Alu elements shape the primate transcriptome by cis-regulation of RNA editing

Genome Biology

Volumn 15, Issue 2, 2014, Pages

  Daniel, Chammiran ^a   Silberberg, Gilad ^b   Behm, Mikaela ^a   Öhman, Marie ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTOME; ZINC FINGER PROTEIN; ADENOSINE; INOSINE; UNTRANSLATED REGION; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA3; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN 14;

ALU SEQUENCE; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE ONTOLOGY; GLI1 GENE; HUMAN; HUMAN TISSUE; INTRON; INVERTED REPEAT; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; ONCOGENE; PROMOTER REGION; RNA EDITING; RNA TRANSLATION; SEQUENCE ANALYSIS; UNTRANSLATED REGION; ANIMAL; DEAMINATION; GENE EXPRESSION REGULATION; GENETICS; HUMAN GENOME; PRIMATE; 3' UNTRANSLATED REGION; ADULT; DOWN REGULATION; GENETIC ANALYSIS; ONCOGENE GLI1; PROTEIN EXPRESSION; RHESUS MONKEY; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS; UPREGULATION;

ADENOSINE; ALU ELEMENTS; ANIMALS; DEAMINATION; GENE EXPRESSION REGULATION; GENOME, HUMAN; HUMANS; INOSINE; PRIMATES; RNA EDITING; TRANSCRIPTOME; UNTRANSLATED REGIONS;

PRIMATES;

EID: 84896707317     PISSN: None     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2014-15-2-r28     Document Type: Article

References (46)

1. Bass BL, Nishikura K, Keller W, Seeburg PH, Emeson RB, O'Connell MA, Samuel CE, Herbert A. A standardized nomenclature for adenosine deaminases that act on RNA. RNA 1997, 3:947-949. 1369539, 9292492.
2. Nishikura K. Functions and regulation of RNA editing by ADAR deaminases. Annu Rev Biochem 2010, 79:321-349. 10.1146/annurev-biochem-060208-105251, 2953425, 20192758.
3. Wahlstedt H, Öhman M. Site-selective versus promiscuous A-to-I editing. Wiley Interdiscip Rev RNA 2011, 2:761-771. 10.1002/wrna.89, 21976281.
4. Bhalla T, Rosenthal JJ, Holmgren M, Reenan R. Control of human potassium channel inactivation by editing of a small mRNA hairpin. Nat Struct Mol Biol 2004, 11:950-956. 10.1038/nsmb825, 15361858.
5. Brusa R, Zimmermann F, Koh DS, Feldmeyer D, Gass P, Seeburg PH, Sprengel R. Early-onset epilepsy and postnatal lethality associated with an editing-deficient GluR-B allele in mice. Science 1995, 270:1677-1680. 10.1126/science.270.5242.1677, 7502080.
6. Burns CM, Chu H, Rueter SM, Hutchinson LK, Canton H, Sanders-Bush E, Emeson RB. Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature 1997, 387:303-308. 10.1038/387303a0, 9153397.
7. Higuchi M, Single FN, Kohler M, Sommer B, Sprengel R, Seeburg PH. RNA editing of AMPA receptor subunit GluR-B: a base-paired intron-exon structure determines position and efficiency. Cell 1993, 75:1361-1370. 10.1016/0092-8674(93)90622-W, 8269514.
8. Lomeli H, Mosbacher J, Melcher T, Hoger T, Geiger JR, Kuner T, Monyer H, Higuchi M, Bach A, Seeburg PH. Control of kinetic properties of AMPA receptor channels by nuclear RNA editing. Science 1994, 266:1709-1713. 10.1126/science.7992055, 7992055.
9. Sommer B, Köhler M, Sprengel R, Seeburg PH. RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 1991, 67:11-19. 10.1016/0092-8674(91)90568-J, 1717158.
10. Ohlson J, Pedersen JS, Haussler D, Öhman M. Editing modifies the GABAA receptor subunit α3. RNA 2007, 13:698-703. 10.1261/rna.349107, 1852825, 17369310.
11. Daniel C, Venø MT, Ekdahl Y, Kjems J, Öhman M. A distant cis acting intronic element induces site-selective RNA editing. Nucleic Acids Res 2012, 40:9876-9886. 10.1093/nar/gks691, 3479170, 22848101.
12. Paz-Yaacov N, Levanon EY, Nevo E, Kinar Y, Harmelin A, Jacob-Hirsch J, Amariglio N, Eisenberg E, Rechavi G. Adenosine-to-inosine RNA editing shapes transcriptome diversity in primates. Proc Natl Acad Sci USA 2010, 107:12174-12179. 10.1073/pnas.1006183107, 2901480, 20566853.
13. Athanasiadis A, Rich A, Maas S. Widespread A-to-I RNA editing of Alu-containing mRNAs in the human transcriptome. PLoS Biol 2004, 2:e391. 10.1371/journal.pbio.0020391, 526178, 15534692.
14. Blow M, Futreal PA, Wooster R, Stratton MR. A survey of RNA editing in human brain. Genome Res 2004, 14:2379-2387. 10.1101/gr.2951204, 534661, 15545495.
15. Carmi S, Borukhov I, Levanon EY. Identification of widespread ultra-edited human RNAs. PLoS Genet 2011, 7:e1002317. 10.1371/journal.pgen.1002317, 3197674, 22028664.
16. Lev-Maor G, Sorek R, Levanon EY, Paz N, Eisenberg E, Ast G. RNA-editing-mediated exon evolution. Genome Biol 2007, 8:R29. 10.1186/gb-2007-8-2-r29, 1852406, 17326827.
17. Levanon EY, Eisenberg E, Yelin R, Nemzer S, Hallegger M, Shemesh R, Fligelman ZY, Shoshan A, Pollock SR, Sztybel D, Olshansky M, Rechavi G, Jantsch MF. Systematic identification of abundant A-to-I editing sites in the human transcriptome. Nat Biotechnol 2004, 22:1001-1005. 10.1038/nbt996, 15258596.
18. Kiran A, Baranov PV. DARNED: a database of RNA editing in humans. Bioinformatics 2010, 26:1772-1776. 10.1093/bioinformatics/btq285, 20547637.
19. Peng Z, Cheng Y, Tan BC, Kang L, Tian Z, Zhu Y, Zhang W, Liang Y, Hu X, Tan X, Guo J, Dong Z, Liang Y, Bao L, Wang J. Comprehensive analysis of RNA-seq data reveals extensive RNA editing in a human transcriptome. Nat Biotechnol 2012, 30:253-260. 10.1038/nbt.2122, 22327324.
20. Ramaswami G, Lin W, Piskol R, Tan MH, Davis C, Li JB. Accurate identification of human Alu and non-Alu RNA editing sites. Nat Methods 2012, 9:579-581. 10.1038/nmeth.1982, 3662811, 22484847.
21. Hundley HA, Krauchuk AA, Bass BL. C. elegans and H. sapiens mRNAs with edited 3' UTRs are present on polysomes. RNA 2008, 14:2050-2060. 10.1261/rna.1165008, 2553745, 18719245.
22. Morse DP, Aruscavage PJ, Bass BL. RNA hairpins in noncoding regions of human brain and Caenorhabditis elegans mRNA are edited by adenosine deaminases that act on RNA. Proc Natl Acad Sci USA 2002, 99:7906-7911. 10.1073/pnas.112704299, 122993, 12048240.
23. Källman AM, Sahlin M, Öhman M. ADAR2 A-I editing: site selectivity and editing efficiency are separate events. Nucleic Acids Res 2003, 31:4874-4881. 10.1093/nar/gkg681, 169957, 12907730.
24. Thorrez L, Tranchevent LC, Chang HJ, Moreau Y, Schuit F. Detection of novel 3' untranslated region extensions with 3' expression microarrays. BMC Genomics 2010, 11:205. 10.1186/1471-2164-11-205, 2858751, 20346121.
25. Pollard KS, Hubisz MJ, Rosenbloom KR, Siepel A. Detection of nonneutral substitution rates on mammalian phylogenies. Genome Res 2010, 20:110-121. 10.1101/gr.097857.109, 2798823, 19858363.
26. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K, Clawson H, Spieth J, Hillier LW, Richards S, Weinstock GM, Wilson RK, Gibbs RA, Kent WJ, Miller W, Haussler D. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 2005, 15:1034-1050. 10.1101/gr.3715005, 1182216, 16024819.
27. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
28. da Huang W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009, 37:1-13. 10.1093/nar/gkn923, 2615629, 19033363.
29. Shen S, Lin L, Cai JJ, Jiang P, Kenkel EJ, Stroik MR, Sato S, Davidson BL, Xing Y. Widespread establishment and regulatory impact of Alu exons in human genes. Proc Natl Acad Sci USA 2011, 108:2837-2842. 10.1073/pnas.1012834108, 3041063, 21282640.
30. Li JB, Levanon EY, Yoon JK, Aach J, Xie B, Leproust E, Zhang K, Gao Y, Church GM. Genome-wide identification of human RNA editing sites by parallel DNA capturing and sequencing. Science 2009, 324:1210-1213. 10.1126/science.1170995, 19478186.
31. Yeo J, Goodman RA, Schirle NT, David SS, Beal PA. RNA editing changes the lesion specificity for the DNA repair enzyme NEIL1. Proc Natl Acad Sci USA 2010, 107:20715-20719. 10.1073/pnas.1009231107, 2996456, 21068368.
32. Shimokawa T, Rahman MF, Tostar U, Sonkoly E, Stahle M, Pivarcsi A, Palaniswamy R, Zaphiropoulos PG. RNA editing of the GLI1 transcription factor modulates the output of Hedgehog signaling. RNA Biol 2013, 10:321-333. 10.4161/rna.23343, 3594290, 23324600.
33. Suliman BA, Xu D, Williams BR. The promyelocytic leukemia zinc finger protein: two decades of molecular oncology. Front Oncol 2012, 2:74. 3398472, 22822476.
34. Ensterö M, Åkerborg O, Lundin D, Wang B, Furey TS, Öhman M, Lagergren J. A computational screen for site selective A-to-I editing detects novel sites in neuron specific Hu proteins. BMC Bioinformatics 2010, 11:6. 10.1186/1471-2105-11-6, 2831006, 20047656.
35. Gommans WM, Mullen SP, Maas S. RNA editing: a driving force for adaptive evolution?. Bioessays 2009, 31:1137-1145. 10.1002/bies.200900045, 2829293, 19708020.
36. Bratt E, Öhman M. Coordination of editing and splicing of glutamate receptor pre-mRNA. RNA 2003, 9:309-318. 10.1261/rna.2750803, 1370398, 12592005.
37. Desterro JM, Keegan LP, Lafarga M, Berciano MT, O'Connell M, Carmo-Fonseca M. Dynamic association of RNA-editing enzymes with the nucleolus. J Cell Sci 2003, 116:1805-1818. 10.1242/jcs.00371, 12665561.
38. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003, 31:3406-3415. 10.1093/nar/gkg595, 169194, 12824337.
39. Ding Y, Chan CY, Lawrence CE. RNA secondary structure prediction by centroids in a Boltzmann weighted ensemble. RNA 2005, 11:1157-1166. 10.1261/rna.2500605, 1370799, 16043502.
40. McLaren W, Pritchard B, Rios D, Chen Y, Flicek P, Cunningham F. Deriving the consequences of genomic variants with the Ensembl API and SNP effect predictor. BMC Bioinformatics 2010, 26:2069-2070.
41. UCSC table browser. [http://genome.ucsc.edu/cgi-bin/hgTables].
42. dbSNP. [http://www.ncbi.nlm.nih.gov/snp].
43. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-842. 10.1093/bioinformatics/btq033, 2832824, 20110278.
44. GNU core utilities sort program. [http://www.gnu.org/software/coreutils].
45. R core team. [http://www.R-project.org].
46. Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E. The role of site accessibility in microRNA target recognition. Nat Genet 2007, 39:1278-1284. 10.1038/ng2135, 17893677.