Editor meets silencer: crosstalk between RNA editing and RNA interference (original) (raw)
Bentley, D. L. Rules of engagement: co-transcriptional recruitment of pre-mRNA processing factors. Curr. Opin. Cell Biol.17, 251–256 (2005). ArticleCASPubMed Google Scholar
Gott, J. M. & Emeson, R. B. Functions and mechanisms of RNA editing. Annu. Rev. Genet.34, 499–531 (2000). ArticleCASPubMed Google Scholar
Bass, B. L. RNA editing by adenosine deaminases that act on RNA. Annu. Rev. Biochem.71, 817–846 (2002). ArticleCASPubMed Google Scholar
Keegan, L. P., Leroy, A., Sproul, D. & O'Connell, M. A. Adenosine deaminases acting on RNA (ADARs): RNA-editing enzymes. Genome Biol.5, 209 (2004). ArticlePubMedPubMed Central Google Scholar
Valente, L. & Nishikura, K. ADAR gene family and A-to-I RNA editing: diverse roles in posttranscriptional gene regulation. Prog. Nucleic Acid Res. Mol. Biol.79, 299–338 (2005). An up-to-date review on A→I editing and ADAR genes. ArticleCASPubMed Google Scholar
Athanasiadis, A., Rich, A. & Maas, S. Widespread A-to-I RNA editing of Alu-containing mRNAs in the human transcriptome. PLoS Biol.2, e391 (2004). ArticlePubMedPubMed Central Google Scholar
Levanon, E. Y. et al. Systematic identification of abundant A-to-I editing sites in the human transcriptome. Nature Biotechnol.22, 1001–1005 (2004). References 6–9 report a genome-wide screening strategy, leading to the identification of numerous A→I editing sites in non-coding Alu repeat RNAs. ArticleCAS Google Scholar
Fire, A. et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature391, 806–811 (1998). ArticleCASPubMed Google Scholar
Filipowicz, W., Jaskiewicz, L., Kolb, F. A. & Pillai, R. S. Post-transcriptional gene silencing by siRNAs and miRNAs. Curr. Opin. Struct. Biol.15, 331–341 (2005). ArticleCASPubMed Google Scholar
Bartel, D. P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell116, 281–297 (2004). ArticleCASPubMed Google Scholar
Du, T. & Zamore, P. D. microPrimer: the biogenesis and function of microRNA. Development132, 4645–4652 (2005). ArticleCASPubMed Google Scholar
Yang, W. et al. Modulation of microRNA processing and expression through RNA editing by ADAR deaminases. Nature Struct. Mol. Biol.13, 13–21 (2006). Shows that A→I editing of a miRNA-142 precursor suppresses its processing by Drosha–DGCR8 and also that the highly edited precursor RNAs are degraded by Tudor-SN. ArticleCAS Google Scholar
Pfeffer, S. et al. Identification of microRNAs of the herpesvirus family. Nature Methods2, 269–276 (2005). ArticleCASPubMed Google Scholar
Yang, W. et al. ADAR1 RNA deaminase limits short interfering RNA efficacy in mammalian cells. J. Biol. Chem.280, 3946–3953 (2005). Shows that ADAR1L functions as an RNAi suppressor by sequestering siRNAs. ArticleCASPubMed Google Scholar
Tonkin, L. A. & Bass, B. L. Mutations in RNAi rescue aberrant chemotaxis of ADAR mutants. Science302, 1725 (2003). Shows the RNAi dependence of ADAR-null worm phenotypes. ArticleCASPubMedPubMed Central Google Scholar
Knight, S. W. & Bass, B. L. The role of RNA editing by ADARs in RNAi. Mol. Cell10, 809–817 (2002). Shows, for the first time, that A→I editing prevents RNAi-mediated transgene silencing, which implies an interaction between RNAi and RNA-editing pathways. ArticleCASPubMed Google Scholar
Bass, B. L. & Weintraub, H. An unwinding activity that covalently modifies its double-stranded RNA substrate. Cell55, 1089–1098 (1988). ArticleCASPubMed Google Scholar
Wagner, R. W., Smith, J. E., Cooperman, B. S. & Nishikura, K. A double-stranded RNA unwinding activity introduces structural alterations by means of adenosine to inosine conversions in mammalian cells and Xenopus eggs. Proc. Natl Acad. Sci. USA86, 2647–2651 (1989). ArticleCASPubMedPubMed Central Google Scholar
Bass, B. L. & Weintraub, H. A developmentally regulated activity that unwinds RNA duplexes. Cell48, 607–613 (1987). ArticleCASPubMed Google Scholar
Rebagliati, M. R. & Melton, D. A. Antisense RNA injections in fertilized frog eggs reveal an RNA duplex unwinding activity. Cell48, 599–605 (1987). ArticleCASPubMed Google Scholar
Kim, U., Wang, Y., Sanford, T., Zeng, Y. & Nishikura, K. Molecular cloning of cDNA for double-stranded RNA adenosine deaminase, a candidate enzyme for nuclear RNA editing. Proc. Natl Acad. Sci. USA91, 11457–11461 (1994). ArticleCASPubMedPubMed Central Google Scholar
Lai, F., Chen, C. X., Carter, K. C. & Nishikura, K. Editing of glutamate receptor B subunit ion channel RNAs by four alternatively spliced DRADA2 double-stranded RNA adenosine deaminases. Mol. Cell. Biol.17, 2413–2424 (1997). ArticleCASPubMedPubMed Central Google Scholar
Gerber, A., O'Connell, M. A. & Keller, W. Two forms of human double-stranded RNA-specific editase 1 (hRED1) generated by the insertion of an Alu cassette. RNA3, 453–463 (1997). CASPubMedPubMed Central Google Scholar
Melcher, T. et al. RED2, a brain-specific member of the RNA-specific adenosine deaminase family. J. Biol. Chem.271, 31795–31798 (1996). ArticleCASPubMed Google Scholar
Chen, C. X. et al. A third member of the RNA-specific adenosine deaminase gene family, ADAR3, contains both single- and double-stranded RNA binding domains. RNA6, 755–767 (2000). ArticleCASPubMedPubMed Central Google Scholar
Palladino, M. J., Keegan, L. P., O'Connell, M. A. & Reenan, R. A. A-to-I pre-mRNA editing in Drosophila is primarily involved in adult nervous system function and integrity. Cell102, 437–449 (2000). ArticleCASPubMed Google Scholar
Ryter, J. M. & Schultz, S. C. Molecular basis of double-stranded RNA-protein interactions: structure of a dsRNA-binding domain complexed with dsRNA. EMBO J.17, 7505–7513 (1998). ArticleCASPubMedPubMed Central Google Scholar
Lai, F., Drakas, R. & Nishikura, K. Mutagenic analysis of double-stranded RNA adenosine deaminase, a candidate enzyme for RNA editing of glutamate-gated ion channel transcripts. J. Biol. Chem.270, 17098–17105 (1995). ArticleCASPubMed Google Scholar
Macbeth, M. R. et al. Inositol hexakisphosphate is bound in the ADAR2 core and required for RNA editing. Science309, 1534–1539 (2005). ArticleCASPubMedPubMed Central Google Scholar
Patterson, J. B. & Samuel, C. E. 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 (1995). ArticleCASPubMedPubMed Central Google Scholar
Kawakubo, K. & Samuel, C. E. Human RNA-specific adenosine deaminase (ADAR1) gene specifies transcripts that initiate from a constitutively active alternative promoter. Gene258, 165–172 (2000). ArticleCASPubMed Google Scholar
Yang, J. H. et al. Widespread inosine-containing mRNA in lymphocytes regulated by ADAR1 in response to inflammation. Immunology109, 15–23 (2003). ArticleCASPubMedPubMed Central Google Scholar
Peng, P. L. et al. ADAR2-dependent RNA editing of AMPA receptor subunit GluR2 determines vulnerability of neurons in forebrain ischemia. Neuron49, 719–733 (2006). ArticleCASPubMed Google Scholar
Desterro, J. M. et al. Dynamic association of RNA-editing enzymes with the nucleolus. J. Cell Sci.116, 1805–1818 (2003). ArticleCASPubMed Google Scholar
Poulsen, H., Nilsson, J., Damgaard, C. K., Egebjerg, J. & Kjems, J. CRM1 mediates the export of ADAR1 through a nuclear export signal within the Z-DNA binding domain. Mol. Cell. Biol.21, 7862–7871 (2001). ArticleCASPubMedPubMed Central Google Scholar
Sansam, C. L., Wells, K. S. & Emeson, R. B. Modulation of RNA editing by functional nucleolar sequestration of ADAR2. Proc. Natl Acad. Sci. USA100, 14018–14023 (2003). ArticleCASPubMedPubMed Central Google Scholar
Lehmann, K. A. & Bass, B. L. The importance of internal loops within RNA substrates of ADAR1. J. Mol. Biol.291, 1–13 (1999). ArticleCASPubMed Google Scholar
Higuchi, M. et al. RNA editing of AMPA receptor subunit GluR-B: a base-paired intron–exon structure determines position and efficiency. Cell75, 1361–1370 (1993). ArticleCASPubMed Google Scholar
Wang, Q. et al. Altered G protein-coupling functions of RNA editing isoform and splicing variant serotonin2C receptors. J. Neurochem.74, 1290–1300 (2000). ArticleCASPubMed Google Scholar
Seeburg, P. H. & Hartner, J. Regulation of ion channel/neurotransmitter receptor function by RNA editing. Curr. Opin. Neurobiol.13, 279–283 (2003). ArticleCASPubMed Google Scholar
Reenan, R. A. The RNA world meets behavior: A→I pre-mRNA editing in animals. Trends Genet.17, 53–56 (2001). ArticleCASPubMed Google Scholar
Stefl, R., Xu, M., Skrisovska, L., Emeson, R. B. & Allain, F. H. Structure and specific RNA binding of ADAR2 double-stranded RNA binding motifs. Structure14, 345–355 (2006). ArticleCASPubMed Google Scholar
Cho, D. S. et al. Requirement of dimerization for RNA editing activity of adenosine deaminases acting on RNA. J. Biol. Chem.278, 17093–17102 (2003). ArticleCASPubMed Google Scholar
Burns, C. M. et al. Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature387, 303–308 (1997). ArticleCASPubMed Google Scholar
Hoopengardner, B., Bhalla, T., Staber, C. & Reenan, R. Nervous system targets of RNA editing identified by comparative genomics. Science301, 832–836 (2003). ArticleCASPubMed Google Scholar
Reenan, R. A., Hanrahan, C. J. & Ganetzky, B. The mle(napts) RNA helicase mutation in Drosophila results in a splicing catastrophe of the para Na+ channel transcript in a region of RNA editing. Neuron25, 139–149 (2000). ArticleCASPubMed Google Scholar
Polson, A. G., Bass, B. L. & Casey, J. L. RNA editing of hepatitis delta virus antigenome by dsRNA-adenosine deaminase. Nature380, 454–456 (1996). ArticleCASPubMed Google Scholar
Higuchi, M. et al. Point mutation in an AMPA receptor gene rescues lethality in mice deficient in the RNA-editing enzyme ADAR2. Nature406, 78–81 (2000). ArticleCASPubMed Google Scholar
Wang, Q., Khillan, J., Gadue, P. & Nishikura, K. Requirement of the RNA editing deaminase ADAR1 gene for embryonic erythropoiesis. Science290, 1765–1768 (2000). ArticleCASPubMed Google Scholar
Wang, Q. et al. Stress-induced apoptosis associated with null mutation of ADAR1 RNA editing deaminase gene. J. Biol. Chem.279, 4952–4961 (2004). ArticleCASPubMed Google Scholar
Hartner, J. C. et al. Liver disintegration in the mouse embryo caused by deficiency in the RNA-editing enzyme ADAR1. J. Biol. Chem.279, 4894–4902 (2004). ArticleCASPubMed Google Scholar
Maas, S., Kawahara, Y., Tamburro, K. M. & Nishikura, K. A-to-I RNA editing and human disease. RNA Biol.3, 1–9 (2006). An up-to-date review on human diseases caused by defective A→I editing. ArticleCASPubMed Google Scholar
Schmauss, C. Regulation of serotonin 2C receptor pre-mRNA editing by serotonin. Int. Rev. Neurobiol.63, 83–100 (2005). ArticleCASPubMed Google Scholar
Miyamura, Y. et al. Mutations of the RNA-specific adenosine deaminase gene (DSRAD) are involved in dyschromatosis symmetrica hereditaria. Am. J. Hum. Genet.73, 693–699 (2003). ArticleCASPubMedPubMed Central Google Scholar
Kawahara, Y. et al. Glutamate receptors: RNA editing and death of motor neurons. Nature427, 801 (2004). ArticleCASPubMed Google Scholar
Gurevich, I. et al. Altered editing of serotonin 2C receptor pre-mRNA in the prefrontal cortex of depressed suicide victims. Neuron34, 349–356 (2002). ArticleCASPubMed Google Scholar
Niswender, C. M. et al. RNA editing of the human serotonin 5-HT2C receptor. Alterations in suicide and implications for serotonergic pharmacotherapy. Neuropsychopharmacology24, 478–491 (2001). ArticleCASPubMed Google Scholar
Paul, M. S. & Bass, B. L. Inosine exists in mRNA at tissue-specific levels and is most abundant in brain mRNA. EMBO J.17, 1120–1127 (1998). ArticleCASPubMedPubMed Central Google Scholar
Levanon, E. Y. et al. Evolutionarily conserved human targets of adenosine to inosine RNA editing. Nucleic Acids Res.33, 1162–1168 (2005). ArticleCASPubMedPubMed Central Google Scholar
Clutterbuck, D. R., Leroy, A., O'Connell, M. A. & Semple, C. A. A bioinformatic screen for novel A–I RNA editing sites reveals recoding editing in BC10. Bioinformatics21, 2590–2595 (2005). References 70 and 71 report that A→I editing of protein-coding regions is exceptionally rare, as demonstrated by a genome-wide screening strategy. ArticleCASPubMed Google Scholar
Eisenberg, E. et al. Is abundant A-to-I RNA editing primate-specific? Trends Genet.21, 77–81 (2005). ArticleCASPubMed Google Scholar
Katayama, S. et al. Antisense transcription in the mammalian transcriptome. Science309, 1564–1566 (2005). ArticlePubMed Google Scholar
Chen, J., Sun, M., Hurst, L. D., Carmichael, G. G. & Rowley, J. D. Genome-wide analysis of coordinate expression and evolution of human _cis_-encoded sense–antisense transcripts. Trends Genet.21, 326–329 (2005). ArticleCASPubMed Google Scholar
Neeman, Y., Dahary, D., Levanon, E. Y., Sorek, R. & Eisenberg, E. Is there any sense in antisense editing? Trends Genet.21, 544–547 (2005). ArticleCASPubMed Google Scholar
Kawahara, Y. & Nishikura, K. Extensive adenosine-to-inosine editing detected in Alu repeats of antisense RNAs reveals scarcity of sense–antisense duplex formation. FEBS Lett.580, 2301–2305 (2006). References 75 and 76 show that antisense RNA is extensively edited, but only in regions containing an inverted Alu repeat dsRNA, showing that the formation of sense–antisense intermolecular dsRNAs is very rare. ArticleCASPubMedPubMed Central Google Scholar
Rueter, S. M., Dawson, T. R. & Emeson, R. B. Regulation of alternative splicing by RNA editing. Nature399, 75–80 (1999). ArticleCASPubMed Google Scholar
Sorek, R. et al. Minimal conditions for exonization of intronic sequences: 5′ splice site formation in Alu exons. Mol. Cell14, 221–231 (2004). ArticleCASPubMed Google Scholar
Dagan, T., Sorek, R., Sharon, E., Ast, G. & Graur, D. AluGene: a database of Alu elements incorporated within protein-coding genes. Nucleic Acids Res.32, D489–D492 (2004). ArticleCASPubMedPubMed Central Google Scholar
Zhang, Z. & Carmichael, G. G. The fate of dsRNA in the nucleus: a p54nrb-containing complex mediates the nuclear retention of promiscuously A-to-I edited RNAs. Cell106, 465–475 (2001). ArticleCASPubMed Google Scholar
Prasanth, K. V. et al. Regulating gene expression through RNA nuclear retention. Cell123, 249–263 (2005). Reports that A→I editing of SINE repeats located in the 3′ UTR might regulate nuclear retention and the release of cationic amino-acid transporter-2 mRNAs. ArticleCASPubMed Google Scholar
Scadden, A. D. The RISC subunit Tudor-SN binds to hyper-edited double-stranded RNA and promotes its cleavage. Nature Struct. Mol. Biol.12, 489–496 (2005). Reports that Tudor-SN, previously identified as a RISC-associated protein, is a ribonuclease specific for inosine-containing dsRNAs, revealing a mechanistic connection between RNAi and RNA-editing pathways. ArticleCAS Google Scholar
Tong, X., Drapkin, R., Yalamanchili, R., Mosialos, G. & Kieff, E. The Epstein–Barr virus nuclear protein 2 acidic domain forms a complex with a novel cellular coactivator that can interact with TFIIE. Mol. Cell. Biol.15, 4735–4744 (1995). ArticleCASPubMedPubMed Central Google Scholar
Wang, Q., Zhang, Z., Blackwell, K. & Carmichael, G. G. Vigilins bind to promiscuously A-to-I-edited RNAs and are involved in the formation of heterochromatin. Curr. Biol.15, 384–391 (2005). Vigilin in complex with ADAR1 binds to inosine-containing RNAs, revealing a possible role for A→I editing in the heterochomatic gene-silencing mechanism. ArticleCASPubMed Google Scholar
Martienssen, R. A., Zaratiegui, M. & Goto, D. B. RNA interference and heterochromatin in the fission yeast Schizosaccharomyces pombe. Trends Genet.21, 450–456 (2005). ArticleCASPubMed Google Scholar
Shilatifard, A. Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu. Rev. Biochem. (2006).
Aravin, A. A. et al. The small RNA profile during Drosophila melanogaster development. Dev. Cell5, 337–350 (2003). ArticleCASPubMed Google Scholar
Sijen, T. & Plasterk, R. H. Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi. Nature426, 310–314 (2003). ArticleCASPubMed Google Scholar
Aravin, A. & Tuschl, T. Identification and characterization of small RNAs involved in RNA silencing. FEBS Lett.579, 5830–5840 (2005). ArticleCASPubMed Google Scholar
Matzke, M. A. & Birchler, J. A. RNAi-mediated pathways in the nucleus. Nature Rev. Genet.6, 24–35 (2005). ArticleCASPubMed Google Scholar
Watanabe, T. et al. Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev.20, 1732–1743 (2006). CASPubMedPubMed Central Google Scholar
Saccomanno, L. & Bass, B. L. The cytoplasm of Xenopus oocytes contains a factor that protects double-stranded RNA from adenosine-to-inosine modification. Mol. Cell. Biol.14, 5425–5432 (1994). CASPubMedPubMed Central Google Scholar
Saunders, L. R. & Barber, G. N. The dsRNA binding protein family: critical roles, diverse cellular functions. FASEB J.17, 961–983 (2003). ArticleCASPubMed Google Scholar
Vance, V. & Vaucheret, H. RNA silencing in plants-defense and counterdefense. Science292, 2277–2280 (2001). ArticleCASPubMed Google Scholar
Kennedy, S., Wang, D. & Ruvkun, G. A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans. Nature427, 645–649 (2004). ArticleCASPubMed Google Scholar
Vargason, J. M., Szittya, G., Burgyan, J. & Tanaka Hall, T. M. Size selective recognition of siRNA by an RNA silencing suppressor. Cell115, 799–811 (2003). ArticleCASPubMed Google Scholar
Ye, K., Malinina, L. & Patel, D. J. Recognition of small interfering RNA by a viral suppressor of RNA silencing. Nature426, 874–878 (2003). ArticleCASPubMedPubMed Central Google Scholar
Hong, J. et al. High doses of siRNAs induce eri-1 and adar-1 gene expression and reduce the efficiency of RNA interference in the mouse. Biochem. J.390, 675–679 (2005). Reports the induction of ADAR-1 and ERI-1, an siRNA-specific ribonuclease and an RNAi suppressor, respectively, by high concentrations of siRNA. This indicates the presence of a feedback mechanism. ArticleCASPubMedPubMed Central Google Scholar
Aravin, A. et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature442, 203–207 (2006). ArticleCASPubMed Google Scholar
Girard, A., Sachidanandam, R., Hannon, G. J. & Carmell, M. A. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature442, 199–202 (2006). ArticlePubMed Google Scholar
Lau, N. C. et al. Characterization of the piRNA complex from rat testes. Science313, 363–367 (2006). ArticleCASPubMed Google Scholar
Byrne, E. M., Stout, A. & Gott, J. M. Editing site recognition and nucleotide insertion are separable processes in Physarum mitochondria. EMBO J.21, 6154–6161 (2002). ArticleCASPubMedPubMed Central Google Scholar
Gott, J. M., Parimi, N. & Bundschuh, R. Discovery of new genes and deletion editing in Physarum mitochondria enabled by a novel algorithm for finding edited mRNAs. Nucleic Acids Res.33, 5063–5072 (2005). ArticleCASPubMedPubMed Central Google Scholar
Barth, C., Greferath, U., Kotsifas, M. & Fisher, P. R. Polycistronic transcription and editing of the mitochondrial small subunit (SSU) ribosomal RNA in Dictyostelium discoideum. Curr. Genet.36, 55–61 (1999). ArticleCASPubMed Google Scholar
Navaratnam, N. & Sarwar, R. An overview of cytidine deaminases. Int. J. Hematol.83, 195–200 (2006). ArticleCASPubMed Google Scholar
Lohan, A. J. & Gray, M. W. Methods for analysis of mitochondrial tRNA editing in Acanthamoeba castellanii. Methods Mol. Biol.265, 315–331 (2004). CASPubMed Google Scholar
Wolf, J., Gerber, A. P. & Keller, W. tadA, an essential tRNA-specific adenosine deaminase from Escherichia coli. EMBO J.21, 3841–3851 (2002). ArticleCASPubMedPubMed Central Google Scholar
Gerber, A. P. & Keller, W. RNA editing by base deamination: more enzymes, more targets, new mysteries. Trends Biochem. Sci.26, 376–384 (2001). ArticleCASPubMed Google Scholar
Greger, I. H., Khatri, L., Kong, X. & Ziff, E. B. AMPA receptor tetramerization is mediated by Q/R editing. Neuron40, 763–774 (2003). ArticleCASPubMed Google Scholar
Nishikura, K. Editing the message from A to I. Nature Biotechnol.22, 962–963 (2004). ArticleCAS Google Scholar