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PMID: 18337749 Published · ppublish English Journal Article Research Support, N.I.H., Intramural

Specific recognition of RNA/DNA hybrid and enhancement of human RNase H1 activity by HBD.

The EMBO journal ·Vol. 27 ·No. 7 ·2008-04-09 ·Pages 1172-81

Nowotny M, Cerritelli SM, Ghirlando R, Gaidamakov SA, Crouch RJ, Yang W

Abstract

Human RNase H1 contains an N-terminal domain known as dsRHbd for binding both dsRNA and RNA/DNA hybrid. We find that dsRHbd binds preferentially to RNA/DNA hybrids by over 25-fold and rename it as hybrid binding domain (HBD). The crystal structure of HBD complexed with a 12 bp RNA/DNA hybrid reveals that the RNA strand is recognized by a protein loop, which forms hydrogen bonds with the 2'-OH groups. The DNA interface is highly specific and contains polar residues that interact with the phosphate groups and an aromatic patch that appears selective for binding deoxyriboses. HBD is unique relative to non-sequence-specific dsDNA- and dsRNA-binding domains because it does not use positive dipoles of alpha-helices for nucleic acid binding. Characterization of full-length enzymes with defective HBDs indicates that this domain dramatically enhances both the specific activity and processivity of RNase H1. Similar activity enhancement by small substrate-binding domains linked to the catalytic domain likely occurs in other nucleic acid enzymes.

MeSH Terms
Amino Acid Sequence Animals Base Pairing Crystallography, X-Ray DNA/metabolism Humans Mice Models, Biological Molecular Sequence Data Mutagenesis Nucleic Acid Heteroduplexes/metabolism Protein Binding Protein Structure, Secondary Protein Structure, Tertiary RNA/metabolism Ribonuclease H/chemistry,metabolism Substrate Specificity
Chemicals
Nucleic Acid Heteroduplexes RNA DNA Ribonuclease H ribonuclease HI
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Nowotny Marcin
Laboratory of Molecular Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD 20892, USA.
Cerritelli Susana M
Ghirlando Rodolfo
Gaidamakov Sergei A
Crouch Robert J
Yang Wei
References (30)
30 references, click to expand
  1. Cloning, expression, and mapping of ribonucleases H of human and mouse related to bacterial RNase HI.
    Genomics. 1998 Nov 1;53(3):300-7 PMID: 9799596
  2. 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
  3. 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
  4. Common fold in helix-hairpin-helix proteins.
    Nucleic Acids Res. 2000 Jul 15;28(14):2643-50 PMID: 10908318
  5. 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
  6. Atomic positions in rhombohedral 2-zinc insulin crystals.
    Nature. 1971 Jun 25;231(5304):506-11 PMID: 4932997
  7. Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A.
    Science. 1991 May 10;252(5007):809-17 PMID: 2028256
  8. Ribonuclease revisited: structural insights into ribonuclease III family enzymes.
    Curr Opin Struct Biol. 2007 Feb;17(1):138-45 PMID: 17194582
  9. Crystal structures of RNase H bound to an RNA/DNA hybrid: substrate specificity and metal-dependent catalysis.
    Cell. 2005 Jul 1;121(7):1005-16 PMID: 15989951
  10. The helix-hairpin-helix DNA-binding motif: a structural basis for non-sequence-specific recognition of DNA.
    Nucleic Acids Res. 1996 Jul 1;24(13):2488-97 PMID: 8692686
  11. Eukaryotic RNases H1 act processively by interactions through the duplex RNA-binding domain.
    Nucleic Acids Res. 2005 Apr 14;33(7):2166-75 PMID: 15831789
  12. Stepwise analyses of metal ions in RNase H catalysis from substrate destabilization to product release.
    EMBO J. 2006 May 3;25(9):1924-33 PMID: 16601679
  13. NMR structure of the N-terminal domain of Saccharomyces cerevisiae RNase HI reveals a fold with a strong resemblance to the N-terminal domain of ribosomal protein L9.
    J Mol Biol. 1999 Aug 20;291(3):661-9 PMID: 10448044
  14. RNA recognition by a Staufen double-stranded RNA-binding domain.
    EMBO J. 2000 Mar 1;19(5):997-1009 PMID: 10698941
  15. 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
  16. Dissection of cauliflower mosaic virus transactivator/viroplasmin reveals distinct essential functions in basic virus replication.
    J Virol. 2003 Aug;77(15):8577-83 PMID: 12857928
  17. Eukaryotic RNAse H shares a conserved domain with caulimovirus proteins that facilitate translation of polycistronic RNA.
    Nucleic Acids Res. 1994 Oct 11;22(20):4163-6 PMID: 7937142
  18. Multiple RNA binding domains (RBDs) just don't add up.
    Nucleic Acids Res. 1995 Mar 11;23(5):725-8 PMID: 7535921
  19. 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
  20. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons.
    Proteins. 1991;11(4):281-96 PMID: 1758883
  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. Structural insight into the mechanism of double-stranded RNA processing by ribonuclease III.
    Cell. 2006 Jan 27;124(2):355-66 PMID: 16439209
  23. Coot: model-building tools for molecular graphics.
    Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32 PMID: 15572765
  24. RNA-binding proteins: modular design for efficient function.
    Nat Rev Mol Cell Biol. 2007 Jun;8(6):479-90 PMID: 17473849
  25. Failure to produce mitochondrial DNA results in embryonic lethality in Rnaseh1 null mice.
    Mol Cell. 2003 Mar;11(3):807-15 PMID: 12667461
  26. Effects of the alpha-helix dipole upon the functioning and structure of proteins and peptides.
    Adv Biophys. 1985;19:133-65 PMID: 2424281
  27. 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
  28. Structural basis for DNA bridging by barrier-to-autointegration factor.
    Nat Struct Mol Biol. 2005 Oct;12(10):935-6 PMID: 16155580
  29. Identification of the genes encoding Mn2+-dependent RNase HII and Mg2+-dependent RNase HIII from Bacillus subtilis: classification of RNases H into three families.
    Biochemistry. 1999 Jan 12;38(2):605-18 PMID: 9888800
  30. Structure of human RNase H1 complexed with an RNA/DNA hybrid: insight into HIV reverse transcription.
    Mol Cell. 2007 Oct 26;28(2):264-76 PMID: 17964265
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
1460-2075
Published
2008-04-09
Epub
2008-00-13
Pages
1172-81
Language
English
Region
England
NLM ID
8208664
PMCID
PMC2323259
Subset
IM
Grants
Intramural NIH HHS · United States
Databases
PDB
Analysis Services
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