Identification of widespread ultra-edited human RNAs

PLoS Genetics

Volumn 7, Issue 10, 2011, Pages

  Carmi, Shai ^a   Borukhov, Itamar ^b   Levanon, Erez Y ^a  

^a BAR ILAN UNIVERSITY   (Israel)

^b Compugen Ltd ^*  (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; DOUBLE STRANDED RNA; GENOMIC DNA; GLYCINE; INOSINE; RNA; ADENOSINE DEAMINASE; DSRNA ADENOSINE DEAMINASE; GUANOSINE;

ARTICLE; BASE MISPAIRING; BASE PAIRING; CONTROLLED STUDY; DNA STRUCTURE; EXON; GENETIC ALGORITHM; GENETIC TRANSFORMATION; HUMAN; HUMAN TISSUE; NUCLEOTIDE SEQUENCE; RNA ANALYSIS; RNA CLEAVAGE; RNA EDITING; RNA SEQUENCE; RNA SPLICING; RNA STRUCTURE; SEQUENCE ALIGNMENT; ALU SEQUENCE; CHEMISTRY; EXPRESSED SEQUENCE TAG; GENETICS; GENOME; GENOMICS; MOLECULAR GENETICS;

ADENOSINE; ADENOSINE DEAMINASE; ALU ELEMENTS; BASE PAIR MISMATCH; BASE PAIRING; BASE SEQUENCE; EXONS; EXPRESSED SEQUENCE TAGS; GENOME; GENOMICS; GUANOSINE; HUMANS; INOSINE; MOLECULAR SEQUENCE DATA; RNA; RNA EDITING; RNA, DOUBLE-STRANDED;

EID: 80055076214     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002317     Document Type: Article

References (67)

1. Farajollahi S, Maas S, (2010) Molecular diversity through RNA editing: a balancing act. Trends in Genetics 26: 221-230.
2. Nishikura K, (2010) Functions and Regulation of RNA Editing by ADAR Deaminases. Annual Review of Biochemistry 79: 321-349.
3. Bass BL, (2002) RNA editing by adenosine deaminases that act on RNA. Annual Review of Biochemistry 71: 817-846.
4. Keegan LP, Gallo A, O'Connell MA, (2001) The many roles of an RNA editor. Nature Reviews Genetics 2: 869-878.
5. Wang Q, Khillan J, Gadue P, Nishikura K, (2000) Requirement of the RNA Editing Deaminase ADAR1 Gene for Embryonic Erythropoiesis. Science 290: 1765-1768.
6. Higuchi M, Maas S, Single FN, Hartner JC, Rozov A, 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.
7. Maas S, Kawahara Y, Tamburro KM, Nishikura K, (2006) A-to-I RNA Editing and Human Disease. RNA Biology 3: 1-9.
8. Samuel CE, (2011) Adenosine deaminases acting on RNA (ADARs) are both antiviral and proviral. Virology 411: 180-193.
9. Chen L-L, Carmichael GG, (2008) Genes regulation by SINES and inosines. Cell Cycle 7: 3294-3301.
10. Zhang Z, Carmichael GG, (2001) The Fate of dsRNA in the Nucleus: A p54 nrb-Containing Complex Mediates the Nuclear Retention of Promiscuously A-to-I Edited RNAs. Cell 106: 465-475.
11. George CX, Gan Z, Liu Y, Samuel CE, (2011) Adenosine Deaminases Acting on RNA, RNA Editing, and Interferon Action. Journal of Interferon & Cytokine Research 31: 99-117.
12. Yang W, Chendrimada TP, Wang Q, Higuchi M, Seeburg PH, et al. (2006) Modulation of microRNA processing and expression through RNA editing by ADAR deaminases. Nature Structural & Molecular Biology 13: 13-21.
13. Scadden ADJ, (2007) Inosine-containing dsRNA binds a stress-granule-like complex and downregulates gene expression in trans. Molecular Cell 28: 491-500.
14. Prasanth KV, Prasanth SG, Xuan Z, Hearn S, Freier SM, et al. (2005) Regulating gene expression through RNA nuclear retention. Cell 123: 249-263.
15. Gommans WM, Mullen SP, Maas S, (2009) RNA editing: a driving force for adaptive evolution? BioEssays 31: 1137-45.
16. St Laurent GI, Savva YA, Reenan R, (2009) Enhancing non-coding RNA information content with ADAR editing. Neuroscience Letters 466: 89-98.
17. 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. Nature Biotechnology 22: 1001-1005.
18. 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 Research 14: 1719-1725.
19. Athanasiadis A, Rich A, Maas S, (2004) Widespread A-to-I RNA editing of Alu-containing mRNAs in the human transcriptome. PLoS Biology 2: e391.
20. Blow M, Futreal PA, Wooster R, Stratton MR, (2004) A survey of RNA editing in human brain. Genome Research 14: 2379-2387.
21. Wait Zaranek A, Levanon EY, Zecharia T, Clegg T, Church GM, (2010) A Survey of Genomic Traces Reveals a Common Sequencing Error, RNA Editing, and DNA Editing. PLoS Genetics 6: e1000954.
22. Ensterö M, Akerborg O, Lundin D, Wang B, Furey TS, et al. (2010) A computational screen for site selective A-to-I editing detects novel sites in neuron specific Hu proteins. BMC Bioinformatics 11: 6.
23. Gommans WM, Tatalias NE, Sie CP, Dupuis D, Vendetti N, et al. (2008) Screening of human SNP database identifies recoding sites of A-to-I RNA editing. RNA 14: 2074-2085.
24. 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.
25. Levanon EY, Hallegger M, Kinar Y, Shemesh R, Djinovic-Carugo K, et al. (2005) Evolutionarily conserved human targets of adenosine to inosine RNA editing. Nucleic Acids Research 33: 1162-1168.
26. Li JB, Levanon EY, Yoon J-K, Aach J, Xie B, et al. (2009) Genome-wide identification of human RNA editing sites by parallel DNA capturing and sequencing. Science 324: 1210-3.
27. Sakurai M, Yano T, Kawabata H, Ueda H, Suzuki T, (2010) Inosine cyanoethylation identifies A-to-I RNA editing sites in the human transcriptome. Nature Chemical Biology 6: 733-740.
28. Ohlson J, Pedersen JS, Haussler D, Ohman M, (2007) Editing modifies the GABA(A) receptor subunit alpha3. RNA 13: 698-703.
29. Wulff B-E, Sakurai M, Nishikura K, (2011) Elucidating the inosinome: global approaches to adenosine-to-inosine RNA editing. Nature Reviews Genetics 12: 81-85.
30. Kiran A, Baranov PV, (2010) DARNED: a DAtabase of RNa EDiting in humans. Bioinformatics 26: 1772-1776.
31. Batzer MA, Deininger PL, (2002) Alu repeats and human genomic diversity. Nature Reviews Genetics 3: 370-379.
32. Scadden ADJ, (2005) The RISC subunit Tudor-SN binds to hyper-edited double-stranded RNA and promotes its cleavage. Nature Structural & Molecular Biology 12: 489-96.
33. Vitali P, Scadden ADJ, (2010) Double-stranded RNAs containing multiple IU pairs are sufficient to suppress interferon induction and apoptosis. Nature structural & molecular biology 17: 1043-50.
34. Rueter SM, Dawson TR, Emeson RB, (1999) Regulation of alternative splicing by RNA editing. Nature 399: 75-80.
35. Lev-Maor G, Sorek R, Levanon EY, Paz N, Eisenberg E, et al. (2007) RNA-editing-mediated exon evolution. Genome Biology 8: R29.
36. Liang H, Landweber LF, (2007) Hypothesis: RNA editing of microRNA target sites in humans? RNA 13: 463-467.
37. Nishikura K, Yoo C, Kim U, Murray JM, Estes PA, et al. (1991) Substrate specificity of the dsRNA unwinding/modifying activity. The EMBO Journal 10: 3523-3532.
38. Polson AG, Bass BL, (1994) Preferential selection of adenosines for modification by double-stranded RNA adenosine deaminase. The EMBO Journal 13: 5701-5711.
39. Lehmann KA, Bass BL, (2000) Double-stranded RNA adenosine deaminases ADAR1 and ADAR2 have overlapping specificities. Biochemistry 39: 12875-12884.
40. Morse DP, Aruscavage PJ, Bass BL, (2002) RNA hairpins in noncoding regions of human brain and Caenorhabditis elegans mRNA are edited by adenosine deaminases that act on RNA. Proceedings of the National Academy of Sciences of the United States of America 99: 7906-11.
41. Barak M, Levanon EY, Eisenberg E, Paz N, Rechavi G, et al. (2009) Evidence for large diversity in the human transcriptome created by Alu RNA editing. Nucleic Acids Research 37: 6905-6915.
42. Cattaneo R, Schmid A, Eschle D, Baczko K, Meulen V ter, et al. (1988) Biased hypermutation and other genetic changes in defective measles viruses in human brain infections. Cell 55: 255-265.
43. Paul MS, Bass BL, (1998) Inosine exists in mRNA at tissue-specific levels and is most abundant in brain mRNA. The EMBO Journal 17: 1120-1127.
44. Fujita PA, Rhead B, Zweig AS, Hinrichs AS, Karolchik D, et al. (2010) The UCSC Genome Browser database: update 2011. Nucleic Acids Research 39: D876-D882.
45. Zhang Z, Schwartz S, Wagner L, Miller W, (2000) A greedy algorithm for aligning DNA sequences. Journal of Computational Biology 7: 203-214 doi:10.1089/10665270050081478.
46. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, et al. (2005) Repbase Update, a database of eukaryotic repetitive elements. Cytogenetic and Genome Research 110: 462-467.
47. Patterson JB, Samuel CE, (1995) Expression and regulation by interferon of a double-stranded-RNA-specific adenosine deaminase from human cells: evidence for two forms of the deaminase. Molecular and Cellular Biology 15: 5376-5388.
48. Paz N, Levanon EY, Amariglio N, Heimberger AB, Ram Z, et al. (2007) Altered adenosine-to-inosine RNA editing in human cancer. Genome Research 17: 1586-1595.
49. Bass BL, (1997) RNA editing and hypermutation by adenosine deamination. Trends in Biochemical Sciences 22: 157-162.
50. Gruber AR, Lorenz R, Bernhart SH, Neuböck R, Hofacker IL, (2008) The Vienna RNA websuite. Nucleic Acids Research 36: W70-W744.
51. Milo R, Jorgensen P, Moran U, Weber G, Springer M, (2010) BioNumbers-the database of key numbers in molecular and cell biology. Nucleic Acids Research 38: D750-D753.
52. Hartner JC, Walkley CR, Lu J, Orkin SH, (2009) ADAR1 is essential for the maintenance of hematopoiesis and suppression of interferon signaling. Nature Immunology 10: 109-115.
53. Wang Q, Miyakoda M, Yang W, Khillan J, Stachura DL, et al. (2004) Stress-induced apoptosis associated with null mutation of ADAR1 RNA editing deaminase gene. The Journal of Biological Chemistry 279: 4952-4961.
54. Meltzer M, Long K, Nie Y, Gupta M, Yang J, et al. (2010) The RNA editor gene ADAR1 is induced in myoblasts by inflammatory ligands and buffers stress response. Clinical and Translational Science 3: 73-80.
55. Yang J-H, Luo X, Nie Y, Su Y, Zhao Q, et al. (2003) Widespread inosine-containing mRNA in lymphocytes regulated by ADAR1 in response to inflammation. Immunology 109: 15-23.
56. Hartner JC, Schmittwolf C, Kispert A, Müller AM, Higuchi M, et al. (2004) Liver disintegration in the mouse embryo caused by deficiency in the RNA-editing enzyme ADAR1. The Journal of Biological Chemistry 279: 4894-4902.
57. Scadden ADJ, Smith CWJ, (1997) A ribonuclease specific for inosine-containing RNA: a potential role in antiviral defence? The EMBO Journal 16: 2140-2149.
58. Scadden ADJ, Smith CWJ, (2001) Specific cleavage of hyper-edited dsRNAs. The EMBO Journal 20: 4243-52.
59. Osenberg S, Dominissini D, Rechavi G, Eisenberg E, (2009) Widespread cleavage of A-to-I hyperediting substrates. RNA 15: 1632-1639.
60. Chen C, Ara T, Gautheret D, (2009) Using Alu elements as polyadenylation sites: A case of retroposon exaptation. Molecular Biology and Evolution 26: 327-334.
61. Lee JY, Ji Z, Tian B, (2008) Phylogenetic analysis of mRNA polyadenylation sites reveals a role of transposable elements in evolution of the 3′-end of genes. Nucleic Acids Research 36: 5581-5590.
62. Pollard KS, Hubisz MJ, Rosenbloom KR, Siepel A, (2010) Detection of nonneutral substitution rates on mammalian phylogenies. Genome Research 20: 110-121.
63. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Research 15: 1034-1050.
64. 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. Molecular and Cellular Biology 15: 1389-1397.
65. Melcher T, Maas S, Herb A, Sprengel R, Seeburg PH, et al. (1996) A mammalian RNA editing enzyme. Nature 379: 460-464.
66. Paz-Yaacov N, Levanon EY, Nevo E, Kinar Y, Harmelin A, et al. (2010) Adenosine-to-inosine RNA editing shapes transcriptome diversity in primates. Proceedings of the National Academy of Sciences 107: 12174-12179.
67. Enstero M, Daniel C, Wahlstedt H, Major F, Ohman M, (2009) Recognition and coupling of A-to-I edited sites are determined by the tertiary structure of the RNA. Nucleic Acids Research 37: 6916-6926.