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PMID: 14612560 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Modulation of RNA editing by functional nucleolar sequestration of ADAR2.

Sansam CL, Wells KS, Emeson RB

Abstract

The adenosine deaminases that act on RNA (ADARs) catalyze the site-specific conversion of adenosine to inosine (A to I) in primary mRNA transcripts, thereby affecting the splicing pattern or coding potential of mature mRNAs. Although the subnuclear localization of A-to-I editing has not been precisely defined, ADARs have been shown to act before splicing, suggesting that they function near nucleoplasmic sites of transcription. Here we demonstrate that ADAR2, a member of the vertebrate ADAR family, is concentrated in the nucleolus, a subnuclear domain disparate from the sites of mRNA transcription. Selective inhibition of ribosomal RNA synthesis or the introduction of mutations in the double-stranded RNA-binding domains within ADAR2 results in translocation of the protein to the nucleoplasm, suggesting that nucleolar association of ADAR2 depends on its ability to bind to ribosomal RNA. Fluorescence recovery after photobleaching reveals that ADAR2 can shuttle rapidly between subnuclear compartments. Enhanced translocation of endogenous ADAR2 from the nucleolus to the nucleoplasm results in increased editing of endogenous ADAR2 substrates. These observations indicate that the nucleolar localization of ADAR2 represents an important mechanism by which RNA editing can be modulated by the sequestration of enzymatic activity from potential RNA substrates in the nucleoplasm.

MeSH Terms
Adenosine Deaminase/genetics,metabolism Amino Acid Sequence Animals Base Sequence Cell Line Cell Nucleolus/metabolism In Vitro Techniques Mice Molecular Sequence Data NIH 3T3 Cells RNA Editing RNA Precursors/genetics,metabolism RNA, Double-Stranded/genetics,metabolism RNA, Ribosomal/genetics,metabolism RNA-Binding Proteins Rats Recombinant Fusion Proteins/genetics,metabolism Substrate Specificity
Chemicals
RNA Precursors RNA, Double-Stranded RNA, Ribosomal RNA-Binding Proteins Recombinant Fusion Proteins ADARB1 protein, human Adenosine Deaminase
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Sansam Christopher L
Department of Pharmacology, Vanderbilt University, Nashville, TN 37232, USA.
Wells K Sam
Emeson Ronald B
References (57)
57 references, click to expand
  1. Nucleolar Arf sequesters Mdm2 and activates p53.
    Nat Cell Biol. 1999 May;1(1):20-6 PMID: 10559859
  2. To be or not to be in the nucleolus.
    Nat Cell Biol. 2000 Jun;2(6):E107-12 PMID: 10854340
  3. Dynamics and three-dimensional localization of ribosomal RNA within the nucleolus.
    RNA. 2000 Dec;6(12):1750-61 PMID: 11142375
  4. Protein dynamics: implications for nuclear architecture and gene expression.
    Science. 2001 Feb 2;291(5505):843-7 PMID: 11225636
  5. On the importance of being co-transcriptional.
    J Cell Sci. 2002 Oct 15;115(Pt 20):3865-71 PMID: 12244124
  6. A nucleolar targeting sequence in the Werner syndrome protein resides within residues 949-1092.
    J Cell Sci. 2002 Oct 15;115(Pt 20):3901-7 PMID: 12244128
  7. RNA editing by adenosine deaminases generates RNA and protein diversity.
    Biochimie. 2002 Aug;84(8):791-803 PMID: 12457566
  8. A-to-I RNA editing: recent news and residual mysteries.
    J Biol Chem. 2003 Jan 17;278(3):1391-4 PMID: 12446659
  9. Dynamic association of RNA-editing enzymes with the nucleolus.
    J Cell Sci. 2003 May 1;116(Pt 9):1805-18 PMID: 12665561
  10. Biochemical analysis and scanning force microscopy reveal productive and nonproductive ADAR2 binding to RNA substrates.
    RNA. 2003 Jul;9(7):839-46 PMID: 12810917
  11. Structure of an alanine transfer ribonucleic acid.
    JAMA. 1965 Nov 22;194(8):868-71 PMID: 5898068
  12. Inhibition of RNA synthesis by actinomycin D: characteristic dose-response of different RNA species.
    J Cell Physiol. 1970 Oct;76(2):127-39 PMID: 5500970
  13. Structure of mouse rRNA precursors. Complete sequence and potential folding of the spacer regions between 18S and 28S rRNA.
    Nucleic Acids Res. 1983 May 25;11(10):3375-91 PMID: 6304630
  14. High-efficiency transformation of mammalian cells by plasmid DNA.
    Mol Cell Biol. 1987 Aug;7(8):2745-52 PMID: 3670292
  15. Sequence and secondary structure of the 5' external transcribed spacer of mouse pre-rRNA.
    DNA. 1988 Apr;7(3):181-91 PMID: 2836145
  16. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells.
    Nucleic Acids Res. 1989 Aug 11;17(15):6419 PMID: 2771659
  17. Effects of a highly basic region of human immunodeficiency virus Tat protein on nucleolar localization.
    J Virol. 1990 Apr;64(4):1803-7 PMID: 2108259
  18. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line.
    Nucleic Acids Res. 1990 Jun 25;18(12):3587-96 PMID: 2194165
  19. The mechanism of adenosine to inosine conversion by the double-stranded RNA unwinding/modifying activity: a high-performance liquid chromatography-mass spectrometry analysis.
    Biochemistry. 1991 Dec 10;30(49):11507-14 PMID: 1747369
  20. Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit.
    Neuron. 1992 Jan;8(1):189-98 PMID: 1370372
  21. A conserved double-stranded RNA-binding domain.
    Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10979-83 PMID: 1438302
  22. Determinants of Ca2+ permeability in both TM1 and TM2 of high affinity kainate receptor channels: diversity by RNA editing.
    Neuron. 1993 Mar;10(3):491-500 PMID: 7681676
  23. Production of high titre helper-free recombinant retroviral vectors by lipofection.
    Nucleic Acids Res. 1994 Mar 25;22(6):1117-8 PMID: 8152916
  24. Purification and characterization of double-stranded RNA adenosine deaminase from bovine nuclear extracts.
    J Biol Chem. 1994 May 6;269(18):13480-9 PMID: 8175781
  25. Control of kinetic properties of AMPA receptor channels by nuclear RNA editing.
    Science. 1994 Dec 9;266(5191):1709-13 PMID: 7992055
  26. Mutational analysis of the double-stranded RNA (dsRNA) binding domain of the dsRNA-activated protein kinase, PKR.
    J Biol Chem. 1995 Feb 10;270(6):2601-6 PMID: 7852324
  27. Cloning of cDNAs encoding mammalian double-stranded RNA-specific adenosine deaminase.
    Mol Cell Biol. 1995 Mar;15(3):1389-97 PMID: 7862132
  28. Glutamate receptor RNA editing in vitro by enzymatic conversion of adenosine to inosine.
    Science. 1995 Mar 10;267(5203):1491-4 PMID: 7878468
  29. Mutational analysis of p80 coilin indicates a functional interaction between coiled bodies and the nucleolus.
    J Cell Biol. 1995 Nov;131(4):817-31 PMID: 7490287
  30. A mammalian RNA editing enzyme.
    Nature. 1996 Feb 1;379(6564):460-4 PMID: 8559253
  31. Regulation of serotonin-2C receptor G-protein coupling by RNA editing.
    Nature. 1997 May 15;387(6630):303-8 PMID: 9153397
  32. Xlrbpa, a double-stranded RNA-binding protein associated with ribosomes and heterogeneous nuclear RNPs.
    J Cell Biol. 1997 Jul 28;138(2):239-53 PMID: 9230068
  33. A CTD function linking transcription to splicing.
    Trends Biochem Sci. 1997 Nov;22(11):413-6 PMID: 9397679
  34. Tad1p, a yeast tRNA-specific adenosine deaminase, is related to the mammalian pre-mRNA editing enzymes ADAR1 and ADAR2.
    EMBO J. 1998 Aug 17;17(16):4780-9 PMID: 9707437
  35. Mutational analysis of the structure and localization of the nucleolus in the yeast Saccharomyces cerevisiae.
    J Cell Biol. 1998 Oct 5;143(1):23-34 PMID: 9763418
  36. Molecular basis of double-stranded RNA-protein interactions: structure of a dsRNA-binding domain complexed with dsRNA.
    EMBO J. 1998 Dec 15;17(24):7505-13 PMID: 9857205
  37. Structure and functions of nucleolin.
    J Cell Sci. 1999 Mar;112 ( Pt 6):761-72 PMID: 10036227
  38. Regulation of alternative splicing by RNA editing.
    Nature. 1999 May 6;399(6731):75-80 PMID: 10331393
  39. Evolutionarily conserved structural features in the ITS2 of mammalian pre-rRNAs and potential interactions with the snoRNA U8 detected by comparative analysis of new mouse sequences.
    Nucleic Acids Res. 1999 Jun 1;27(11):2271-82 PMID: 10325414
  40. mRNA polyadenylation and its coupling to other RNA processing reactions and to transcription.
    Curr Opin Cell Biol. 1999 Jun;11(3):352-7 PMID: 10395555
  41. Base pairing between U3 small nucleolar RNA and the 5' end of 18S rRNA is required for pre-rRNA processing.
    Mol Cell Biol. 1999 Sep;19(9):6012-9 PMID: 10454548
  42. The dynamics of a pre-mRNA splicing factor in living cells.
    Nature. 1997 May 29;387(6632):523-7 PMID: 9168118
  43. UV induces nucleolar translocation of ING1 through two distinct nucleolar targeting sequences.
    Nucleic Acids Res. 2001 May 15;29(10):2052-8 PMID: 11353074
  44. RNA editing activity is associated with splicing factors in lnRNP particles: The nuclear pre-mRNA processing machinery.
    Proc Natl Acad Sci U S A. 2001 Jun 5;98(12):6571-6 PMID: 11381114
  45. The rules and roles of nucleocytoplasmic shuttling proteins.
    FEBS Lett. 2001 Jun 8;498(2-3):157-63 PMID: 11412848
  46. Nuclear domains.
    J Cell Sci. 2001 Aug;114(Pt 16):2891-3 PMID: 11686292
  47. RNA editing of the human serotonin 5-HT2C receptor alters receptor-mediated activation of G13 protein.
    J Biol Chem. 2001 Nov 30;276(48):44663-8 PMID: 11572865
  48. RNA editing by adenosine deaminases that act on RNA.
    Annu Rev Biochem. 2002;71:817-46 PMID: 12045112
  49. 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 U S A. 2002 Jun 11;99(12):7906-11 PMID: 12048240
  50. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis.
    Nature. 2002 Jun 27;417(6892):967-70 PMID: 12068309
  51. Subnuclear shuttling of human telomerase induced by transformation and DNA damage.
    Nat Cell Biol. 2002 Sep;4(9):731-6 PMID: 12198499
  52. Signal recognition particle components in the nucleolus.
    Proc Natl Acad Sci U S A. 2000 Jan 4;97(1):55-60 PMID: 10618370
  53. Altered G protein-coupling functions of RNA editing isoform and splicing variant serotonin2C receptors.
    J Neurochem. 2000 Mar;74(3):1290-300 PMID: 10693963
  54. RNA recognition by a Staufen double-stranded RNA-binding domain.
    EMBO J. 2000 Mar 1;19(5):997-1009 PMID: 10698941
  55. Identification of a cryptic nucleolar-localization signal in MDM2.
    Nat Cell Biol. 2000 Mar;2(3):179-81 PMID: 10707090
  56. High mobility of proteins in the mammalian cell nucleus.
    Nature. 2000 Apr 6;404(6778):604-9 PMID: 10766243
  57. Nuclear lamins A and B1: different pathways of assembly during nuclear envelope formation in living cells.
    J Cell Biol. 2000 Dec 11;151(6):1155-68 PMID: 11121432
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2003-11-25
Epub
2003-00-11
Pages
14018-23
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC283538
Subset
IM
Grants
NINDS NIH HHS · R01 NS033323 · United States
NINDS NIH HHS · NS33323 · United States
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