Advertisement

Biochemistry (Moscow)

, Volume 84, Issue 8, pp 896–904 | Cite as

RNA Editing by ADAR Adenosine Deaminases: From Molecular Plasticity of Neural Proteins to the Mechanisms of Human Cancer

  • A. O. Goncharov
  • A. A. Kliuchnikova
  • S. S. Nasaev
  • S. A. MoshkovskiiEmail author
Review
  • 1 Downloads

Abstract

RNA editing by adenosine deaminases of the ADAR family attracts a growing interest of researchers, both zoologists studying ecological and evolutionary plasticity of invertebrates and medical biochemists focusing on the mechanisms of cancer and other human diseases. These enzymes deaminate adenosine residues in the double-stranded (ds) regions of RNA with the formation of inosine. As a result, some RNAs change their three-dimensional structure and functions. Adenosine-to-inosine editing in the mRNA coding sequences may cause amino acid substitutions in the encoded proteins. Here, we reviewed current concepts on the functions of two active ADAR isoforms identified in mammals (including humans). The ADAR1 protein, which acts non-specifically on extended dsRNA regions, is capable of immunosuppression via inactivation of the dsRNA interactions with specific sensors inducing the cell immunity. Expression of a specific ADAR1 splicing variant is regulated by the type I interferons by the negative feedback mechanism. It was shown that immunosuppressing effects of ADAR1 facilitate progression of some types of cancer. On the other hand, changes in the amino acid sequences resulting from the mRNA editing by the ADAR enzymes can result in the formation of neoantigens that can activate the antitumor immunity. The ADAR2 isoform acts on RNA more selectively; its function is associated with the editing of mRNA coding regions and can lead to the amino acid substitutions, in particular, those essential for the proper functioning of some neurotransmitter receptors in the central nervous system.

Keywords

adenosine deaminase RNA editing ADAR cancer immunity neoantigen 

Abbreviations

ADAR

adenosine deaminase, RNA-dependent

dsRNA

double-stranded RNA

PKR

protein kinase R

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Funding. This work is supported by the Russian Science Foundation (project no. 17-15-01229).

Conflict of interest. The authors declare no conflict of interest in financial of any other sphere.

Ethical approval. This paper contains no studies using animal or human subjects.

References

  1. 1.
    Lobas, A. A., Pyatnitskiy, M. A., Chernobrovkin, A. L., Ilina, I. Y., Karpov, D. S., Solovyeva, E. M., Kuznetsova, K. G., Ivanov, M. V., Lyssuk, E. Y., Kliuchnikova, A. A., Voronko, O. E., Larin, S. S., Zubarev, R. A., Gorshkov, M. V., and Moshkovskii, S. A. (2018) Proteogenomics of malignant melanoma cell lines: the effect of stringency of exome data filtering on variant peptide identification in shotgun proteomics, J. Proteome Res., 17, 1801–1811, doi:  https://doi.org/10.1021/acs.jproteome.7b00841.CrossRefGoogle Scholar
  2. 2.
    Kuznetsova, K. G., Kliuchnikova, A. A., Ilina, I. U., Chernobrovkin, A. L., Novikova, S. E., Farafonova, T. E., Karpov, D. S., Ivanov, M. V., Goncharov, A. O., Ilgisonis, E. V., Voronko, O. E., Nasaev, S. S., Zgoda, V. G., Zubarev, R. A., Gorshkov, M. V., and Moshkovskii, S. A. (2018) Proteogenomics of adenosine-to-inosine RNA editing in the fruit fly, J. Proteome Res., 17, 3889–3903, doi:  https://doi.org/10.1021/acs.jproteome.8b00553.CrossRefGoogle Scholar
  3. 3.
    Ishizuka, J. J., Manguso, R. T., Cheruiyot, C. K., Bi, K., Panda, A., Iracheta-Vellve, A., Miller, B. C., Du, P. P., Yates, K. B., Dubrot, J., Buchumenski, I., Comstock, D. E., Brown, F. D., Ayer, A., Kohnle, I. C., Pope, H. W., Zimmer, M. D., Sen, D. R., Lane-Reticker, S. K., Robitschek, E. J., Griffin, G. K., Collins, N. B., Long, A. H., Doench, J. G., Kozono, D., Levanon, E. Y., and Haining, W. N. (2019) Loss of ADAR1 in tumours overcomes resistance to immune checkpoint blockade, Nature, 565, 43–48, doi:  https://doi.org/10.1038/s41586-018-0768-9.CrossRefGoogle Scholar
  4. 4.
    Orecchini, E., Doria, M., Antonioni, A., Galardi, S., Ciafre, S. A., Frassinelli, L., Mancone, C., Montaldo, C., Tripodi, M., and Michienzi, A. (2017) ADAR1 restricts LINE-1 retrotransposition, Nucleic Acids Res., 45, 155–168, doi:  https://doi.org/10.1093/nar/gkw834.CrossRefGoogle Scholar
  5. 5.
    Bass, B. L. (2002) RNA editing by adenosine deaminases that act on RNA, Annu. Rev. Biochem., 71, 817–846, doi:  https://doi.org/10.1146/annurev.biochem.71.110601.135501.CrossRefGoogle Scholar
  6. 6.
    Hough, R. F., and Bass, B. L. (1994) Purification of the Xenopus laevis double-stranded RNA adenosine deaminase, J. Biol. Chem., 269, 9933–9939.Google Scholar
  7. 7.
    Jin, Y., Zhang, W., and Li, Q. (2009) Origins and evolution of ADAR-mediated RNA editing, IUBMB Life, 61, 572–578, doi:  https://doi.org/10.1002/iub.207.CrossRefGoogle Scholar
  8. 8.
    Palladino, M. J., Keegan, L. P., O’Connell, M. A., and Reenan, R. A. (2000) dADAR, a Drosophila double-stranded RNA-specific adenosine deaminase is highly developmentally regulated and is itself a target for RNA editing, RNA, 6, 1004–1018.CrossRefGoogle Scholar
  9. 9.
    Melcher, T., Maas, S., Herb, A., Sprengel, R., Higuchi, M., and Seeburg, P. H. (1996) RED2, a brain-specific member of the RNA-specific adenosine deaminase family, J. Biol. Chem., 271, 31795–31798.CrossRefGoogle Scholar
  10. 10.
    Oakes, E., Anderson, A., Cohen-Gadol, A., and Hundley, H. A. (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, doi:  https://doi.org/10.1074/jbc.M117.779868.CrossRefGoogle Scholar
  11. 11.
    Schumacher, J. M., Lee, K., Edelhoff, S., and Braun, R. E. (1995) Distribution of Tenr, an RNA-binding protein, in a lattice-like network within the spermatid nucleus in the mouse, Biol. Reprod., 52, 1274–1283.CrossRefGoogle Scholar
  12. 12.
    Saunders, L. R., and Barber, G. N. (2003) The dsRNA binding protein family: critical roles, diverse cellular functions, FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol., 17, 961–983, doi:  https://doi.org/10.1096/fj.02-0958rev.Google Scholar
  13. 13.
    Herbert, A., Alfken, J., Kim, Y. G., Mian, I. S., Nishikura, K., and Rich, A. (1997 A Z-DNA binding domain present in the human editing enzyme, double-stranded RNA adenosine deaminase, Proc. Natl. Acad. Sci. USA, 94, 8421–8426.CrossRefGoogle Scholar
  14. 14.
    Nishikura, K., Yoo, C., Kim, U., Murray, J. M., Estes, P. A., Cash, F. E., and Liebhaber, S. A. (1991) Substrate specificity of the dsRNA unwinding/modifying activity, EMBO J., 10, 3523–3532.CrossRefGoogle Scholar
  15. 15.
    Bass, B. L., and Weintraub, H. (1988) An unwinding activity that covalently modifies its double-stranded RNA substrate, Cell, 55, 1089–1098.CrossRefGoogle Scholar
  16. 16.
    Licht, K., Janisiw, M. P., Jantsch, M. F., Anrather, D., Hartl, M., and Amman, F. (2018) Inosine induces context-dependent recoding and translational stalling, Nucleic Acids Res., 47, 3–14, doi:  https://doi.org/10.1093/nar/gky1163.CrossRefGoogle Scholar
  17. 17.
    Levanon, E. Y., Eisenberg, E., Yelin, R., Nemzer, S., Hallegger, M., Shemesh, R., Fligelman, Z. Y., Shoshan, A., Pollock, S. R., Sztybel, D., Olshansky, M., Rechavi, G., and Jantsch, M. F. (2004) Systematic identification of abundant A-to-I editing sites in the human transcriptome, Nat. Biotechnol., 22, 1001–1005, doi:  https://doi.org/10.1038/nbt996.CrossRefGoogle Scholar
  18. 18.
    Kim, D. D. Y., Kim, T. T. Y., Walsh, T., Kobayashi, Y., Matise, T. C., Buyske, S., and Gabriel, A. (2004) Widespread RNA editing of embedded alu elements in the human transcriptome, Genome Res., 14, 1719–1725, doi:  https://doi.org/10.1101/gr.2855504.CrossRefGoogle Scholar
  19. 19.
    Athanasiadis, A., Rich, A., and Maas, S. (2004) Wide-spread A-to-I RNA editing of Alu-containing mRNAs in the human transcriptome, PLoS Biol., 2, e391, doi:  https://doi.org/10.1371/journal.pbio.0020391.CrossRefGoogle Scholar
  20. 20.
    Blow, M., Futreal, P. A., Wooster, R., and Stratton, M. R. (2004) A survey of RNA editing in human brain, Genome Res., 14, 2379–2387, doi:  https://doi.org/10.1101/gr.2951204.CrossRefGoogle Scholar
  21. 21.
    Eisenberg, E., Nemzer, S., Kinar, Y., Sorek, R., Rechavi, G., and Levanon, E. Y. (2005) Is abundant A-to-I RNA editing primate-specific?, Trends Genet., 21, 77–81, doi:  https://doi.org/10.1016/j.tig.2004.12.005..CrossRefGoogle Scholar
  22. 22.
    Shen, M. R., Batzer, M. A., and Deininger, P. L. (1991) Evolution of the master Alu gene(s), J. Mol. Evol., 33, 311–320.CrossRefGoogle Scholar
  23. 23.
    Garcia, M. A., Gil, J., Ventoso, I., Guerra, S., Domingo, E., Rivas, C., and Esteban, M. (2006) Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action, Microbiol. Mol. Biol. Rev., 70, 1032–1060, doi:  https://doi.org/10.1128/MMBR.00027-06.CrossRefGoogle Scholar
  24. 24.
    Yang, J.-H., Nie, Y., Zhao, Q., Su, Y., Pypaert, M., Su, H., and Rabinovici, R. (2003) Intracellular localization of differentially regulated RNA-specific adenosine deaminase isoforms in inflammation, J. Biol. Chem., 278, 45833–45842, doi:  https://doi.org/10.1074/jbc.M308612200.CrossRefGoogle Scholar
  25. 25.
    Clerzius, G., Gelinas, J.-F., Daher, A., Bonnet, M., Meurs, E. F., and Gatignol, A. (2009) ADAR1 interacts with PKR during human immunodeficiency virus infection of lymphocytes and contributes to viral replication, J. Virol., 83, 10119–10128, doi:  https://doi.org/10.1128/JVI.02457-08.CrossRefGoogle Scholar
  26. 26.
    Porath, H. T., Knisbacher, B. A., Eisenberg, E., and Levanon, E. Y. (2017) Massive A-to-I RNA editing is common across the Metazoa and correlates with dsRNA abundance, Genome Biol., 18, 185, doi:  https://doi.org/10.1186/s13059-017-1315-y.CrossRefGoogle Scholar
  27. 27.
    Pestal, K., Funk, C. C., Snyder, J. M., Price, N. D., Treuting, P. M., and Stetson, D. B. (2015) Isoforms of RNA-editing enzyme ADAR1 independently control nucleic acid sensor MDA5-driven autoimmunity and multi-organ development, Immunity, 43, 933–944, doi:  https://doi.org/10.1016/j.immuni.2015.11.001.CrossRefGoogle Scholar
  28. 28.
    Mannion, N. M., Greenwood, S. M., Young, R., Cox, S., Brindle, J., Read, D., Nellaker, C., Vesely, C., Ponting, C. P., McLaughlin, P. J., Jantsch, M. F., Dorin, J., Adams, I. R., Scadden, A. D. J., Ohman, M., Keegan, L. P., and O’Connell, M. A. (2014) The RNA-editing enzyme ADAR1 controls innate immune responses to RNA, Cell Rep., 9, 1482–1494, doi:  https://doi.org/10.1016/j.celrep.2014.10.041.CrossRefGoogle Scholar
  29. 29.
    Amberger, J. S., Bocchini, C. A., Schiettecatte, F., Scott, A. F., and Hamosh, A. (2015) OMIM.org: Online Mendelian Inheritance in Man (OMIM®), an online catalog of human genes and genetic disorders, Nucleic Acids Res., 43, D789–D798, doi:  https://doi.org/10.1093/nar/gku1205.CrossRefGoogle Scholar
  30. 30.
    Rice, G. I., Kasher, P. R., Forte, G. M. A., Mannion, N. M., Greenwood, S. M., Szynkiewicz, M., Dickerson, J. E., Bhaskar, S. S., Zampini, M., Briggs, T. A., Jenkinson, E. M., Bacino, C. A., Battini, R., Bertini, E., Brogan, P. A., Brueton, L. A., Carpanelli, M., De Laet, C., de Lonlay, P., del Toro, M., Desguerre, I., Fazzi, E., Garcia-Cazorla, A., Heiberg, A., Kawaguchi, M., Kumar, R., Lin, J. P., Lourenco, C. M., Male, A. M., Marques, W., Jr., Mignot, C., Olivieri, I., Orcesi, S., Prabhakar, P., Rasmussen, M., Robinson, R. A., Rozenberg, F., Schmidt, J. L., Steindl, K., Tan, T. Y., van der Merwe, W. G., Vanderver, A., Vassallo, G., Wakeling, E. L., Wassmer, E., Whittaker, E., Livingston, J. H., Lebon, P., Suzuki, T., McLaughlin, P. J., Keegan, L. P., O’Connell, M. A., Lovell, S. C., and Crow, Y. J. (2012) Mutations in ADAR1 cause Aicardi-Goutieres syndrome associated with a type I interferon signature, Nat. Genet., 44, 1243–1248, doi:  https://doi.org/10.1038/ng.2414.CrossRefGoogle Scholar
  31. 31.
    Miyamura, Y., Suzuki, T., Kono, M., Inagaki, K., Ito, S., Suzuki, N., and Tomita, Y. (2003) Mutations of the RNA-specific adenosine deaminase gene (DSRAD) are involved in dyschromatosis symmetrica hereditaria, Am. J. Hum. Genet., 73, 693–699, doi:  https://doi.org/10.1086/378209.CrossRefGoogle Scholar
  32. 32.
    Samuel, C. E. (2011) Adenosine deaminases acting on RNA (ADARs) are both antiviral and proviral, Virology, 411, 180–193, doi:  https://doi.org/10.1016/j.virol.2010.12.004.CrossRefGoogle Scholar
  33. 33.
    Taylor, D. R., Puig, M., Darnell, M. E. R., Mihalik, K., and Feinstone, S. M. (2005) New antiviral pathway that mediates hepatitis C virus replicon interferon sensitivity through ADAR1, J. Virol., 79, 6291–6298, doi:  https://doi.org/10.1128/JVI.79.10.6291-6298.2005.CrossRefGoogle Scholar
  34. 34.
    Zahn, R. C., Schelp, I., Utermohlen, O., and von Laer, D. (2007) A-to-G hypermutation in the genome of lymphocytic choriomeningitis virus, J. Virol., 81, 457–464, doi:  https://doi.org/10.1128/JVI.00067-06.CrossRefGoogle Scholar
  35. 35.
    Suspene, R., Petit, V., Puyraimond-Zemmour, D., Aynaud, M.-M., Henry, M., Guetard, D., Rusniok, C., Wain-Hobson, S., and Vartanian, J.-P. (2011) Double-stranded RNA adenosine deaminase ADAR-1-induced hypermutated genomes among inactivated seasonal influenza and live attenuated measles virus vaccines, J. Virol., 85, 2458–2462, doi:  https://doi.org/10.1128/JVI.02138-10.CrossRefGoogle Scholar
  36. 36.
    Gandy, S. Z., Linnstaedt, S. D., Muralidhar, S., Cashman, K. A., Rosenthal, L. J., and Casey, J. L. (2007) RNA editing of the human herpesvirus 8 kaposin transcript eliminates its transforming activity and is induced during lytic replication, J. Virol., 81, 13544–13551, doi:  https://doi.org/10.1128/JVI.01521-07.CrossRefGoogle Scholar
  37. 37.
    Iizasa, H., Wulff, B.-E., Alla, N. R., Maragkakis, M., Megraw, M., Hatzigeorgiou, A., Iwakiri, D., Takada, K., Wiedmer, A., Showe, L., Lieberman, P., and Nishikura, K. (2010) Editing of Epstein-Barr virus-encoded BART6 microRNAs controls their dicer targeting and consequently affects viral latency, J. Biol. Chem., 285, 33358–33370, doi:  https://doi.org/10.1074/jbc.M110.138362.CrossRefGoogle Scholar
  38. 38.
    Toth, A. M., Li, Z., Cattaneo, R., and Samuel, C. E. (2009) RNA-specific adenosine deaminase ADAR1 suppresses measles virus-induced apoptosis and activation of protein kinase PKR, J. Biol. Chem., 284, 29350–29356, doi:  https://doi.org/10.1074/jbc.M109.045146.CrossRefGoogle Scholar
  39. 39.
    Gelinas, J.-F., Clerzius, G., Shaw, E., and Gatignol, A. (2011) Enhancement of replication of RNA viruses by ADAR1 via RNA editing and inhibition of RNA-activated protein kinase, J. Virol., 85, 8460–8466, doi:  https://doi.org/10.1128/JVI.00240-11.CrossRefGoogle Scholar
  40. 40.
    Casey, J. L. (2011) Control of ADAR1 editing of hepatitis delta virus RNAs, in Current Topics in Microbiology and Immunology, Vol. 353, pp. 123–143, doi:  https://doi.org/10.1007/82_2011_146.Google Scholar
  41. 41.
    De Cecco, M., Ito, T., Petrashen, A. P., Elias, A. E., Skvir, N. J., Criscione, S. W., Caligiana, A., Brocculi, G., Adney, E. M., Boeke, J. D., Le, O., Beausejour, C., Ambati, J., Ambati, K., Simon, M., Seluanov, A., Gorbunova, V., Slagboom, P. E., Helfand, S. L., Neretti, N., and Sedivy, J. M. (2019) L1 drives IFN in senescent cells and promotes age-associated inflammation, Nature, 566, 73–78, doi:  https://doi.org/10.1038/s41586-018-0784-9.CrossRefGoogle Scholar
  42. 42.
    Gannon, H. S., Zou, T., Kiessling, M. K., Gao, G. F., Cai, D., Choi, P. S., Ivan, A. P., Buchumenski, I., Berger, A. C., Goldstein, J. T., Cherniack, A. D., Vazquez, F., Tsherniak, A., Levanon, E. Y., Hahn, W. C., and Meyerson, M. (2018) Identification of ADAR1 adenosine deaminase dependency in a subset of cancer cells, Nat. Commun., 9, 5450, doi:  https://doi.org/10.1038/s41467-018-07824-4.CrossRefGoogle Scholar
  43. 43.
    Xu, L.-D., and Ohman, M. (2018) ADAR1 editing and its role in cancer, Genes (Basel), 10, E12, doi:  https://doi.org/10.3390/genes10010012.CrossRefGoogle Scholar
  44. 44.
    Zhang, M., Fritsche, J., Roszik, J., Williams, L. J., Peng, X., Chiu, Y., Tsou, C.-C., Hoffgaard, F., Goldfinger, V., Schoor, O., Talukder, A., Forget, M. A., Haymaker, C., Bernatchez, C., Han, L., Tsang, Y.-H., Kong, K., Xu, X., Scott, K. L., Singh-Jasuja, H., Lizee, G., Liang, H., Weinschenk, T., Mills, G. B., and Hwu, P. (2018) RNA editing derived epitopes function as cancer antigens to elicit immune responses, Nat. Commun., 9, 3919, doi:  https://doi.org/10.1038/s41467-018-06405-9.CrossRefGoogle Scholar
  45. 45.
    Higuchi, M., Single, F. N., Kohler, M., Sommer, B., Sprengel, R., and Seeburg, P. H. (1993) RNA editing of AMPA receptor subunit GluR-B: a base-paired intron-exon structure determines position and efficiency, Cell, 75, 1361–1370, doi:  https://doi.org/10.1016/0092-8674(93)90622-W.CrossRefGoogle Scholar
  46. 46.
    Egebjerg, J., Kukekov, V., and Heinemann, S. F. (1994) Intron sequence directs RNA editing of the glutamate receptor subunit GluR2 coding sequence, Proc. Natl. Acad. Sci. USA, 91, 10270–10274, doi:  https://doi.org/10.1073/pnas.91.22.10270.CrossRefGoogle Scholar
  47. 47.
    Grice, L. F., and Degnan, B. M. (2015) The origin of the ADAR gene family and animal RNA editing, BMC Evol. Biol., 15, 4, doi:  https://doi.org/10.1186/s12862-015-0279-3.CrossRefGoogle Scholar
  48. 48.
    Yablonovitch, A. L., Deng, P., Jacobson, D., and Li, J. B. (2017) The evolution and adaptation of A-to-I RNA editing, PLoS Genet., 13, e1007064, doi:  https://doi.org/10.1371/journal.pgen.1007064.CrossRefGoogle Scholar
  49. 49.
    Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E., and Mello, C. C. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans, Nature, 391, 806–811, doi:  https://doi.org/10.1038/35888.CrossRefGoogle Scholar
  50. 50.
    Walkley, C. R., and Li, J. B. (2017) Rewriting the transcriptome: adenosine-to-inosine RNA editing by ADARs, Genome Biol., 18, 205, doi:  https://doi.org/10.1186/s13059-017-1347-3.CrossRefGoogle Scholar
  51. 51.
    Liscovitch-Brauer, N., Alon, S., Porath, H. T., Elstein, B., Unger, R., Ziv, T., Admon, A., Levanon, E. Y., Rosenthal, J. J. C., and Eisenberg, E. (2017) Trade-off between transcriptome plasticity and genome evolution in cephalopods, Cell, 169, 191–202.e11, doi:  https://doi.org/10.1016/j.cell.2017.03.025.CrossRefGoogle Scholar
  52. 52.
    Garrett, S., and Rosenthal, J. J. C. (2012) RNA editing underlies temperature adaptation in K+ channels from polar octopuses, Science, 335, 848–851, doi:  https://doi.org/10.1126/science.1212795.CrossRefGoogle Scholar
  53. 53.
    Iwamoto, K., Bundo, M., and Kato, T. (2009) Serotonin receptor 2C and mental disorders: genetic, expression, and RNA editing studies, RNA Biol., 6, 248–53, doi:  https://doi.org/10.4161/rna.6.3.8370.CrossRefGoogle Scholar
  54. 54.
    Barbon, A., and Barlati, S. (2011) Glutamate receptor RNA editing in health and disease, Biochemistry (Moscow), 76, 882–889, doi:  https://doi.org/10.1134/S0006297911080037..CrossRefGoogle Scholar
  55. 55.
    Gallo, A., Vukic, D., Michalik, D., O’Connell, M. A., and Keegan, L. P. (2017) ADAR RNA editing in human disease; more to it than meets the I, Hum. Genet., 136, 1265–1278, doi:  https://doi.org/10.1007/s00439-017-1837-0.CrossRefGoogle Scholar
  56. 56.
    Higuchi, M., Maas, S., Single, F. N., Hartner, J., Rozov, A., Burnashev, N., Feldmeyer, D., Sprengel, R., and Seeburg, P. H. (2000) Point mutation in an AMPA receptor gene rescues lethality in mice deficient in the RNA-editing enzyme ADAR2, Nature, 406, 78–81, doi:  https://doi.org/10.1038/35017558.CrossRefGoogle Scholar
  57. 57.
    Kawahara, Y., Ito, K., Sun, H., Aizawa, H., Kanazawa, I., and Kwak, S. (2004) RNA editing and death of motor neurons, Nature, 427, 801, doi:  https://doi.org/10.1038/427801a.CrossRefGoogle Scholar
  58. 58.
    Kwak, S., and Kawahara, Y. (2005) Deficient RNA editing of GluR2 and neuronal death in amyotropic lateral sclerosis, J. Mol. Med., 83, 110–120, doi:  https://doi.org/10.1007/s00109-004-0599-z.CrossRefGoogle Scholar
  59. 59.
    Lyddon, R., Dwork, A. J., Keddache, M., Siever, L. J., and Dracheva, S. (2013) Serotonin 2c receptor RNA editing in major depression and suicide, World J. Biol. Psychiatry, 14, 590–601, doi:  https://doi.org/10.3109/15622975.2011.630406.CrossRefGoogle Scholar
  60. 60.
    Sommer, B., Kohler, M., Sprengel, R., and Seeburg, P. H. (1991) RNA editing in brain controls a determinant of ion flow in glutamate-gated channels, Cell, 67, 11–19, doi:  https://doi.org/10.1016/0092-8674(91)90568-J.CrossRefGoogle Scholar
  61. 61.
    Patterson, J. B., and Samuel, C. E. (1995) Expression and regulation by interferon of a double-stranded-RNA-specific adenosine deaminase from human cells: evidence for two forms of the deaminase, Mol. Cell. Biol., 15, 5376–5388.CrossRefGoogle Scholar
  62. 62.
    Wright, A., and Vissel, B. (2012) The essential role of AMPA receptor GluR2 subunit RNA editing in the normal and diseased brain, Front. Mol. Neurosci., 5, 34, doi:  https://doi.org/10.3389/fnmol.2012.00034.Google Scholar

Copyright information

© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  • A. O. Goncharov
    • 1
  • A. A. Kliuchnikova
    • 1
    • 2
  • S. S. Nasaev
    • 2
  • S. A. Moshkovskii
    • 1
    • 2
    Email author
  1. 1.Institute of Biomedical ChemistryMoscowRussia
  2. 2.Pirogov Russian National Research Medical UniversityMoscowRussia

Personalised recommendations