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PMID: 24722121 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

RNA editome in rhesus macaque shaped by purifying selection.

PLoS genetics ·Vol. 10 ·No. 4 ·2014-04-00 ·Pages e1004274

Chen JY, Peng Z, Zhang R, Yang XZ, Tan BC, Fang H, Liu CJ, Shi M, Ye ZQ, Zhang YE, Deng M, Zhang X, Li CY

Abstract

Understanding of the RNA editing process has been broadened considerably by the next generation sequencing technology; however, several issues regarding this regulatory step remain unresolved--the strategies to accurately delineate the editome, the mechanism by which its profile is maintained, and its evolutionary and functional relevance. Here we report an accurate and quantitative profile of the RNA editome for rhesus macaque, a close relative of human. By combining genome and transcriptome sequencing of multiple tissues from the same animal, we identified 31,250 editing sites, of which 99.8% are A-to-G transitions. We verified 96.6% of editing sites in coding regions and 97.5% of randomly selected sites in non-coding regions, as well as the corresponding levels of editing by multiple independent means, demonstrating the feasibility of our experimental paradigm. Several lines of evidence supported the notion that the adenosine deamination is associated with the macaque editome--A-to-G editing sites were flanked by sequences with the attributes of ADAR substrates, and both the sequence context and the expression profile of ADARs are relevant factors in determining the quantitative variance of RNA editing across different sites and tissue types. In support of the functional relevance of some of these editing sites, substitution valley of decreased divergence was detected around the editing site, suggesting the evolutionary constraint in maintaining some of these editing substrates with their double-stranded structure. These findings thus complement the "continuous probing" model that postulates tinkering-based origination of a small proportion of functional editing sites. In conclusion, the macaque editome reported here highlights RNA editing as a widespread functional regulation in primate evolution, and provides an informative framework for further understanding RNA editing in human.

MeSH Terms
Adenosine/genetics Adenosine Deaminase/genetics Animals Genome/genetics Macaca mulatta/genetics RNA/genetics RNA Editing/genetics Transcriptome/genetics
Chemicals
RNA Adenosine Deaminase Adenosine
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
Chen Jia-Yu
Beijing Key Laboratory of Cardiometabolic Molecular Medicine, Institute of Molecular Medicine, Peking University, Beijing, China.
Peng Zhiyu
BGI-Guangzhou, Guangzhou, China; BGI-Shenzhen, Shenzhen, China.
Zhang Rongli
Beijing Key Laboratory of Cardiometabolic Molecular Medicine, Institute of Molecular Medicine, Peking University, Beijing, China.
Yang Xin-Zhuang
Beijing Key Laboratory of Cardiometabolic Molecular Medicine, Institute of Molecular Medicine, Peking University, Beijing, China.
Tan Bertrand Chin-Ming
Department of Biomedical Sciences and Graduate Institute of Biomedical Sciences, College of Medicine, Chang Gung University, Tao-Yuan, Taiwan.
Fang Huaying
School of Mathematical Sciences and Center for Quantitative Biology, Peking University, Beijing, China.
Liu Chu-Jun
Beijing Key Laboratory of Cardiometabolic Molecular Medicine, Institute of Molecular Medicine, Peking University, Beijing, China.
Shi Mingming
BGI-Shenzhen, Shenzhen, China.
Ye Zhi-Qiang
Lab of Computational Chemistry and Drug Design, Key Laboratory of Chemical Genomics, Peking University Shenzhen Graduate School, Shenzhen, China.
Zhang Yong E
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.
Deng Minghua
School of Mathematical Sciences and Center for Quantitative Biology, Peking University, Beijing, China.
Zhang Xiuqin
Beijing Key Laboratory of Cardiometabolic Molecular Medicine, Institute of Molecular Medicine, Peking University, Beijing, China.
Li Chuan-Yun
Beijing Key Laboratory of Cardiometabolic Molecular Medicine, Institute of Molecular Medicine, Peking University, Beijing, China.
References (57)
57 references, click to expand
  1. Adenosine-to-inosine RNA editing shapes transcriptome diversity in primates.
    Proc Natl Acad Sci U S A. 2010 Jul 6;107(27):12174-9 PMID: 20566853
  2. Adenosine-to-inosine RNA editing affects trafficking of the gamma-aminobutyric acid type A (GABA(A)) receptor.
    J Biol Chem. 2011 Jan 21;286(3):2031-40 PMID: 21030585
  3. Hominoid-specific de novo protein-coding genes originating from long non-coding RNAs.
    PLoS Genet. 2012 Sep;8(9):e1002942 PMID: 23028352
  4. The difficult calls in RNA editing. Interviewed by H Craig Mak.
    Nat Biotechnol. 2012 Dec;30(12):1207-9 PMID: 23222792
  5. Widespread RNA and DNA sequence differences in the human transcriptome.
    Science. 2011 Jul 1;333(6038):53-8 PMID: 21596952
  6. Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA.
    Cell. 1986 Sep 12;46(6):819-26 PMID: 3019552
  7. Posttranscriptional recoding by RNA editing.
    Adv Protein Chem Struct Biol. 2012;86:193-224 PMID: 22243585
  8. Mammalian microRNAs: experimental evaluation of novel and previously annotated genes.
    Genes Dev. 2010 May 15;24(10):992-1009 PMID: 20413612
  9. Comment on "Widespread RNA and DNA sequence differences in the human transcriptome".
    Science. 2012 Mar 16;335(6074):1302; author reply 1302 PMID: 22422962
  10. Transcriptome analysis by strand-specific sequencing of complementary DNA.
    Nucleic Acids Res. 2009 Oct;37(18):e123 PMID: 19620212
  11. The Gene Ontology: enhancements for 2011.
    Nucleic Acids Res. 2012 Jan;40(Database issue):D559-64 PMID: 22102568
  12. Evolutionarily conserved A-to-I editing increases protein stability of the alternative splicing factor Nova1.
    RNA Biol. 2012 Jan;9(1):12-21 PMID: 22258141
  13. Double-stranded RNA adenosine deaminases ADAR1 and ADAR2 have overlapping specificities.
    Biochemistry. 2000 Oct 24;39(42):12875-84 PMID: 11041852
  14. RNA editing in brain controls a determinant of ion flow in glutamate-gated channels.
    Cell. 1991 Oct 4;67(1):11-9 PMID: 1717158
  15. RNA editing at arg607 controls AMPA receptor exit from the endoplasmic reticulum.
    Neuron. 2002 May 30;34(5):759-72 PMID: 12062022
  16. Identification of widespread ultra-edited human RNAs.
    PLoS Genet. 2011 Oct;7(10):e1002317 PMID: 22028664
  17. Human BLCAP transcript: new editing events in normal and cancerous tissues.
    Int J Cancer. 2010 Jul 1;127(1):127-37 PMID: 19908260
  18. RhesusBase: a knowledgebase for the monkey research community.
    Nucleic Acids Res. 2013 Jan;41(Database issue):D892-905 PMID: 22965133
  19. Evolutionary interrogation of human biology in well-annotated genomic framework of rhesus macaque.
    Mol Biol Evol. 2014 May;31(5):1309-24 PMID: 24577841
  20. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project.
    Nature. 2007 Jun 14;447(7146):799-816 PMID: 17571346
  21. Resequencing of 200 human exomes identifies an excess of low-frequency non-synonymous coding variants.
    Nat Genet. 2010 Nov;42(11):969-72 PMID: 20890277
  22. Evolutionary dynamics of gene and isoform regulation in Mammalian tissues.
    Science. 2012 Dec 21;338(6114):1593-9 PMID: 23258891
  23. Genome-wide in silico identification and analysis of cis natural antisense transcripts (cis-NATs) in ten species.
    Nucleic Acids Res. 2006 Jul 18;34(12):3465-75 PMID: 16849434
  24. Comment on "Widespread RNA and DNA sequence differences in the human transcriptome".
    Science. 2012 Mar 16;335(6074):1302; author reply 1302 PMID: 22422964
  25. Systematic identification of abundant A-to-I editing sites in the human transcriptome.
    Nat Biotechnol. 2004 Aug;22(8):1001-5 PMID: 15258596
  26. Comprehensive analysis of RNA-Seq data reveals extensive RNA editing in a human transcriptome.
    Nat Biotechnol. 2012 Feb 12;30(3):253-60 PMID: 22327324
  27. IGFBP7's susceptibility to proteolysis is altered by A-to-I RNA editing of its transcript.
    FEBS Lett. 2012 Jul 30;586(16):2313-7 PMID: 22750143
  28. Two Sample Logo: a graphical representation of the differences between two sets of sequence alignments.
    Bioinformatics. 2006 Jun 15;22(12):1536-7 PMID: 16632492
  29. Two potential biomarkers identified in mesenchymal stem cells and leukocytes of patients with sporadic amyotrophic lateral sclerosis.
    Dis Markers. 2012;32(4):211-20 PMID: 22430187
  30. Accurate identification of A-to-I RNA editing in human by transcriptome sequencing.
    Genome Res. 2012 Jan;22(1):142-50 PMID: 21960545
  31. A-to-I RNA editing alters less-conserved residues of highly conserved coding regions: implications for dual functions in evolution.
    RNA. 2008 Aug;14(8):1516-25 PMID: 18567816
  32. Evolutionarily conserved human targets of adenosine to inosine RNA editing.
    Nucleic Acids Res. 2005 Feb 24;33(4):1162-8 PMID: 15731336
  33. Editing modifies the GABA(A) receptor subunit alpha3.
    RNA. 2007 May;13(5):698-703 PMID: 17369310
  34. The evolution of gene expression levels in mammalian organs.
    Nature. 2011 Oct 19;478(7369):343-8 PMID: 22012392
  35. Early-onset epilepsy and postnatal lethality associated with an editing-deficient GluR-B allele in mice.
    Science. 1995 Dec 8;270(5242):1677-80 PMID: 7502080
  36. RNA editing changes the lesion specificity for the DNA repair enzyme NEIL1.
    Proc Natl Acad Sci U S A. 2010 Nov 30;107(48):20715-9 PMID: 21068368
  37. Comment on "Widespread RNA and DNA sequence differences in the human transcriptome".
    Science. 2012 Mar 16;335(6074):1302; author reply 1302 PMID: 22422963
  38. A-to-I editing sites are a genomically encoded G: implications for the evolutionary significance and identification of novel editing sites.
    RNA. 2008 Feb;14(2):211-6 PMID: 18094120
  39. Genome-wide identification of human RNA editing sites by parallel DNA capturing and sequencing.
    Science. 2009 May 29;324(5931):1210-3 PMID: 19478186
  40. Editing of AMPA and serotonin 2C receptors in individual central neurons, controlling wakefulness.
    Cell Mol Neurobiol. 2007 Aug;27(5):669-80 PMID: 17554622
  41. Accurate identification of human Alu and non-Alu RNA editing sites.
    Nat Methods. 2012 Jun;9(6):579-81 PMID: 22484847
  42. Extensive genomic and transcriptional diversity identified through massively parallel DNA and RNA sequencing of eighteen Korean individuals.
    Nat Genet. 2011 Jul 03;43(8):745-52 PMID: 21725310
  43. RNA editing of the glutamate receptor subunits GluR2 and GluR6 in human brain tissue.
    J Neurochem. 1994 Nov;63(5):1596-602 PMID: 7523595
  44. Evidence of altered RNA stirs debate.
    Nature. 2011 May 26;473(7348):432 PMID: 21614050
  45. Large-scale analysis of structural, sequence and thermodynamic characteristics of A-to-I RNA editing sites in human Alu repeats.
    BMC Genomics. 2010 Jul 28;11:453 PMID: 20667096
  46. RNA editing: a driving force for adaptive evolution?
    Bioessays. 2009 Oct;31(10):1137-45 PMID: 19708020
  47. Evolution and tinkering.
    Science. 1977 Jun 10;196(4295):1161-6 PMID: 860134
  48. Lineage-specific variation in intensity of natural selection in mammals.
    Mol Biol Evol. 2011 Jan;28(1):383-98 PMID: 20688808
  49. Predicting sites of ADAR editing in double-stranded RNA.
    Nat Commun. 2011;2:319 PMID: 21587236
  50. Consistent levels of A-to-I RNA editing across individuals in coding sequences and non-conserved Alu repeats.
    BMC Genomics. 2010 Oct 28;11:608 PMID: 21029430
  51. Nervous system targets of RNA editing identified by comparative genomics.
    Science. 2003 Aug 8;301(5634):832-6 PMID: 12907802
  52. Very few RNA and DNA sequence differences in the human transcriptome.
    PLoS One. 2011;6(10):e25842 PMID: 22022455
  53. A rapid, sensitive, reproducible and cost-effective method for mutation profiling of colon cancer and metastatic lymph nodes.
    BMC Cancer. 2010 Mar 16;10:101 PMID: 20233444
  54. The UCSC Genome Browser database: extensions and updates 2011.
    Nucleic Acids Res. 2012 Jan;40(Database issue):D918-23 PMID: 22086951
  55. Limitations of the rhesus macaque draft genome assembly and annotation.
    BMC Genomics. 2012 May 30;13:206 PMID: 22646658
  56. ADAR1 and ADAR2 expression and editing activity during forebrain development.
    Dev Neurosci. 2009;31(3):223-37 PMID: 19325227
  57. Antisense sequencing improves the accuracy and precision of A-to-I editing measurements using the peak height ratio method.
    BMC Res Notes. 2012 Jan 24;5:63 PMID: 22269019
Article Info
Journal
PLoS genetics
Abbr.
PLoS Genet
ISSN
1553-7404
Published
2014-04-00
Epub
2014-00-10
Pages
e1004274
Language
English
Region
United States
NLM ID
101239074
PMCID
PMC3983040
Subset
IM
Analysis Services
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