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PMID: 15899853 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, P.H.S.

Yeast Rmi1/Nce4 controls genome stability as a subunit of the Sgs1-Top3 complex.

Molecular and cellular biology ·Vol. 25 ·No. 11 ·2005-06-00 ·Pages 4476-87

Mullen JR, Nallaseth FS, Lan YQ, Slagle CE, Brill SJ

Abstract

Genome stability requires a set of RecQ-Top3 DNA helicase-topoisomerase complexes whose sole budding yeast homolog is encoded by SGS1-TOP3. RMI1/NCE4 was identified as a potential intermediate in the SGS1-TOP3 pathway, based on the observation that strains lacking any one of these genes require MUS81 and MMS4 for viability. This idea was tested by confirming that sgs1 and rmi1 mutants display the same spectrum of synthetic lethal interactions, including the requirements for SLX1, SLX4, SLX5, and SLX8, and by demonstrating that rmi1 mus81 synthetic lethality is dependent on homologous recombination. On their own, mutations in RMI1 result in phenotypes that mimic those of sgs1 or top3 strains including slow growth, hyperrecombination, DNA damage sensitivity, and reduced sporulation. And like top3 strains, most rmi1 phenotypes are suppressed by mutations in SGS1. We show that Rmi1 forms a heteromeric complex with Sgs1-Top3 in yeast and that these proteins interact directly in a recombinant system. The Rmi1-Top3 complex is stable in the absence of the Sgs1 helicase, but the loss of either Rmi1 or Top3 in yeast compromises its partner's interaction with Sgs1. Biochemical studies demonstrate that recombinant Rmi1 is a structure-specific DNA binding protein with a preference for cruciform structures. We propose that the DNA binding specificity of Rmi1 plays a role in targeting Sgs1-Top3 to appropriate substrates.

MeSH Terms
Amino Acid Sequence Conserved Sequence DNA Damage DNA Helicases/genetics,metabolism DNA Topoisomerases, Type I/metabolism DNA, Single-Stranded/metabolism DNA-Binding Proteins/genetics,metabolism,physiology Endonucleases/metabolism Genome, Fungal Genomic Instability Molecular Sequence Data Mutation Protein Subunits/genetics,physiology RecQ Helicases Recombination, Genetic Saccharomyces cerevisiae/enzymology,genetics Saccharomyces cerevisiae Proteins/genetics,metabolism,physiology
Chemicals
DNA, Single-Stranded DNA-Binding Proteins Protein Subunits Rmi1 protein, S cerevisiae Saccharomyces cerevisiae Proteins Endonucleases MUS81 protein, S cerevisiae SGS1 protein, S cerevisiae DNA Helicases RecQ Helicases DNA Topoisomerases, Type I
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Mullen Janet R
Department of Molecular Biology and Biochemistry, Rutgers University, CABM, 679 Hoes Ln., Piscataway, NJ 08854, USA.
Nallaseth Ferez S
Lan Yan Q
Slagle Christopher E
Brill Steven J
References (60)
60 references, click to expand
  1. Elg1 forms an alternative RFC complex important for DNA replication and genome integrity.
    EMBO J. 2003 Aug 15;22(16):4304-13 PMID: 12912927
  2. The essential role of yeast topoisomerase III in meiosis depends on recombination.
    EMBO J. 1999 Mar 15;18(6):1701-11 PMID: 10075939
  3. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast.
    Cell. 2003 Nov 14;115(4):401-11 PMID: 14622595
  4. The Bloom's syndrome helicase suppresses crossing over during homologous recombination.
    Nature. 2003 Dec 18;426(6968):870-4 PMID: 14685245
  5. Global mapping of the yeast genetic interaction network.
    Science. 2004 Feb 6;303(5659):808-13 PMID: 14764870
  6. Determination of mitotic recombination rates by fluctuation analysis in Saccharomyces cerevisiae.
    Methods Mol Biol. 2004;262:3-12 PMID: 14769952
  7. Identification of a potent decatenating enzyme from Escherichia coli.
    J Biol Chem. 1988 Sep 15;263(26):13366-73 PMID: 2843517
  8. Multiple sequence alignment with hierarchical clustering.
    Nucleic Acids Res. 1988 Nov 25;16(22):10881-90 PMID: 2849754
  9. Elevated recombination rates in transcriptionally active DNA.
    Cell. 1989 Feb 24;56(4):619-30 PMID: 2645056
  10. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
    Genetics. 1989 May;122(1):19-27 PMID: 2659436
  11. A hyper-recombination mutation in S. cerevisiae identifies a novel eukaryotic topoisomerase.
    Cell. 1989 Jul 28;58(2):409-19 PMID: 2546682
  12. Use of T7 RNA polymerase to direct expression of cloned genes.
    Methods Enzymol. 1990;185:60-89 PMID: 2199796
  13. Identification of the yeast TOP3 gene product as a single strand-specific DNA topoisomerase.
    J Biol Chem. 1992 Aug 25;267(24):17178-85 PMID: 1324925
  14. A gene with specific and global effects on recombination of sequences from tandemly repeated genes in Saccharomyces cerevisiae.
    Genetics. 1993 Nov;135(3):711-8 PMID: 8293975
  15. RecQ helicase and topoisomerase III comprise a novel DNA strand passage function: a conserved mechanism for control of DNA recombination.
    Mol Cell. 1999 May;3(5):611-20 PMID: 10360177
  16. Oligomeric ring structure of the Bloom's syndrome helicase.
    Curr Biol. 1999 Jun 3;9(11):597-600 PMID: 10359700
  17. Binding specificity determines polarity of DNA unwinding by the Sgs1 protein of S. cerevisiae.
    J Mol Biol. 1999 Jun 4;289(2):235-48 PMID: 10366502
  18. Defending genome integrity during DNA replication: a proposed role for RecQ family helicases.
    Bioessays. 1999 Apr;21(4):286-94 PMID: 10377891
  19. Topoisomerase III is essential for accurate nuclear division in Schizosaccharomyces pombe.
    Nucleic Acids Res. 1999 Oct 15;27(20):4050-8 PMID: 10497270
  20. The ability of Sgs1 to interact with DNA topoisomerase III is essential for damage-induced recombination.
    DNA Repair (Amst). 2005 Feb 3;4(2):191-201 PMID: 15590327
  21. Decatenating activity of Escherichia coli DNA gyrase and topoisomerases I and III during oriC and pBR322 DNA replication in vitro.
    J Biol Chem. 1994 Jan 21;269(3):2093-9 PMID: 8294462
  22. The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase.
    Mol Cell Biol. 1994 Dec;14(12):8391-8 PMID: 7969174
  23. The top3(+) gene is essential in Schizosaccharomyces pombe and the lethality associated with its loss is caused by Rad12 helicase activity.
    Nucleic Acids Res. 1999 Dec 15;27(24):4715-24 PMID: 10572171
  24. The Bloom's syndrome gene product interacts with topoisomerase III.
    J Biol Chem. 2000 Mar 31;275(13):9636-44 PMID: 10734115
  25. Functional characterization of Caenorhabditis elegans DNA topoisomerase IIIalpha.
    Nucleic Acids Res. 2000 May 1;28(9):2012-7 PMID: 10756204
  26. Bipartite structure of the SGS1 DNA helicase in Saccharomyces cerevisiae.
    Genetics. 2000 Mar;154(3):1101-14 PMID: 10757756
  27. Homologous recombination is responsible for cell death in the absence of the Sgs1 and Srs2 helicases.
    Nat Genet. 2000 Jun;25(2):192-4 PMID: 10835635
  28. The Bloom's syndrome gene product promotes branch migration of holliday junctions.
    Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6504-8 PMID: 10823897
  29. Sgs1 helicase activity is required for mitotic but apparently not for meiotic functions.
    Mol Cell Biol. 2000 Sep;20(17):6399-409 PMID: 10938117
  30. Interaction between yeast sgs1 helicase and DNA topoisomerase III.
    J Biol Chem. 2000 Sep 1;275(35):26898-905 PMID: 10862619
  31. Genetic analysis of the Saccharomyces cerevisiae Sgs1 helicase defines an essential function for the Sgs1-Top3 complex in the absence of SRS2 or TOP1.
    Mol Gen Genet. 2000 Sep;264(1-2):89-97 PMID: 11016837
  32. LCD1: an essential gene involved in checkpoint control and regulation of the MEC1 signalling pathway in Saccharomyces cerevisiae.
    EMBO J. 2000 Nov 1;19(21):5801-12 PMID: 11060031
  33. SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination.
    Nat Genet. 2001 Jan;27(1):113-6 PMID: 11138010
  34. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae.
    Genetics. 2001 Jan;157(1):103-18 PMID: 11139495
  35. Involvement of SGS1 in DNA damage-induced heteroallelic recombination that requires RAD52 in Saccharomyces cerevisiae.
    Mol Gen Genet. 2001 Jan;264(5):702-8 PMID: 11212925
  36. Werner's syndrome protein (WRN) migrates Holliday junctions and co-localizes with RPA upon replication arrest.
    EMBO Rep. 2000 Jul;1(1):80-4 PMID: 11256630
  37. Mapping the DNA topoisomerase III binding domain of the Sgs1 DNA helicase.
    J Biol Chem. 2001 Mar 23;276(12):8848-55 PMID: 11124263
  38. The N-terminal region of Sgs1, which interacts with Top3, is required for complementation of MMS sensitivity and suppression of hyper-recombination in sgs1 disruptants.
    Mol Genet Genomics. 2001 Jul;265(5):837-50 PMID: 11523801
  39. Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease.
    Genes Dev. 2001 Oct 15;15(20):2730-40 PMID: 11641278
  40. Mus81-Eme1 are essential components of a Holliday junction resolvase.
    Cell. 2001 Nov 16;107(4):537-48 PMID: 11719193
  41. Systematic genetic analysis with ordered arrays of yeast deletion mutants.
    Science. 2001 Dec 14;294(5550):2364-8 PMID: 11743205
  42. Functional and physical interaction between Sgs1 and Top3 and Sgs1-independent function of Top3 in DNA recombination repair.
    Genes Genet Syst. 2002 Feb;77(1):11-21 PMID: 12036100
  43. Mutations in homologous recombination genes rescue top3 slow growth in Saccharomyces cerevisiae.
    Genetics. 2002 Oct;162(2):647-62 PMID: 12399378
  44. The severe slow growth of Deltasrs2 Deltarqh1 in Schizosaccharomyces pombe is suppressed by loss of recombination and checkpoint genes.
    Nucleic Acids Res. 2002 Nov 1;30(21):4781-92 PMID: 12409469
  45. Alternate pathways involving Sgs1/Top3, Mus81/ Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication.
    Proc Natl Acad Sci U S A. 2002 Dec 24;99(26):16887-92 PMID: 12475932
  46. A genome-wide screen for methyl methanesulfonate-sensitive mutants reveals genes required for S phase progression in the presence of DNA damage.
    Proc Natl Acad Sci U S A. 2002 Dec 24;99(26):16934-9 PMID: 12482937
  47. Inactivation of homologous recombination suppresses defects in topoisomerase III-deficient mutants.
    DNA Repair (Amst). 2002 Jun 21;1(6):463-82 PMID: 12509234
  48. Topoisomerase III can serve as the cellular decatenase in Escherichia coli.
    J Biol Chem. 2003 Mar 7;278(10):8653-60 PMID: 12509418
  49. RecQ helicases: caretakers of the genome.
    Nat Rev Cancer. 2003 Mar;3(3):169-78 PMID: 12612652
  50. The mechanism of Mus81-Mms4 cleavage site selection distinguishes it from the homologous endonuclease Rad1-Rad10.
    Mol Cell Biol. 2003 May;23(10):3487-96 PMID: 12724407
  51. Role for the fission yeast RecQ helicase in DNA repair in G2.
    Mol Cell Biol. 2003 May;23(10):3692-705 PMID: 12724426
  52. Characterization of a novel origin recognition complex-like complex: implications for DNA recognition, cell cycle control, and locus-specific gene amplification.
    Mol Cell Biol. 2003 Jul;23(14):5005-17 PMID: 12832485
  53. Sgs1: a eukaryotic homolog of E. coli RecQ that interacts with topoisomerase II in vivo and is required for faithful chromosome segregation.
    Cell. 1995 Apr 21;81(2):253-60 PMID: 7736577
  54. A new efficient gene disruption cassette for repeated use in budding yeast.
    Nucleic Acids Res. 1996 Jul 1;24(13):2519-24 PMID: 8692690
  55. A hierarchy of SSB protomers in replication protein A.
    Genes Dev. 1996 Sep 1;10(17):2222-33 PMID: 8804316
  56. SGS1, a homologue of the Bloom's and Werner's syndrome genes, is required for maintenance of genome stability in Saccharomyces cerevisiae.
    Genetics. 1996 Nov;144(3):935-45 PMID: 8913739
  57. Role of Schizosaccharomyces pombe RecQ homolog, recombination, and checkpoint genes in UV damage tolerance.
    Mol Cell Biol. 1997 Dec;17(12):6868-75 PMID: 9372918
  58. Fission yeast rad12+ regulates cell cycle checkpoint control and is homologous to the Bloom's syndrome disease gene.
    Mol Cell Biol. 1998 May;18(5):2721-8 PMID: 9566891
  59. Bloom's and Werner's syndrome genes suppress hyperrecombination in yeast sgs1 mutant: implication for genomic instability in human diseases.
    Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8733-8 PMID: 9671747
  60. DNA helicase gene interaction network defined using synthetic lethality analyzed by microarray.
    Nat Genet. 2003 Nov;35(3):277-86 PMID: 14566339
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2005-06-00
Pages
4476-87
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC1140617
Subset
IM
Grants
NIGMS NIH HHS · R01 GM071268 · United States
NIGMS NIH HHS · GM071268 · United States
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