Home LiteratureArticle Details
PMID: 25921533 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Cis regulatory effects on A-to-I RNA editing in related Drosophila species.

Cell reports ·Vol. 11 ·No. 5 ·2015-05-05 ·Pages 697-703

Sapiro AL, Deng P, Zhang R, Li JB

Abstract

Adenosine-to-inosine RNA editing modifies maturing mRNAs through the binding of adenosine deaminase acting on RNA (Adar) proteins to double-stranded RNA structures in a process critical for neuronal function. Editing levels at individual editing sites span a broad range and are mediated by both cis-acting elements (surrounding RNA sequence and secondary structure) and trans-acting factors. Here, we aim to determine the roles that cis-acting elements and trans-acting factors play in regulating editing levels. Using two closely related Drosophila species, D. melanogaster and D. sechellia, and their F1 hybrids, we dissect the effects of cis sequences from trans regulators on editing levels by comparing species-specific editing in parents and their hybrids. We report that cis sequence differences are largely responsible for editing level differences between these two Drosophila species. This study presents evidence for cis sequence and structure changes as the dominant evolutionary force that modulates RNA editing levels between these Drosophila species.

MeSH Terms
Adenosine/metabolism Adenosine Deaminase/chemistry,genetics,metabolism Animals Drosophila/metabolism Drosophila Proteins/chemistry,genetics,metabolism Female Inosine/metabolism Male Nucleic Acid Conformation RNA Editing RNA, Double-Stranded/chemistry,metabolism RNA, Messenger/metabolism Regulatory Elements, Transcriptional/genetics
Chemicals
Drosophila Proteins RNA, Double-Stranded RNA, Messenger Inosine Adar protein, Drosophila Adenosine Deaminase Adenosine
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Sapiro Anne L
Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA.
Deng Patricia
Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA.
Zhang Rui
Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA.
Li Jin Billy
Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA. Electronic address: [email protected].
References (32)
32 references, click to expand
  1. Functions and regulation of RNA editing by ADAR deaminases.
    Annu Rev Biochem. 2010;79:321-49 PMID: 20192758
  2. Nascent-seq indicates widespread cotranscriptional RNA editing in Drosophila.
    Mol Cell. 2012 Jul 13;47(1):27-37 PMID: 22658416
  3. Predicting sites of ADAR editing in double-stranded RNA.
    Nat Commun. 2011;2:319 PMID: 21587236
  4. Detection of regulatory variation in mouse genes.
    Nat Genet. 2002 Nov;32(3):432-7 PMID: 12410233
  5. 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.
    Neuron. 2000 Jan;25(1):139-49 PMID: 10707979
  6. The developmental transcriptome of Drosophila melanogaster.
    Nature. 2011 Mar 24;471(7339):473-9 PMID: 21179090
  7. Modulation of dADAR-dependent RNA editing by the Drosophila fragile X mental retardation protein.
    Nat Neurosci. 2011 Dec;14(12):1517-24 PMID: 22037499
  8. Deep sequencing the circadian and diurnal transcriptome of Drosophila brain.
    Genome Res. 2012 Jul;22(7):1266-81 PMID: 22472103
  9. Tuning of RNA editing by ADAR is required in Drosophila.
    EMBO J. 2005 Jun 15;24(12):2183-93 PMID: 15920480
  10. A distant cis acting intronic element induces site-selective RNA editing.
    Nucleic Acids Res. 2012 Oct;40(19):9876-86 PMID: 22848101
  11. Deciphering the functions and regulation of brain-enriched A-to-I RNA editing.
    Nat Neurosci. 2013 Nov;16(11):1518-22 PMID: 24165678
  12. RNA editing by adenosine deaminases that act on RNA.
    Annu Rev Biochem. 2002;71:817-46 PMID: 12045112
  13. RNAstructure: software for RNA secondary structure prediction and analysis.
    BMC Bioinformatics. 2010;11:129 PMID: 20230624
  14. A high-throughput screen to identify enhancers of ADAR-mediated RNA-editing.
    RNA Biol. 2013 Feb;10(2):192-204 PMID: 23353575
  15. Tertiary structural elements determine the extent and specificity of messenger RNA editing.
    Nat Commun. 2013;4:2232 PMID: 23903876
  16. Pin1 and WWP2 regulate GluR2 Q/R site RNA editing by ADAR2 with opposing effects.
    EMBO J. 2011 Oct 19;30(20):4211-22 PMID: 21847096
  17. Genome-wide analysis of A-to-I RNA editing by single-molecule sequencing in Drosophila.
    Nat Struct Mol Biol. 2013 Nov;20(11):1333-9 PMID: 24077224
  18. RADAR: a rigorously annotated database of A-to-I RNA editing.
    Nucleic Acids Res. 2014 Jan;42(Database issue):D109-13 PMID: 24163250
  19. Auto-regulatory RNA editing fine-tunes mRNA re-coding and complex behaviour in Drosophila.
    Nat Commun. 2012;3:790 PMID: 22531175
  20. ADAR regulates RNA editing, transcript stability, and gene expression.
    Cell Rep. 2013 Nov 14;5(3):849-60 PMID: 24183664
  21. A-to-I pre-mRNA editing in Drosophila is primarily involved in adult nervous system function and integrity.
    Cell. 2000 Aug 18;102(4):437-49 PMID: 10966106
  22. Functional conservation in human and Drosophila of Metazoan ADAR2 involved in RNA editing: loss of ADAR1 in insects.
    Nucleic Acids Res. 2011 Sep 1;39(16):7249-62 PMID: 21622951
  23. Transcript diversification in the nervous system: a to I RNA editing in CNS function and disease development.
    Front Neurosci. 2012 Jul 09;6:99 PMID: 22787438
  24. The intricate relationship between RNA structure, editing, and splicing.
    Semin Cell Dev Biol. 2012 May;23(3):281-8 PMID: 22178616
  25. Functions and mechanisms of RNA editing.
    Annu Rev Genet. 2000;34:499-531 PMID: 11092837
  26. A structural determinant required for RNA editing.
    Nucleic Acids Res. 2011 Jul;39(13):5669-81 PMID: 21427087
  27. Quantifying RNA allelic ratios by microfluidic multiplex PCR and sequencing.
    Nat Methods. 2014 Jan;11(1):51-4 PMID: 24270603
  28. A-to-I RNA editing: effects on proteins key to neural excitability.
    Neuron. 2012 May 10;74(3):432-9 PMID: 22578495
  29. RNA-interacting proteins act as site-specific repressors of ADAR2-mediated RNA editing and fluctuate upon neuronal stimulation.
    Nucleic Acids Res. 2013 Feb 1;41(4):2581-93 PMID: 23275536
  30. Identifying RNA editing sites using RNA sequencing data alone.
    Nat Methods. 2013 Feb;10(2):128-32 PMID: 23291724
  31. Molecular determinants and guided evolution of species-specific RNA editing.
    Nature. 2005 Mar 17;434(7031):409-13 PMID: 15772668
  32. Evolutionary changes in cis and trans gene regulation.
    Nature. 2004 Jul 1;430(6995):85-8 PMID: 15229602
Article Info
Journal
Cell reports
Abbr.
Cell Rep
ISSN
2211-1247
Published
2015-05-05
Epub
2015-00-23
Pages
697-703
Language
English
Region
United States
NLM ID
101573691
PMCID
PMC4418222
Subset
IM
Grants
NIGMS NIH HHS · R01 GM102484 · United States
NIGMS NIH HHS · T32 GM007276 · United States
NHGRI NIH HHS · T32 HG000044 · United States
NIGMS NIH HHS · T32 GM007790 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]