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PMID: 21177854 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The structure of the human RNase H2 complex defines key interaction interfaces relevant to enzyme function and human disease.

The Journal of biological chemistry ·Vol. 286 ·No. 12 ·2011-03-25 ·Pages 10530-9

Reijns MA, Bubeck D, Gibson LC, Graham SC, Baillie GS, Jones EY, Jackson AP

Abstract

Ribonuclease H2 (RNase H2) is the major nuclear enzyme involved in the degradation of RNA/DNA hybrids and removal of ribonucleotides misincorporated in genomic DNA. Mutations in each of the three RNase H2 subunits have been implicated in a human auto-inflammatory disorder, Aicardi-Goutières Syndrome (AGS). To understand how mutations impact on RNase H2 function we determined the crystal structure of the human heterotrimer. In doing so, we correct several key regions of the previously reported murine RNase H2 atomic model and provide biochemical validation for our structural model. Our results provide new insights into how the subunits are arranged to form an enzymatically active complex. In particular, we establish that the RNASEH2A C terminus is a eukaryotic adaptation for binding the two accessory subunits, with residues within it required for enzymatic activity. This C-terminal extension interacts with the RNASEH2C C terminus and both are necessary to form a stable, enzymatically active heterotrimer. Disease mutations cluster at this interface between all three subunits, destabilizing the complex and/or impairing enzyme activity. Altogether, we locate 25 out of 29 residues mutated in AGS patients, establishing a firm basis for future investigations into disease pathogenesis and function of the RNase H2 enzyme.

MeSH Terms
Animals Autoimmune Diseases of the Nervous System/enzymology,genetics Crystallography, X-Ray Humans Mice Models, Molecular Nervous System Malformations/enzymology,genetics Protein Structure, Quaternary Protein Structure, Tertiary Protein Subunits Ribonuclease H/chemistry,genetics,metabolism Structure-Activity Relationship
Chemicals
Protein Subunits ribonuclease HII Ribonuclease H
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Reijns Martin A M
Medical Research Council Human Genetics Unit, Institute of Genetics and Molecular Medicine, Western General Hospital, Edinburgh EH4 2XU, United Kingdom.
Bubeck Doryen
Gibson Lucien C D
Graham Stephen C
Baillie George S
Jones E Yvonne
Jackson Andrew P
Supplementary Concepts
Aicardi-Goutieres syndrome (Disease)
References (32)
32 references, click to expand
  1. Clinical and molecular phenotype of Aicardi-Goutieres syndrome.
    Am J Hum Genet. 2007 Oct;81(4):713-25 PMID: 17846997
  2. Mutations in the gene encoding the 3'-5' DNA exonuclease TREX1 cause Aicardi-Goutières syndrome at the AGS1 locus.
    Nat Genet. 2006 Aug;38(8):917-20 PMID: 16845398
  3. The SPOT-synthesis technique. Synthetic peptide arrays on membrane supports--principles and applications.
    J Immunol Methods. 2002 Sep 1;267(1):13-26 PMID: 12135797
  4. Ribonuclease H from K562 human erythroleukemia cells. Purification, characterization, and substrate specificity.
    J Biol Chem. 1991 Apr 5;266(10):6472-9 PMID: 1706718
  5. Methods for protein characterization by mass spectrometry, thermal shift (ThermoFluor) assay, and multiangle or static light scattering.
    Methods Mol Biol. 2008;426:299-318 PMID: 18542872
  6. RNaseH2 mutants that cause Aicardi-Goutieres syndrome are active nucleases.
    J Mol Med (Berl). 2009 Jan;87(1):25-30 PMID: 19034401
  7. Inactivation of the SR protein splicing factor ASF/SF2 results in genomic instability.
    Cell. 2005 Aug 12;122(3):365-78 PMID: 16096057
  8. Mutations in genes encoding ribonuclease H2 subunits cause Aicardi-Goutières syndrome and mimic congenital viral brain infection.
    Nat Genet. 2006 Aug;38(8):910-6 PMID: 16845400
  9. A scanning peptide array approach uncovers association sites within the JNK/beta arrestin signalling complex.
    FEBS Lett. 2009 Oct 20;583(20):3310-6 PMID: 19782076
  10. RNase H2 of Saccharomyces cerevisiae is a complex of three proteins.
    Nucleic Acids Res. 2004 Jan 20;32(2):407-14 PMID: 14734815
  11. Trex1 prevents cell-intrinsic initiation of autoimmunity.
    Cell. 2008 Aug 22;134(4):587-98 PMID: 18724932
  12. Synthesis of peptide arrays using SPOT-technology and the CelluSpots-method.
    Methods Mol Biol. 2009;570:157-74 PMID: 19649591
  13. Molecular replacement with MOLREP.
    Acta Crystallogr D Biol Crystallogr. 2010 Jan;66(Pt 1):22-5 PMID: 20057045
  14. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions.
    Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2256-68 PMID: 15572779
  15. Discontinuous replication of replicative form DNA from bacteriophage phiX174.
    Proc Natl Acad Sci U S A. 1977 Jul;74(7):2776-9 PMID: 268627
  16. Effect of the disease-causing mutations identified in human ribonuclease (RNase) H2 on the activities and stabilities of yeast RNase H2 and archaeal RNase HII.
    FEBS J. 2008 Oct;275(19):4836-49 PMID: 18721139
  17. Telomerase limits the extent of base pairing between template RNA and telomeric DNA.
    EMBO Rep. 2005 Apr;6(4):361-6 PMID: 15776019
  18. PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations.
    Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W665-7 PMID: 15215472
  19. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids.
    Nucleic Acids Res. 2007 Jul;35(Web Server issue):W375-83 PMID: 17452350
  20. Expanding the phenotypic spectrum of lupus erythematosus in Aicardi-Goutières syndrome.
    Arthritis Rheum. 2010 May;62(5):1469-77 PMID: 20131292
  21. MEK1 binds directly to betaarrestin1, influencing both its phosphorylation by ERK and the timing of its isoprenaline-stimulated internalization.
    J Biol Chem. 2009 Apr 24;284(17):11425-35 PMID: 19153083
  22. Structural biochemistry of a type 2 RNase H: RNA primer recognition and removal during DNA replication.
    J Mol Biol. 2001 Mar 23;307(2):541-56 PMID: 11254381
  23. The Uppsala Electron-Density Server.
    Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2240-9 PMID: 15572777
  24. Abundant ribonucleotide incorporation into DNA by yeast replicative polymerases.
    Proc Natl Acad Sci U S A. 2010 Mar 16;107(11):4949-54 PMID: 20194773
  25. The structure of the mammalian RNase H2 complex provides insight into RNA.NA hybrid processing to prevent immune dysfunction.
    J Biol Chem. 2010 Feb 5;285(6):3617-3624 PMID: 19923215
  26. Electrostatics of nanosystems: application to microtubules and the ribosome.
    Proc Natl Acad Sci U S A. 2001 Aug 28;98(18):10037-41 PMID: 11517324
  27. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT.
    Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2210-21 PMID: 15572774
  28. Proliferating cell nuclear antigen (PCNA): a dancer with many partners.
    J Cell Sci. 2003 Aug 1;116(Pt 15):3051-60 PMID: 12829735
  29. PHENIX: a comprehensive Python-based system for macromolecular structure solution.
    Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21 PMID: 20124702
  30. Contributions of the two accessory subunits, RNASEH2B and RNASEH2C, to the activity and properties of the human RNase H2 complex.
    Nucleic Acids Res. 2009 Jan;37(1):96-110 PMID: 19015152
  31. ALINE: a WYSIWYG protein-sequence alignment editor for publication-quality alignments.
    Acta Crystallogr D Biol Crystallogr. 2009 May;65(Pt 5):510-2 PMID: 19390156
  32. Trex1 exonuclease degrades ssDNA to prevent chronic checkpoint activation and autoimmune disease.
    Cell. 2007 Nov 30;131(5):873-86 PMID: 18045533
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
1083-351X
Published
2011-03-25
Epub
2010-00-22
Pages
10530-9
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC3060506
Subset
IM
Grants
Medical Research Council · G0900084 · United Kingdom
Wellcome Trust · 075491/Z04 · United Kingdom
Cancer Research UK · United Kingdom
Biotechnology and Biological Sciences Research Council · United Kingdom
Databases
PDB
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