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PMID: 19442245 Published · ppublish English Lecture Research Support, Non-U.S. Gov't

The search for a human Holliday junction resolvase.

Biochemical Society transactions ·Vol. 37 ·No. Pt 3 ·2009-06-00 ·Pages 519-26

West SC

Abstract

Four-way DNA intermediates, known as Holliday junctions, are formed during mitotic and meiotic recombination, and their efficient resolution is essential for proper chromosome segregation. Bacteria, bacteriophages and archaea promote Holliday junction resolution by the introduction of symmetrically related nicks across the junction, in reactions mediated by Holliday junction resolvases. In 2008, after a search that lasted almost 20 years, a Holliday junction resolvase was identified in humans. The protein, GEN1, was identified using MS following the brute-force fractionation of extracts prepared from human cells grown in tissue culture. GEN1 fits the paradigm developed from studies of prokaryotic Holliday junction resolvases, in that it specifically recognizes junctions and resolves them using a mechanism similar to that exhibited by the Escherichia coli RuvC protein.

MeSH Terms
DNA, Cruciform/genetics,metabolism Holliday Junction Resolvases/genetics,metabolism Humans Models, Biological Nucleic Acid Conformation Saccharomyces cerevisiae/enzymology,genetics Saccharomyces cerevisiae Proteins/genetics,metabolism
Chemicals
DNA, Cruciform Saccharomyces cerevisiae Proteins Holliday Junction Resolvases
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
West Stephen C
London Research Institute, Clare Hall Laboratories, Cancer Research UK, South Mimms, Hertfordshire, UK. stephen.west@cancer.org.uk
References (66)
66 references, click to expand
  1. RNA interference inhibition of Mus81 reduces mitotic recombination in human cells.
    Mol Biol Cell. 2004 Feb;15(2):552-62 PMID: 14617801
  2. Enzymes of general recombination.
    Annu Rev Biochem. 1987;56:229-62 PMID: 3304134
  3. Resolution of synthetic Holliday junctions in DNA by an endonuclease activity from calf thymus.
    EMBO J. 1990 Sep;9(9):2931-6 PMID: 2167838
  4. Involvement of mammalian Mus81 in genome integrity and tumor suppression.
    Science. 2004 Jun 18;304(5678):1822-6 PMID: 15205536
  5. Eme1 is involved in DNA damage processing and maintenance of genomic stability in mammalian cells.
    EMBO J. 2003 Nov 17;22(22):6137-47 PMID: 14609959
  6. Homologous pairing in genetic recombination: recA protein makes joint molecules of gapped circular DNA and closed circular DNA.
    Cell. 1980 May;20(1):223-35 PMID: 7388943
  7. Cleavage of cruciform DNA structures by an activity from Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1985 Oct;82(19):6445-9 PMID: 3901001
  8. Mus81-Eme1 are essential components of a Holliday junction resolvase.
    Cell. 2001 Nov 16;107(4):537-48 PMID: 11719193
  9. The structure of the Holliday junction, and its resolution.
    Cell. 1988 Oct 7;55(1):79-89 PMID: 3167979
  10. A role for MMS4 in the processing of recombination intermediates during meiosis in Saccharomyces cerevisiae.
    Genetics. 2001 Dec;159(4):1511-25 PMID: 11779793
  11. Enzymes and molecular mechanisms of genetic recombination.
    Annu Rev Biochem. 1992;61:603-40 PMID: 1497320
  12. Generating crossovers by resolution of nicked Holliday junctions: a role for Mus81-Eme1 in meiosis.
    Mol Cell. 2003 Sep;12(3):761-74 PMID: 14527420
  13. The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast.
    Genetics. 2003 May;164(1):81-94 PMID: 12750322
  14. Figure-8 configuration of dimers of S13 and phiX174 replicative form DNA.
    J Mol Biol. 1975 Feb 5;91(4):409-19 PMID: 1080203
  15. Atomic structure of the RuvC resolvase: a holliday junction-specific endonuclease from E. coli.
    Cell. 1994 Sep 23;78(6):1063-72 PMID: 7923356
  16. Occurrence of crossed strand-exchange forms in yeast DNA during meiosis.
    Proc Natl Acad Sci U S A. 1979 Jul;76(7):3445-9 PMID: 386340
  17. Escherichia coli RuvC protein is an endonuclease that resolves the Holliday structure.
    EMBO J. 1991 Dec;10(13):4381-9 PMID: 1661673
  18. Crystal structure of a DNA Holliday junction.
    Nat Struct Biol. 1999 Oct;6(10):913-7 PMID: 10504723
  19. Resolution of Holliday junctions in vitro requires the Escherichia coli ruvC gene product.
    Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6063-7 PMID: 1829835
  20. Global analysis of protein expression in yeast.
    Nature. 2003 Oct 16;425(6959):737-41 PMID: 14562106
  21. Enzymatic formation of biparental figure-eight molecules from plasmid DNA and their resolution in E. coli.
    Cell. 1983 Mar;32(3):817-29 PMID: 6339073
  22. Identification of Holliday junction resolvases from humans and yeast.
    Nature. 2008 Nov 20;456(7220):357-61 PMID: 19020614
  23. Crystal structure of an 82-nucleotide RNA-DNA complex formed by the 10-23 DNA enzyme.
    Nat Struct Biol. 1999 Feb;6(2):151-6 PMID: 10048927
  24. Disruption of murine Mus81 increases genomic instability and DNA damage sensitivity but does not promote tumorigenesis.
    Mol Cell Biol. 2005 Sep;25(17):7569-79 PMID: 16107704
  25. Resolution of Holliday junctions in Escherichia coli: identification of the ruvC gene product as a 19-kilodalton protein.
    J Bacteriol. 1991 Dec;173(23):7711-5 PMID: 1657895
  26. Biochemistry of genetic recombination: energetics and mechanism of DNA strand exchange.
    Annu Rev Biophys Biophys Chem. 1991;20:539-75 PMID: 1831022
  27. More complexity to the Bloom's syndrome complex.
    Genes Dev. 2008 Oct 15;22(20):2737-42 PMID: 18923071
  28. Fluorescence energy transfer shows that the four-way DNA junction is a right-handed cross of antiparallel molecules.
    Nature. 1989 Oct 26;341(6244):763-6 PMID: 2797209
  29. Crystal structure of the fission yeast mitochondrial Holliday junction resolvase Ydc2.
    EMBO J. 2001 Dec 3;20(23):6601-11 PMID: 11726496
  30. Processing of recombination intermediates by the RuvABC proteins.
    Annu Rev Genet. 1997;31:213-44 PMID: 9442895
  31. Holliday junction resolvase in Schizosaccharomyces pombe has identical endonuclease activity to the CCE1 homologue YDC2.
    Nucleic Acids Res. 1998 Jan 15;26(2):594-601 PMID: 9421521
  32. Synthetic junctions as tools to identify and characterize Holliday junction resolvases.
    Methods Enzymol. 2006;408:485-501 PMID: 16793388
  33. The fuss about Mus81.
    Cell. 2001 Nov 30;107(5):551-4 PMID: 11733053
  34. Molecular analysis of the Escherichia coli ruvC gene, which encodes a Holliday junction-specific endonuclease.
    J Bacteriol. 1991 Sep;173(18):5747-53 PMID: 1885548
  35. Gel electrophoretic analysis of the geometry of a DNA four-way junction.
    J Mol Biol. 1987 Dec 20;198(4):711-9 PMID: 2828644
  36. Biochemical characterization of the hjc holliday junction resolvase of Pyrococcus furiosus.
    Nucleic Acids Res. 2000 Nov 15;28(22):4544-51 PMID: 11071944
  37. Mismatch repair in replication fidelity, genetic recombination, and cancer biology.
    Annu Rev Biochem. 1996;65:101-33 PMID: 8811176
  38. T4 endonuclease VII cleaves holliday structures.
    Cell. 1982 Jun;29(2):357-65 PMID: 6288255
  39. Mus81 cleavage of Holliday junctions: a failsafe for processing meiotic recombination intermediates?
    EMBO J. 2007 Apr 4;26(7):1891-901 PMID: 17363897
  40. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast.
    Cell. 2003 Nov 14;115(4):401-11 PMID: 14622595
  41. A new Holliday junction resolving enzyme from Schizosaccharomyces pombe that is homologous to CCE1 from Saccharomyces cerevisiae.
    J Mol Biol. 1997 Oct 3;272(4):509-22 PMID: 9325108
  42. Recombinant DNA molecules of bacteriophage phi chi174.
    Proc Natl Acad Sci U S A. 1975 Jan;72(1):235-9 PMID: 1054500
  43. Saccharomyces cerevisiae Mus81-Mms4 is a catalytic, DNA structure-selective endonuclease.
    Nucleic Acids Res. 2008 Apr;36(7):2182-95 PMID: 18281703
  44. Enzymes and sites of genetic recombination: studies with gene-3 endonuclease of phage T7 and with site-affinity mutants of phage lambda.
    Cold Spring Harb Symp Quant Biol. 1984;49:715-26 PMID: 6099255
  45. Structures of helical junctions in nucleic acids.
    Q Rev Biophys. 2000 May;33(2):109-59 PMID: 11131562
  46. XPG endonuclease makes the 3' incision in human DNA nucleotide excision repair.
    Nature. 1994 Sep 29;371(6496):432-5 PMID: 8090225
  47. The structure of Escherichia coli RusA endonuclease reveals a new Holliday junction DNA binding fold.
    Structure. 2003 Dec;11(12):1557-67 PMID: 14656440
  48. The Bloom's syndrome helicase suppresses crossing over during homologous recombination.
    Nature. 2003 Dec 18;426(6968):870-4 PMID: 14685245
  49. EXO1-A multi-tasking eukaryotic nuclease.
    DNA Repair (Amst). 2004 Dec 2;3(12):1549-59 PMID: 15474417
  50. Resolution of recombination intermediates by a mammalian activity functionally analogous to Escherichia coli RuvC resolvase.
    J Biol Chem. 1994 Feb 18;269(7):5202-9 PMID: 8106502
  51. X-ray structure of T4 endonuclease VII: a DNA junction resolvase with a novel fold and unusual domain-swapped dimer architecture.
    EMBO J. 1999 Mar 15;18(6):1447-58 PMID: 10075917
  52. The endogenous Mus81-Eme1 complex resolves Holliday junctions by a nick and counternick mechanism.
    Mol Cell. 2003 Sep;12(3):747-59 PMID: 14527419
  53. Identification and characterization of the human mus81-eme1 endonuclease.
    J Biol Chem. 2003 Jul 4;278(27):25172-8 PMID: 12721304
  54. Crystal structure of the Holliday junction resolving enzyme T7 endonuclease I.
    Nat Struct Biol. 2001 Jan;8(1):62-7 PMID: 11135673
  55. A conserved nuclease domain in the archaeal Holliday junction resolving enzyme Hjc.
    J Biol Chem. 2000 Aug 18;275(33):25540-6 PMID: 10940317
  56. Formation and resolution of recombination intermediates by E. coli RecA and RuvC proteins.
    Nature. 1991 Dec 19-26;354(6354):506-10 PMID: 1758493
  57. Flap endonuclease 1: a central component of DNA metabolism.
    Annu Rev Biochem. 2004;73:589-615 PMID: 15189154
  58. BLAP75/RMI1 promotes the BLM-dependent dissolution of homologous recombination intermediates.
    Proc Natl Acad Sci U S A. 2006 Mar 14;103(11):4068-73 PMID: 16537486
  59. Structure of Hjc, a Holliday junction resolvase, from Sulfolobus solfataricus.
    Proc Natl Acad Sci U S A. 2001 May 8;98(10):5509-14 PMID: 11331763
  60. The FEN-1 family of structure-specific nucleases in eukaryotic DNA replication, recombination and repair.
    Bioessays. 1997 Mar;19(3):233-40 PMID: 9080773
  61. Genetic recombination in Escherichia coli: Holliday junctions made by RecA protein are resolved by fractionated cell-free extracts.
    Proc Natl Acad Sci U S A. 1990 Nov;87(21):8476-80 PMID: 2146685
  62. Partial purification of an enzyme from Saccharomyces cerevisiae that cleaves Holliday junctions.
    Proc Natl Acad Sci U S A. 1985 Nov;82(21):7247-51 PMID: 3903750
  63. Branch migration and Holliday junction resolution catalyzed by activities from mammalian cells.
    Cell. 2001 Jan 26;104(2):259-68 PMID: 11207366
  64. The Holliday junction in an inverted repeat DNA sequence: sequence effects on the structure of four-way junctions.
    Proc Natl Acad Sci U S A. 2000 Apr 11;97(8):3971-6 PMID: 10760268
  65. Identification and characterization of yeast mutants and the gene for a cruciform cutting endonuclease.
    EMBO J. 1992 Feb;11(2):699-704 PMID: 1537343
  66. Role of circular dimer DNA in the primary recombination mechanism of bacteriophage S13.
    Nat New Biol. 1973 Mar 7;242(114):9-12 PMID: 4511842
Article Info
Journal
Biochemical Society transactions
Abbr.
Biochem Soc Trans
ISSN
1470-8752
Published
2009-06-00
Pages
519-26
Language
English
Region
England
NLM ID
7506897
PMCID
PMC4120095
Subset
IM
Grants
Breast Cancer Now · 2009MAYPR01 · United Kingdom
European Research Council · 249145 · International
Cancer Research UK · A3563 · United Kingdom
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