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PMID: 9857205 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Molecular basis of double-stranded RNA-protein interactions: structure of a dsRNA-binding domain complexed with dsRNA.

The EMBO journal ·Vol. 17 ·No. 24 ·1998-12-15 ·Pages 7505-13

Ryter JM, Schultz SC

Abstract

Protein interactions with double-stranded RNA (dsRNA) are critical for many cell processes; however, in contrast to protein-dsDNA interactions, surprisingly little is known about the molecular basis of protein-dsRNA interactions. A large and diverse class of proteins that bind dsRNA do so by utilizing an approximately 70 amino acid motif referred to as the dsRNA-binding domain (dsRBD). We have determined a 1.9 A resolution crystal structure of the second dsRBD of Xenopus laevis RNA-binding protein A complexed with dsRNA. The structure shows that the protein spans 16 bp of dsRNA, interacting with two successive minor grooves and across the intervening major groove on one face of a primarily A-form RNA helix. The nature of these interactions explains dsRBD specificity for dsRNA (over ssRNA or dsDNA) and the apparent lack of sequence specificity. Interestingly, the dsRBD fold resembles a portion of the conserved core structure of a family of polynucleotidyl transferases that includes RuvC, MuA transposase, retroviral integrase and RNase H. Structural comparisons of the dsRBD-dsRNA complex and models proposed for polynucleotidyl transferase-nucleic acid complexes suggest that similarities in nucleic acid binding also exist between these families of proteins.

MeSH Terms
Amino Acid Sequence Animals Binding Sites Consensus Sequence Crystallography, X-Ray Models, Molecular Molecular Sequence Data Nucleic Acid Conformation Nucleotidyltransferases/chemistry Protein Binding Protein Conformation RNA, Double-Stranded/chemistry RNA-Binding Proteins/chemistry Xenopus Proteins Xenopus laevis
Chemicals
RNA, Double-Stranded RNA-Binding Proteins Xenopus Proteins Xlrbpa protein, Xenopus Nucleotidyltransferases
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Ryter J M
Department of Chemistry and Biochemistry, University of Colorado, Boulder, CO 80309-0215, USA.
Schultz S C
References (48)
48 references, click to expand
  1. Complete nucleotide sequence of bacteriophage T7 DNA and the locations of T7 genetic elements.
    J Mol Biol. 1983 Jun 5;166(4):477-535 PMID: 6864790
  2. Crystallography & NMR system: A new software suite for macromolecular structure determination.
    Acta Crystallogr D Biol Crystallogr. 1998 Sep 1;54(Pt 5):905-21 PMID: 9757107
  3. Recombinant-DNA-derived bovine growth hormone from Escherichia coli. 1. Demonstration that the hormone is expressed in reduced form, and isolation of the hormone in oxidized, native form.
    Eur J Biochem. 1987 Mar 2;163(2):313-21 PMID: 3545831
  4. Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates.
    Nucleic Acids Res. 1987 Nov 11;15(21):8783-98 PMID: 3684574
  5. The binding of double-stranded RNA and adenovirus VAI RNA to the interferon-induced protein kinase.
    Eur J Biochem. 1989 Jan 2;178(3):581-9 PMID: 2912723
  6. Protein-RNA interactions in an icosahedral virus at 3.0 A resolution.
    Science. 1989 Jul 14;245(4914):154-9 PMID: 2749253
  7. Structure of E. coli glutaminyl-tRNA synthetase complexed with tRNA(Gln) and ATP at 2.8 A resolution.
    Science. 1989 Dec 1;246(4934):1135-42 PMID: 2479982
  8. Interaction of adenovirus VA RNAl with the protein kinase DAI: nonequivalence of binding and function.
    Cell. 1990 Jun 1;61(5):843-52 PMID: 2188737
  9. Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon.
    Cell. 1990 Jul 27;62(2):379-90 PMID: 1695551
  10. The cleavage specificity of RNase III.
    Nucleic Acids Res. 1990 Aug 25;18(16):4809-15 PMID: 1697676
  11. Structure of ribonuclease H phased at 2 A resolution by MAD analysis of the selenomethionyl protein.
    Science. 1990 Sep 21;249(4975):1398-405 PMID: 2169648
  12. Translational control by the Epstein-Barr virus small RNA EBER-1. Reversal of the double-stranded RNA-induced inhibition of protein synthesis in reticulocyte lysates.
    Eur J Biochem. 1990 Nov 13;193(3):635-41 PMID: 2174360
  13. Characterization of a human TAR RNA-binding protein that activates the HIV-1 LTR.
    Science. 1991 Mar 29;251(5001):1597-600 PMID: 2011739
  14. Crystal structure of the ribonuclease H domain of HIV-1 reverse transcriptase.
    Science. 1991 Apr 5;252(5002):88-95 PMID: 1707186
  15. Improved methods for building protein models in electron density maps and the location of errors in these models.
    Acta Crystallogr A. 1991 Mar 1;47 ( Pt 2):110-9 PMID: 2025413
  16. A conserved sequence element in ribonuclease III processing signals is not required for accurate in vitro enzymatic cleavage.
    Nucleic Acids Res. 1991 Apr 25;19(8):1759-66 PMID: 1709490
  17. Class II aminoacyl transfer RNA synthetases: crystal structure of yeast aspartyl-tRNA synthetase complexed with tRNA(Asp).
    Science. 1991 Jun 21;252(5013):1682-9 PMID: 2047877
  18. Staufen, a gene required to localize maternal RNAs in the Drosophila egg.
    Cell. 1991 Jul 12;66(1):51-63 PMID: 1712672
  19. Mechanism of interferon action: cDNA structure, expression, and regulation of the interferon-induced, RNA-dependent P1/eIF-2 alpha protein kinase from human cells.
    Virology. 1992 May;188(1):33-46 PMID: 1373553
  20. The structure of ribosomal protein S5 reveals sites of interaction with 16S rRNA.
    Nature. 1992 Aug 27;358(6389):768-71 PMID: 1508272
  21. Interactions between double-stranded RNA regulators and the protein kinase DAI.
    Mol Cell Biol. 1992 Nov;12(11):5238-48 PMID: 1357546
  22. A conserved double-stranded RNA-binding domain.
    Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10979-83 PMID: 1438302
  23. Ordered duplex RNA controls capsid architecture in an icosahedral animal virus.
    Nature. 1993 Jan 14;361(6408):176-9 PMID: 8421524
  24. Double-helical RNA in satellite tobacco mosaic virus.
    Nature. 1993 Jan 14;361(6408):179-82 PMID: 8421525
  25. Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 A resolution shows bent DNA.
    Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):6320-4 PMID: 7687065
  26. Two RNA-binding motifs in the double-stranded RNA-activated protein kinase, DAI.
    Genes Dev. 1992 Dec;6(12B):2478-90 PMID: 1364113
  27. Comparative analysis of the regulation of the interferon-inducible protein kinase PKR by Epstein-Barr virus RNAs EBER-1 and EBER-2 and adenovirus VAI RNA.
    Nucleic Acids Res. 1993 Sep 25;21(19):4483-90 PMID: 7901835
  28. Structural characterization of a ribonuclease III processing signal.
    Nucleic Acids Res. 1994 Feb 25;22(4):604-12 PMID: 8127710
  29. Detection of dsRNA-binding domains in RNA helicase A and Drosophila maleless: implications for monomeric RNA helicases.
    Nucleic Acids Res. 1994 Jul 11;22(13):2552-6 PMID: 8041617
  30. Binding properties of newly identified Xenopus proteins containing dsRNA-binding motifs.
    Curr Biol. 1994 Apr 1;4(4):301-14 PMID: 7922339
  31. Atomic structure of the RuvC resolvase: a holliday junction-specific endonuclease from E. coli.
    Cell. 1994 Sep 23;78(6):1063-72 PMID: 7923356
  32. Molecular cloning of cDNA for double-stranded RNA adenosine deaminase, a candidate enzyme for nuclear RNA editing.
    Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11457-61 PMID: 7972084
  33. Preferential selection of adenosines for modification by double-stranded RNA adenosine deaminase.
    EMBO J. 1994 Dec 1;13(23):5701-11 PMID: 7527340
  34. Cloning of cDNAs encoding mammalian double-stranded RNA-specific adenosine deaminase.
    Mol Cell Biol. 1995 Mar;15(3):1389-97 PMID: 7862132
  35. Recombining the structures of HIV integrase, RuvC and RNase H.
    Structure. 1995 Feb 15;3(2):131-4 PMID: 7735828
  36. Structure of the bacteriophage Mu transposase core: a common structural motif for DNA transposition and retroviral integration.
    Cell. 1995 Jul 28;82(2):209-20 PMID: 7628012
  37. NMR solution structure of a dsRNA binding domain from Drosophila staufen protein reveals homology to the N-terminal domain of ribosomal protein S5.
    EMBO J. 1995 Jul 17;14(14):3563-71 PMID: 7628456
  38. Structure of the dsRNA binding domain of E. coli RNase III.
    EMBO J. 1995 Jul 17;14(14):3572-84 PMID: 7628457
  39. The non-RNase H domain of Saccharomyces cerevisiae RNase H1 binds double-stranded RNA: magnesium modulates the switch between double-stranded RNA binding and RNase H activity.
    RNA. 1995 May;1(3):246-59 PMID: 7489497
  40. Minor-groove recognition of double-stranded RNA by the double-stranded RNA-binding domain from the RNA-activated protein kinase PKR.
    Biochemistry. 1996 Aug 6;35(31):9983-94 PMID: 8756460
  41. Comparative mutational analysis of the double-stranded RNA binding domains of Xenopus laevis RNA-binding protein A.
    J Biol Chem. 1996 Nov 8;271(45):28112-9 PMID: 8910425
  42. Solution structure of (rGGCAGGCC)2 by two-dimensional NMR and the iterative relaxation matrix approach.
    Biochemistry. 1997 Apr 15;36(15):4449-60 PMID: 9109652
  43. 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
  44. Crystal structure of the nucleosome core particle at 2.8 A resolution.
    Nature. 1997 Sep 18;389(6648):251-60 PMID: 9305837
  45. Refined structure of satellite tobacco mosaic virus at 1.8 A resolution.
    J Mol Biol. 1998 Mar 20;277(1):37-59 PMID: 9514737
  46. A common 40 amino acid motif in eukaryotic RNases H1 and caulimovirus ORF VI proteins binds to duplex RNAs.
    Nucleic Acids Res. 1998 Apr 1;26(7):1834-40 PMID: 9512560
  47. Binding of the protein kinase PKR to RNAs with secondary structure defects: role of the tandem A-G mismatch and noncontiguous helixes.
    Biochemistry. 1998 May 5;37(18):6303-16 PMID: 9572845
  48. The DNA sequence of the gene (rnc) encoding ribonuclease III of Escherichia coli.
    Nucleic Acids Res. 1985 Jul 11;13(13):4677-85 PMID: 3895158
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1998-12-15
Pages
7505-13
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1171094
Subset
IM
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