Abstract
A-to-I RNA editing results in the conversion of single adenosines into inosines, which alters coding and non-coding sequences in RNA molecules, increasing the complexity of the transcriptome. This modification is vital in a number of brain-specific coding transcripts, where the introduced alternative amino acids impact protein function substantially. Indeed, deviations from normal editing levels have been detected in tissues from individuals affected by neurological diseases and cancer, underscoring the importance of correct and regulated editing. Since the discovery of A-to-I RNA editing, considerable effort has been made to uncover additional editing targets and analyze the subsequent functional consequences for the recoded substrates. The effects of editing on non-coding RNAs (ncRNAs) such as microRNAs (miRNAs) or long ncRNAs are less well explored. ncRNAs act as regulators of gene expression through chromatin modification, imprinting, alternative splicing, and mRNA translation and stability. Editing has the potential to dynamically alter and diversify ncRNAs, thereby redirecting their functions. How editing intersects, interferes with, and modulates the roles of ncRNAs, possibly in response to external stimuli, therefore warrants a deeper look. This review discusses recent advances and new insights in the field.
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References
Hung, T., and Chang, H. Y. (2010) RNA Biol., 7, 582–585.
Mercer, T. R., Dinger, M. E., and Mattick, J. S. (2009) Nat. Rev. Genet., 10, 155–159.
Costa, F. F. (2010) Bioessays, 32, 599–608.
Forster, A. C., and Symons, R. H. (1987) Cell, 50, 9–16.
Mattick, J. S. (2004) Nat. Rev. Genet., 5, 316–323.
St. Laurent, G., 3rd, and Wahlestedt, C. (2007) Trends Neurosci., 30, 612–621.
De la Pena, M., and Garcia-Robles, I. (2010) EMBO Rep., 11, 711–716.
Miura, F., Kawaguchi, N., Sese, J., Toyoda, A., Hattori, M., Morishita, S., and Ito, T. (2006) Proc. Natl. Acad. Sci. USA, 103, 17846–17851.
Kapranov, P., Cawley, S. E., Drenkow, J., Bekiranov, S., Strausberg, R. L., Fodor, S. P., and Gingeras, T. R. (2002) Science, 296, 916–919.
Kapranov, P., Cheng, J., Dike, S., Nix, D. A., Duttagupta, R., Willingham, A. T., Stadler, P. F., Hertel, J., Hackermuller, J., Hofacker, I. L., Bell, I., Cheung, E., Drenkow, J., Dumais, E., Patel, S., Helt, G., Ganesh, M., Ghosh, S., Piccolboni, A., Sementchenko, V., Tammana, H., and Gingeras, T. R. (2007) Science, 316, 1484–1488.
Birney, E., et al. (2007) Nature, 447, 799–816.
Stein, L. D., et al. (2003) PLoS Biol., 1, E45.
International Human Genome Sequencing Consortium (2004) Nature, 431, 931–945.
Lander, E. S., et al. (2001) Nature, 409, 860–921.
Taft, R. J., Pheasant, M., and Mattick, J. S. (2007) Bioessays, 29, 288–299.
Tsai, M. C., Manor, O., Wan, Y., Mosammaparast, N., Wang, J. K., Lan, F., Shi, Y., Segal, E., and Chang, H. Y. (2010) Science, 329, 689–693.
Mattick, J. S. (2010) Bioessays, 32, 548–552.
Jin, Y., Zhang, W., and Li, Q. (2009) IUBMB Life, 61, 572–578.
Palladino, M. J., Keegan, L. P., O’Connell, M. A., and Reenan, R. A. (2000) Cell, 102, 437–449.
Tonkin, L. A., Saccomanno, L., Morse, D. P., Brodigan, T., Krause, M., and Bass, B. L. (2002) EMBO J., 21, 6025–6035.
Higuchi, M., Maas, S., Single, F. N., Hartner, J., Rozov, A., Burnashev, N., Feldmeyer, D., Sprengel, R., and Seeburg, P. H. (2000) Nature, 406, 78–81.
Wang, Q., Khillan, J., Gadue, P., and Nishikura, K. (2000) Science, 290, 1765–1768.
Hartner, J. C., Schmittwolf, C., Kispert, A., Muller, A. M., Higuchi, M., and Seeburg, P. H. (2004) J. Biol. Chem., 279, 4894–4902.
XuFeng, R., Boyer, M. J., Shen, H., Li, Y., Yu, H., Gao, Y., Yang, Q., Wang, Q., and Cheng, T. (2009) Proc. Natl. Acad. Sci. USA, 106, 17763–17768.
Hartner, J. C., Walkley, C. R., Lu, J., and Orkin, S. H. (2009) Nat. Immunol., 10, 109–115.
Chen, C. X., Cho, D. S., Wang, Q., Lai, F., Carter, K. C., and Nishikura, K. (2000) RNA, 6, 755–767.
Mian, I. S., Moser, M. J., Holley, W. R., and Chatterjee, A. (1998) J. Comput. Biol., 5, 57–72.
Lai, F., Drakas, R., and Nishikura, K. (1995) J. Biol. Chem., 270, 17098–17105.
Wong, S. K., Sato, S., and Lazinski, D. W. (2001) RNA, 7, 846–858.
Lehmann, K. A., and Bass, B. L. (2000) Biochemistry, 39, 12875–12884.
Yi-Brunozzi, H. Y., Stephens, O. M., and Beal, P. A. (2001) J. Biol. Chem., 276, 37827–37833.
Stephens, O. M., Haudenschild, B. L., and Beal, P. A. (2004) Chem. Biol., 11, 1239–1250.
Stefl, R., Oberstrass, F. C., Hood, J. L., Jourdan, M., Zimmermann, M., Skrisovska, L., Maris, C., Peng, L., Hofr, C., Emeson, R. B., and Allain, F. H. (2010) Cell, 143, 225–237.
Lehmann, K. A., and Bass, B. L. (1999) J. Mol. Biol., 291, 1–13.
Bass, B. L. (2002) Annu. Rev. Biochem., 71, 817–846.
Enstero, M., Daniel, C., Wahlstedt, H., Major, F., and Ohman, M. (2009) Nucleic Acids Res., 37, 6916–6926.
Paul, M. S., and Bass, B. L. (1998) EMBO J., 17, 1120–1127.
Wahlstedt, H., Daniel, C., Enstero, M., and Ohman, M. (2009) Genome Res., 19, 978–986.
Rula, E. Y., Lagrange, A. H., Jacobs, M. M., Hu, N., Macdonald, R. L., and Emeson, R. B. (2008) J. Neurosci., 28, 6196–6201.
Jacobs, M. M., Fogg, R. L., Emeson, R. B., and Stanwood, G. D. (2009) Dev. Neurosci., 31, 223–237.
Osenberg, S., Paz Yaacov, N., Safran, M., Moshkovitz, S., Shtrichman, R., Sherf, O., Jacob-Hirsch, J., Keshet, G., Amariglio, N., Itskovitz-Eldor, J., and Rechavi, G. (2010) PLoS One, 5, e11173.
Gallo, A., Keegan, L. P., Ring, G. M., and O’Connell, M. A. (2003) EMBO J., 22, 3421–3430.
Cho, D. S., Yang, W., Lee, J. T., Shiekhattar, R., Murray, J. M., and Nishikura, K. (2003) J. Biol. Chem., 278, 17093–17102.
Eckmann, C. R., Neunteufl, A., Pfaffstetter, L., and Jantsch, M. F. (2001) Mol. Biol. Cell, 12, 1911–1924.
George, C. X., Das, S., and Samuel, C. E. (2008) Virology, 380, 338–343.
George, C. X., and Samuel, C. E. (1999) Proc. Natl. Acad. Sci. USA, 96, 4621–4626.
Poulsen, H., Nilsson, J., Damgaard, C. K., Egebjerg, J., and Kjems, J. (2001) Mol. Cell. Biol., 21, 7862–7871.
Fritz, J., Strehblow, A., Taschner, A., Schopoff, S., Pasierbek, P., and Jantsch, M. F. (2009) Mol. Cell. Biol., 29, 1487–1497.
Strehblow, A., Hallegger, M., and Jantsch, M. F. (2002) Mol. Biol. Cell, 13, 3822–3835.
Samuel, C. E. (2011) Virology, 411, 180–193.
Sommer, B., Kohler, M., Sprengel, R., and Seeburg, P. H. (1991) Cell, 67, 11–19.
Burns, C. M., Chu, H., Rueter, S. M., Hutchinson, L. K., Canton, H., Sanders-Bush, E., and Emeson, R. B. (1997) Nature, 387, 303–308.
Berg, K. A., Cropper, J. D., Niswender, C. M., Sanders-Bush, E., Emeson, R. B., and Clarke, W. P. (2001) Br. J. Pharmacol., 134, 386–392.
Marion, S., Weiner, D. M., and Caron, M. G. (2004) J. Biol. Chem., 279, 2945–2954.
Herrick-Davis, K., Grinde, E., and Niswender, C. M. (1999) J. Neurochem., 73, 1711–1717.
Levanon, E. Y., Hallegger, M., Kinar, Y., Shemesh, R., Djinovic-Carugo, K., Rechavi, G., Jantsch, M. F., and Eisenberg, E. (2005) Nucleic Acids Res., 33, 1162–1168.
Li, J. B., Levanon, E. Y., Yoon, J. K., Aach, J., Xie, B., Leproust, E., Zhang, K., Gao, Y., and Church, G. M. (2009) Science, 324, 1210–1213.
Gommans, W. M., Tatalias, N. E., Sie, C. P., Dupuis, D., Vendetti, N., Smith, L., Kaushal, R., and Maas, S. (2008) RNA, 14, 2074–2085.
Eisenberg, E., Adamsky, K., Cohen, L., Amariglio, N., Hirshberg, A., Rechavi, G., and Levanon, E. Y. (2005) Nucleic Acids Res., 33, 4612–4617.
Clutterbuck, D. R., Leroy, A., O’Connell, M. A., and Semple, C. A. (2005) Bioinformatics, 21, 2590–2595.
Pullirsch, D., and Jantsch, M. F. (2010) RNA Biol., 7, 205–212.
Gommans, W. M., Dupuis, D. E., McCane, J. E., Tatalias, N. E., and Maas, S. (2008) Diversifying Exon Code through A-to-I RNA Editing, in RNA and DNA Editing, Wiley InterScience, pp. 1–30.
Gommans, W. M., Mullen, S. P., and Maas, S. (2009) Bioessays, 31, 1137–1145.
Athanasiadis, A., Rich, A., and Maas, S. (2004) PLoS Biol., 2, e391.
Kim, D. D., Kim, T. T., Walsh, T., Kobayashi, Y., Matise, T. C., Buyske, S., and Gabriel, A. (2004) Genome Res., 14, 1719–1725.
Blow, M., Futreal, P. A., Wooster, R., and Stratton, M. R. (2004) Genome Res., 14, 2379–2387.
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) Nat. Biotechnol., 22, 1001–1005.
Batzer, M. A., and Deininger, P. L. (2002) Nat. Rev. Genet., 3, 370–379.
Eisenberg, E., Nemzer, S., Kinar, Y., Sorek, R., Rechavi, G., and Levanon, E. Y. (2005) Trends Genet., 21, 77–81.
Hasler, J., and Strub, K. (2006) Nucleic Acids Res., 34, 5491–5497.
Hasler, J., Samuelsson, T., and Strub, K. (2007) Cell. Mol. Life Sci., 64, 1793–1800.
Mattick, J. S., and Mehler, M. F. (2008) Trends Neurosci., 31, 227–233.
Chen, L. L., and Carmichael, G. G. (2008) Cell Cycle, 7, 3294–3301.
Lev-Maor, G., Sorek, R., Levanon, E. Y., Paz, N., Eisenberg, E., and Ast, G. (2007) Genome Biol., 8, R29.
Moller-Krull, M., Zemann, A., Roos, C., Brosius, J., and Schmitz, J. (2008) J. Mol. Biol., 382, 601–609.
Zhang, Z., and Carmichael, G. G. (2001) Cell, 106, 465–475.
Prasanth, K. V., Prasanth, S. G., Xuan, Z., Hearn, S., Freier, S. M., Bennett, C. F., Zhang, M. Q., and Spector, D. L. (2005) Cell, 123, 249–263.
Scadden, A. D., and Smith, C. W. (2001) EMBO J., 20, 4243–4252.
Chen, L. L., DeCerbo, J. N., and Carmichael, G. G. (2008) EMBO J., 27, 1694–1705.
Scadden, A. D. (2007) Mol. Cell, 28, 491–500.
Hundley, H. A., and Bass, B. L. (2010) Trends Biochem. Sci., 35, 377–383.
Hundley, H. A., Krauchuk, A. A., and Bass, B. L. (2008) RNA, 14, 2050–2060.
Morse, D. P., and Bass, B. L. (1999) Proc. Natl. Acad. Sci. USA, 96, 6048–6053.
Thomson, T., and Lin, H. (2009) Annu. Rev. Cell Dev. Biol., 25, 355–376.
Ding, S. W. (2010) Nat. Rev. Immunol., 10, 632–644.
Djuranovic, S., Nahvi, A., and Green, R. (2011) Science, 331, 550–553.
Griffiths-Jones, S., Saini, H. K., van Dongen, S., and Enright, A. J. (2008) Nucleic Acids Res., 36, D154–D158.
Friedman, R. C., Farh, K. K., Burge, C. B., and Bartel, D. P. (2009) Genome Res., 19, 92–105.
Bartel, D. P. (2004) Cell, 116, 281–297.
Hu, H. Y., Yan, Z., Xu, Y., Hu, H., Menzel, C., Zhou, Y. H., Chen, W., and Khaitovich, P. (2009) BMC Genomics, 10, 413.
Miyoshi, K., Miyoshi, T., and Siomi, H. (2010) Mol. Genet. Genomics, 284, 95–103.
Baskerville, S., and Bartel, D. P. (2005) RNA, 11, 241–247.
Slezak-Prochazka, I., Durmus, S., Kroesen, B. J., and van den Berg, A. (2010) RNA, 16, 1087–1095.
Luciano, D. J., Mirsky, H., Vendetti, N. J., and Maas, S. (2004) RNA, 10, 1174–1177.
Yang, W., Chendrimada, T. P., Wang, Q., Higuchi, M., Seeburg, P. H., Shiekhattar, R., and Nishikura, K. (2006) Nat. Struct. Mol. Biol., 13, 13–21.
Kawahara, Y., Zinshteyn, B., Chendrimada, T. P., Shiekhattar, R., and Nishikura, K. (2007) EMBO Rep., 8, 763–769.
Kawahara, Y., Zinshteyn, B., Sethupathy, P., Iizasa, H., Hatzigeorgiou, A. G., and Nishikura, K. (2007) Science, 315, 1137–1140.
Kawahara, Y., Megraw, M., Kreider, E., Iizasa, H., Valente, L., Hatzigeorgiou, A. G., and Nishikura, K. (2008) Nucleic Acids Res., 36, 5270–5280.
Scadden, A. D., and Smith, C. W. (1997) EMBO J., 16, 2140–2149.
Scadden, A. D. (2005) Nat. Struct. Mol. Biol., 12, 489–496.
Nishikura, K. (2006) Nat. Rev. Mol. Cell Biol., 7, 919–931.
Hislop, A. D., Taylor, G. S., Sauce, D., and Rickinson, A. B. (2007) Annu. Rev. Immunol., 25, 587–617.
Pagano, J. S., Blaser, M., Buendia, M. A., Damania, B., Khalili, K., Raab-Traub, N., and Roizman, B. (2004) Semin. Cancer Biol., 14, 453–471.
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) J. Biol. Chem., 285, 33358–33370.
Skalsky, R. L., and Cullen, B. R. (2010) Annu. Rev. Microbiol., 64, 123–141.
Godshalk, S. E., Bhaduri-McIntosh, S., and Slack, F. J. (2008) Cell Cycle, 7, 3595–3600.
Blow, M. J., Grocock, R. J., van Dongen, S., Enright, A. J., Dicks, E., Futreal, P. A., Wooster, R., and Stratton, M. R. (2006) Genome Biol., 7, R27.
Schulte, J. H., Marschall, T., Martin, M., Rosenstiel, P., Mestdagh, P., Schlierf, S., Thor, T., Vandesompele, J., Eggert, A., Schreiber, S., Rahmann, S., and Schramm, A. (2010) Nucleic Acids Res., 38, 5919–5928.
Heale, B. S., Keegan, L. P., McGurk, L., Michlewski, G., Brindle, J., Stanton, C. M., Caceres, J. F., and O’Connell, M. A. (2009) EMBO J., 28, 3145–3156.
Liang, H., and Landweber, L. F. (2007) RNA, 13, 463–467.
Borchert, G. M., Gilmore, B. L., Spengler, R. M., Xing, Y., Lanier, W., Bhattacharya, D., and Davidson, B. L. (2009) Hum. Mol. Genet., 18, 4801–4807.
Long, D., Lee, R., Williams, P., Chan, C. Y., Ambros, V., and Ding, Y. (2007) Nat. Struct. Mol. Biol., 14, 287–294.
Zamore, P. D. (2001) Nat. Struct. Biol., 8, 746–750.
Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E., and Mello, C. C. (1998) Nature, 391, 806–811.
Tonkin, L. A., and Bass, B. L. (2003) Science, 302, 1725.
Ohta, H., Fujiwara, M., Ohshima, Y., and Ishihara, T. (2008) Genetics, 180, 785–796.
Knight, S. W., and Bass, B. L. (2002) Mol. Cell, 10, 809–817.
Yang, W., Wang, Q., Howell, K. L., Lee, J. T., Cho, D. S., Murray, J. M., and Nishikura, K. (2005) J. Biol. Chem., 280, 3946–3953.
Hong, J., Zhao, Y., Li, Z., and Huang, W. (2007) Biochem. Biophys. Res. Commun., 361, 373–378.
Wu, T., Zhao, Y., Hao, Z., Zhao, H., and Wang, W. (2009) Int. J. Biol. Macromol., 45, 157–162.
Natoli, G., Ghisletti, S., and Barozzi, I. (2011) Genes Dev., 25, 101–106.
Mandel, E. M., and Grosschedl, R. (2010) Curr. Opin. Immunol., 22, 161–167.
Carninci, P., et al. (2005) Science, 309, 1559–1563.
Okazaki, Y., et al. (2002) Nature, 420, 563–573.
Ebralidze, A. K., Guibal, F. C., Steidl, U., Zhang, P., Lee, S., Bartholdy, B., Jorda, M. A., Petkova, V., Rosenbauer, F., Huang, G., Dayaram, T., Klupp, J., O’Brien, K. B., Will, B., Hoogenkamp, M., Borden, K. L., Bonifer, C., and Tenen, D. G. (2008) Genes Dev., 22, 2085–2092.
Nagano, T., and Fraser, P. (2009) Mamm. Genome, 20, 557–562.
Qureshi, I. A., Mattick, J. S., and Mehler, M. F. (2010) Brain Res., 1338, 20–35.
Mercer, T. R., Qureshi, I. A., Gokhan, S., Dinger, M. E., Li, G., Mattick, J. S., and Mehler, M. F. (2010) BMC Neurosci., 11, 14.
Mercer, T. R., Dinger, M. E., Sunkin, S. M., Mehler, M. F., and Mattick, J. S. (2008) Proc. Natl. Acad. Sci. USA, 105, 716–721.
Maas, S., Kawahara, Y., Tamburro, K. M., and Nishikura, K. (2006) RNA Biol., 3, 1–9.
Wang, X., Song, X., Glass, C. K., and Rosenfeld, M. G. (2011) Cold Spring Harb. Perspect. Biol., 3, a003756.
Kent, W. J., Sugnet, C. W., Furey, T. S., Roskin, K. M., Pringle, T. H., Zahler, A. M., and Haussler, D. (2002) Genome Res., 12, 996–1006.
Bennett, E. A., Keller, H., Mills, R. E., Schmidt, S., Moran, J. V., Weichenrieder, O., and Devine, S. E. (2008) Genome Res., 18, 1875–1883.
Li, T. H., and Schmid, C. W. (2001) Gene, 276, 135–141.
Rudin, C. M., and Thompson, C. B. (2001) Genes Chromosomes Cancer, 30, 64–71.
Mariner, P. D., Walters, R. D., Espinoza, C. A., Drullinger, L. F., Wagner, S. D., Kugel, J. F., and Goodrich, J. A. (2008) Mol. Cell, 29, 499–509.
Dewannieux, M., Esnault, C., and Heidmann, T. (2003) Nat. Genet., 35, 41–48.
Hormozdiari, F., Alkan, C., Ventura, M., Hajirasouliha, I., Malig, M., Hach, F., Yorukoglu, D., Dao, P., Bakhshi, M., Sahinalp, S. C., and Eichler, E. E. (2011) Genome Res., 21, 840–849.
Van der Heijden, G. W., and Bortvin, A. (2009) Epigenetics, 4, 76–79.
Bogerd, H. P., Wiegand, H. L., Hulme, A. E., Garcia-Perez, J. L., O’shea, K. S., Moran, J. V., and Cullen, B. R. (2006) Proc. Natl. Acad. Sci. USA, 103, 8780–8785.
Muckenfuss, H., Hamdorf, M., Held, U., Perkovic, M., Lower, J., Cichutek, K., Flory, E., Schumann, G. G., and Munk, C. (2006) J. Biol. Chem., 281, 22161–22172.
Stenglein, M. D., and Harris, R. S. (2006) J. Biol. Chem., 281, 16837–16841.
Van den Hurk, J. A., Meij, I. C., Seleme, M. C., Kano, H., Nikopoulos, K., Hoefsloot, L. H., Sistermans, E. A., de Wijs, I. J., Mukhopadhyay, A., Plomp, A. S., de Jong, P. T., Kazazian, H. H., and Cremers, F. P. (2007) Hum. Mol. Genet., 16, 1587–1592.
Kano, H., Godoy, I., Courtney, C., Vetter, M. R., Gerton, G. L., Ostertag, E. M., and Kazazian, H. H., Jr. (2009) Genes Dev., 23, 1303–1312.
Macia, A., Munoz-Lopez, M., Cortes, J. L., Hastings, R. K., Morell, S., Lucena-Aguilar, G., Marchal, J. A., Badge, R. M., and Garcia-Perez, J. L. (2011) Mol. Cell. Biol., 31, 300–316.
Belancio, V. P., Roy-Engel, A. M., Pochampally, R. R., and Deininger, P. (2010) Nucleic Acids Res., 38, 3909–3922.
Muotri, A. R., Chu, V. T., Marchetto, M. C., Deng, W., Moran, J. V., and Gage, F. H. (2005) Nature, 435, 903–910.
Muotri, A. R., Zhao, C., Marchetto, M. C., and Gage, F. H. (2009) Hippocampus, 19, 1002–1007.
Coufal, N. G., Garcia-Perez, J. L., Peng, G. E., Yeo, G. W., Mu, Y., Lovci, M. T., Morell, M., O’shea, K. S., Moran, J. V., and Gage, F. H. (2009) Nature, 460, 1127–1131.
Lomeli, H., Mosbacher, J., Melcher, T., Hoger, T., Geiger, J. R., Kuner, T., Monyer, H., Higuchi, M., Bach, A., and Seeburg, P. H. (1994) Science, 266, 1709–1713.
Kohler, M., Burnashev, N., Sakmann, B., and Seeburg, P. H. (1993) Neuron, 10, 491–500.
Bhalla, T., Rosenthal, J. J., Holmgren, M., and Reenan, R. (2004) Nat. Struct. Mol. Biol., 11, 950–956.
Ohlson, J., Pedersen, J. S., Haussler, D., and Ohman, M. (2007) RNA, 13, 698–703.
Nimmich, M. L., Heidelberg, L. S., and Fisher, J. L. (2009) Neurosci. Res., 63, 288–293.
Rueter, S. M., Dawson, T. R., and Emeson, R. B. (1999) Nature, 399, 75–80.
Yeo, J., Goodman, R. A., Schirle, N. T., David, S. S., and Beal, P. A. (2010) Proc. Natl. Acad. Sci. USA, 107, 20715–20719.
George, C. X., and Samuel, C. E. (1999) Gene, 229, 203–213.
Desterro, J. M., Keegan, L. P., Lafarga, M., Berciano, M. T., O’Connell, M., and Carmo-Fonseca, M. (2003) J. Cell Sci., 116, 1805–1818.
Nie, Y., Zhao, Q., Su, Y., and Yang, J. H. (2004) J. Biol. Chem., 279, 13249–13255.
Desterro, J. M., Keegan, L. P., Jaffray, E., Hay, R. T., O’Connell, M. A., and Carmo-Fonseca, M. (2005) Mol. Biol. Cell, 16, 5115–5126.
Maas, S., and Gommans, W. M. (2009) PLoS ONE, 4, e4225.
Gerber, A., O’Connell, M. A., and Keller, W. (1997) RNA, 3, 453–463.
Saunders, L. R., and Barber, G. N. (2003) FASEB J., 17, 961–983.
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Published in Russian in Biokhimiya, 2011, Vol. 76, No. 8, pp. 1064–1078.
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Godfried Sie, C.P., Kuchka, M. RNA Editing adds flavor to complexity. Biochemistry Moscow 76, 869–881 (2011). https://doi.org/10.1134/S0006297911080025
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DOI: https://doi.org/10.1134/S0006297911080025