitization and trafficking of 5-hydroxytryptamine 2c receptor isoforms. J. Biol. Chem. 279:2945–54
     [Google Scholar]
  100. 100.
    Khermesh K, D-Erchia AM, Barak M, Annese A, Wachtel C et al. 2016. Reduced levels of protein recoding by A-to-I RNA editing in Alzheimer's disease. RNA 22:290–302
     [Google Scholar]
  101. 101.
    Zaidan H, Ramaswami G, Golumbic YN, Sher N, Malik A 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 Genom. 19:28
     [Google Scholar]
  102. 102.
    O'Connell MA, Gerber A, Keller W. 1997. Purification of human double-stranded RNA-specific editase 1 (hRED1) involved in editing of brain glutamate receptor B pre-mRNA. J. Biol. Chem. 272:473–78
     [Google Scholar]
  103. 103.
    Gerber A, O'Connell MA, Keller W. 1997. Two forms of human double-stranded RNA-specific editase 1 (hRED1) generated by the insertion of an Alu cassette. RNA 3:453–63
     [Google Scholar]
  104. 104.
    Yang J-H, Sklar P, Axel R, Maniatis T 1997. Purification and characterization of a human RNA adenosine deaminase for glutamate receptor B pre-mRNA editing. PNAS 94:4354–59
     [Google Scholar]
  105. 105.
    Yang J-H, Nie Y, Zhao Q, Su Y, Pypaert M et al. 2003. Intracellular localization of differentially regulated ADAR1 isoforms in inflammation. Biochemistry 693:45833–42
     [Google Scholar]
  106. 106.
    George CX, Wagner MV, Samuel CE. 2005. Expression of interferon-inducible RNA adenosine deaminase ADAR1 during pathogen infection and mouse embryo development involves tissue-selective promoter utilization and alternative splicing. J. Biol. Chem. 280:15020–28
     [Google Scholar]
  107. 107.
    Liddicoat BJ, Piskol R, Chalk AM, Ramaswami G, Higuchi M et al. 2015. RNA editing by ADAR1 prevents MDA5 sensing of endogenous dsRNA as nonself. Science 349:1115–20
     [Google Scholar]
  108. 108.
    Mannion NM, Greenwood SM, Young R, Cox S, Brindle J et al. 2014. The RNA-editing enzyme ADAR1 controls innate immune responses to RNA. Cell Rep. 9:1482–94
     [Google Scholar]
  109. 109.
    Palavicini JP, O'Connell MA, Rosenthal JJC 2009. An extra double-stranded RNA binding domain confers high activity to a squid RNA editing enzyme. RNA 15:1208–18
     [Google Scholar]
  110. 110.
    Palavicini JP, Correa-Rojas RA, Rosenthal JJC. 2012. Extra double-stranded RNA binding domain (dsRBD) in a squid RNA editing enzyme confers resistance to high salt environment. J. Biol. Chem. 287:17754–64
     [Google Scholar]
  111. 111.
    Hwang T, Park C-K, Leung AKL, Gao Y, Hyde TM et al. 2016. Dynamic regulation of RNA editing in human brain development and disease. Nat. Neurosci. 19:1093–99
     [Google Scholar]
  112. 112.
    Silvestris DA, Picardi E, Cesarini V, Fosso B, Mangraviti N et al. 2019. Dynamic inosinome profiles reveal novel patient stratification and gender-specific differences in glioblastoma. Genome Biol. 20:33
     [Google Scholar]
  113. 113.
    Desterro JMP, Keegan LP, Lafarga M, Berciano MT, O'Connell M, Carmo-Fonseca M 2003. Dynamic association of RNA-editing enzymes with the nucleolus. J. Cell Sci. 116:1805–18
     [Google Scholar]
  114. 114.
    Maas S, Gommans WM. 2009. Identification of a selective nuclear import signal in adenosine deaminases acting on RNA. Nucleic Acids Res. 37:5822–29
     [Google Scholar]
  115. 115.
    Sansam CL, Wells KS, Emeson RB. 2003. Modulation of RNA editing by functional nucleolar sequestration of ADAR2. PNAS 100:14018–23
     [Google Scholar]
  116. 116.
    Fritz J, Strehblow A, Taschner A, Schopoff S, Pasierbek P, Jantsch MF. 2009. RNA-regulated interaction of transportin-1 and exportin-5 with the double-stranded RNA-binding domain regulates nucleocytoplasmic shuttling of ADAR1. Mol. Cell. Biol. 29:1487–97
     [Google Scholar]
  117. 117.
    Strehblow A, Hallegger M, Jantsch MF. 2002. Nucleocytoplasmic distribution of human RNA-editing enzyme ADAR1 is modulated by double-stranded RNA-binding domains, a leucine-rich export signal, and a putative dimerization domain. Mol. Biol. Cell 13:3822–35
     [Google Scholar]
  118. 118.
    Bazak L, Levanon EY, Eisenberg E. 2014. Genome-wide analysis of Alu editability. Nucleic Acids Res. 42:6876–84
     [Google Scholar]
  119. 119.
    Roth SH, Levanon EY, Eisenberg E. 2019. Genome-wide quantification of ADAR adenosine-to-inosine RNA editing activity. Nat. Methods 16:1131–38
     [Google Scholar]
  120. 120.
    Maas S, Melcher T, Herb A, Seeburg PH, Keller W et al. 1996. Structural requirements for RNA editing in glutamate receptor pre-mRNAs by recombinant double-stranded RNA adenosine deaminase. J. Biol. Chem. 271:12221–26
     [Google Scholar]
  121. 121.
    Reenan RA. 2005. Molecular determinants and guided evolution of species-specific RNA editing. Nature 434:409–13
     [Google Scholar]
  122. 122.
    Crawford K, Diaz Quiroz JF, Koenig KM, Ahuja N, Albertin CB, Rosenthal JJC 2020. Highly efficient knockout of a squid pigmentation gene. Curr. Biol. 30:3484–90.e4
     [Google Scholar]
  123. 123.
    Licht K, Kapoor U, Amman F, Picardi E, Martin D et al. 2019. A high resolution A-to-I editing map in the mouse identifies editing events controlled by pre-mRNA splicing. Genome Res. 29:1453–63
     [Google Scholar]
  124. 124.
    Zhao H-Q, Zhang P, Gao H, He X, Dou Y et al. 2015. Profiling the RNA editomes of wild-type C. elegans and ADAR mutants. Genome Res. 25:66–75
     [Google Scholar]
/content/journals/10.1146/annurev-animal-060322-114534
Loading
Extensive Recoding of the Neural Proteome in Cephalopods by RNA Editing
Annual Review of Animal Biosciences 11, 57 (2023); https://doi.org/10.1146/annurev-animal-060322-114534
/content/journals/10.1146/annurev-animal-060322-114534
/content/journals/10.1146/annurev-animal-060322-114534
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error