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PMID: 16219777 Published · ppublish English Comparative Study Journal Article

Genetic analysis of Saccharomyces cerevisiae H2A serine 129 mutant suggests a functional relationship between H2A and the sister-chromatid cohesion partners Csm3-Tof1 for the repair of topoisomerase I-induced DNA damage.

Genetics ·Vol. 172 ·No. 1 ·2006-01-00 ·Pages 67-76

Redon C, Pilch DR, Bonner WM

Abstract

Collision between a topoisomerase I-DNA intermediate and an advancing replication fork represents a unique form of replicative damage. We have shown previously that yeast H2A serine 129 is involved in the recovery from this type of damage. We now report that efficient repair also requires proteins involved in chromatid cohesion: Csm3; Tof1; Mrc1, and Dcc1. Epistasis analysis defined several pathways involving these proteins. Csm3 and Tof1 function in a same pathway and downstream of H2A. In addition, the pathway involving H2A/Csm3/Tof1 is distinct from the pathways involving the Ctf8/Ctf18/Dcc1 complex, the Rad9 pathway, and another involving Mrc1. Our genetic studies suggest a role for H2A serine 129 in the establishment of specialized cohesion structure necessary for the normal repair of topoisomerase I-induced DNA damage.

MeSH Terms
Cell Cycle Proteins/genetics,metabolism Chromatids/metabolism Chromosomal Proteins, Non-Histone/genetics,metabolism DNA Damage DNA Repair DNA Replication DNA Topoisomerases, Type I/metabolism DNA-Binding Proteins/genetics,metabolism Histones/genetics,metabolism Mutation/genetics Rad52 DNA Repair and Recombination Protein/genetics,metabolism Saccharomyces cerevisiae/genetics,metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism Serine/chemistry,genetics
Chemicals
CTF18 protein, S cerevisiae Cell Cycle Proteins Chromosomal Proteins, Non-Histone Ctf8 protein, S cerevisiae DNA-Binding Proteins Dcc1 protein, S cerevisiae Histones MRC1 protein, S cerevisiae Rad52 DNA Repair and Recombination Protein Saccharomyces cerevisiae Proteins TOF1 protein, S cerevisiae Serine DNA Topoisomerases, Type I
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Redon Christophe
NIH, NCI, DBS, Laboratory of Molecular Pharmacology, Bethesda, Maryland 20892, USA.
Pilch Duane R
Bonner William M
References (45)
45 references, click to expand
  1. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage.
    Curr Biol. 2000 Jul 27-Aug 10;10(15):886-95 PMID: 10959836
  2. Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break.
    Curr Biol. 2004 Oct 5;14(19):1703-11 PMID: 15458641
  3. ATM and ATR: networking cellular responses to DNA damage.
    Curr Opin Genet Dev. 2001 Feb;11(1):71-7 PMID: 11163154
  4. Tof1p regulates DNA damage responses during S phase in Saccharomyces cerevisiae.
    Genetics. 2001 Feb;157(2):567-77 PMID: 11156979
  5. Saccharomyces cerevisiae CTF18 and CTF4 are required for sister chromatid cohesion.
    Mol Cell Biol. 2001 May;21(9):3144-58 PMID: 11287619
  6. A comprehensive two-hybrid analysis to explore the yeast protein interactome.
    Proc Natl Acad Sci U S A. 2001 Apr 10;98(8):4569-74 PMID: 11283351
  7. Identification of RFC(Ctf18p, Ctf8p, Dcc1p): an alternative RFC complex required for sister chromatid cohesion in S. cerevisiae.
    Mol Cell. 2001 May;7(5):959-70 PMID: 11389843
  8. Rad52 forms DNA repair and recombination centers during S phase.
    Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8276-82 PMID: 11459964
  9. Chl12 (Ctf18) forms a novel replication factor C-related complex and functions redundantly with Rad24 in the DNA replication checkpoint pathway.
    Mol Cell Biol. 2001 Sep;21(17):5838-45 PMID: 11486023
  10. Arrest of replication forks by drug-stabilized topoisomerase I-DNA cleavable complexes as a mechanism of cell killing by camptothecin.
    Cancer Res. 1989 Sep 15;49(18):5077-82 PMID: 2548710
  11. New technique for uncoupling the cleavage and religation reactions of eukaryotic topoisomerase I. The mode of action of camptothecin at a specific recognition site.
    J Mol Biol. 1991 Dec 5;222(3):669-78 PMID: 1660929
  12. A novel mutation avoidance mechanism dependent on S. cerevisiae RAD27 is distinct from DNA mismatch repair.
    Cell. 1997 Jan 24;88(2):253-63 PMID: 9008166
  13. Holliday junctions accumulate in replication mutants via a RecA homolog-independent mechanism.
    Cell. 1997 Jul 11;90(1):87-96 PMID: 9230305
  14. RAD9 and RAD24 define two additive, interacting branches of the DNA damage checkpoint pathway in budding yeast normally required for Rad53 modification and activation.
    EMBO J. 1998 May 1;17(9):2687-98 PMID: 9564050
  15. A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools.
    Mol Cell. 1998 Sep;2(3):329-40 PMID: 9774971
  16. Homologous recombination is required for the viability of rad27 mutants.
    Nucleic Acids Res. 1998 Dec 15;26(24):5589-95 PMID: 9837987
  17. Megabase chromatin domains involved in DNA double-strand breaks in vivo.
    J Cell Biol. 1999 Sep 6;146(5):905-16 PMID: 10477747
  18. A requirement for recombinational repair in Saccharomyces cerevisiae is caused by DNA replication defects of mec1 mutants.
    Genetics. 1999 Oct;153(2):595-605 PMID: 10511542
  19. Saccharomyces cerevisiae pol30 (proliferating cell nuclear antigen) mutations impair replication fidelity and mismatch repair.
    Mol Cell Biol. 1999 Nov;19(11):7801-15 PMID: 10523669
  20. DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain.
    Mol Cell. 2004 Dec 22;16(6):991-1002 PMID: 15610741
  21. Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair.
    Mol Cell. 2004 Dec 22;16(6):1003-15 PMID: 15610742
  22. Control of sister chromatid recombination by histone H2AX.
    Mol Cell. 2004 Dec 22;16(6):1017-25 PMID: 15610743
  23. Saccharomyces cerevisiae histone H2A Ser122 facilitates DNA repair.
    Genetics. 2005 Jun;170(2):543-53 PMID: 15781691
  24. Mrc1 transduces signals of DNA replication stress to activate Rad53.
    Nat Cell Biol. 2001 Nov;3(11):958-65 PMID: 11715016
  25. Mrc1 channels the DNA replication arrest signal to checkpoint kinase Cds1.
    Nat Cell Biol. 2001 Nov;3(11):966-72 PMID: 11715017
  26. DNA topoisomerases: structure, function, and mechanism.
    Annu Rev Biochem. 2001;70:369-413 PMID: 11395412
  27. Genomic instability in mice lacking histone H2AX.
    Science. 2002 May 3;296(5569):922-7 PMID: 11934988
  28. Quantitative detection of (125)IdU-induced DNA double-strand breaks with gamma-H2AX antibody.
    Radiat Res. 2002 Oct;158(4):486-92 PMID: 12236816
  29. Yeast Tdp1 and Rad1-Rad10 function as redundant pathways for repairing Top1 replicative damage.
    Proc Natl Acad Sci U S A. 2002 Oct 15;99(21):13669-74 PMID: 12368472
  30. Multiple roles for Saccharomyces cerevisiae histone H2A in telomere position effect, Spt phenotypes and double-strand-break repair.
    Genetics. 2003 May;164(1):47-64 PMID: 12750320
  31. Yeast histone 2A serine 129 is essential for the efficient repair of checkpoint-blind DNA damage.
    EMBO Rep. 2003 Jul;4(7):678-84 PMID: 12792653
  32. Chromosome cohesion is regulated by a clock gene paralogue TIM-1.
    Nature. 2003 Jun 26;423(6943):1002-9 PMID: 12827206
  33. Mrc1 is a replication fork component whose phosphorylation in response to DNA replication stress activates Rad53.
    Genes Dev. 2003 Jul 15;17(14):1755-67 PMID: 12865299
  34. Tipin, a novel timeless-interacting protein, is developmentally co-expressed with timeless and disrupts its self-association.
    J Mol Biol. 2003 Aug 1;331(1):167-76 PMID: 12875843
  35. S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex.
    Nature. 2003 Aug 28;424(6952):1078-83 PMID: 12944972
  36. Lessons in how to hold a fork.
    Nat Struct Biol. 2003 Oct;10(10):778-9 PMID: 14513023
  37. Swi1 prevents replication fork collapse and controls checkpoint kinase Cds1.
    Mol Cell Biol. 2003 Nov;23(21):7861-74 PMID: 14560029
  38. Requirement of mammalian Timeless for circadian rhythmicity.
    Science. 2003 Oct 17;302(5644):439-42 PMID: 14564007
  39. Repair of and checkpoint response to topoisomerase I-mediated DNA damage.
    Mutat Res. 2003 Nov 27;532(1-2):173-203 PMID: 14643436
  40. Global mapping of the yeast genetic interaction network.
    Science. 2004 Feb 6;303(5659):808-13 PMID: 14764870
  41. Identification of protein complexes required for efficient sister chromatid cohesion.
    Mol Biol Cell. 2004 Apr;15(4):1736-45 PMID: 14742714
  42. Mrc1 is required for sister chromatid cohesion to aid in recombination repair of spontaneous damage.
    Mol Cell Biol. 2004 Aug;24(16):7082-90 PMID: 15282308
  43. Swi1 and Swi3 are components of a replication fork protection complex in fission yeast.
    Mol Cell Biol. 2004 Oct;24(19):8342-55 PMID: 15367656
  44. An AIF orthologue regulates apoptosis in yeast.
    J Cell Biol. 2004 Sep 27;166(7):969-74 PMID: 15381687
  45. A role for Saccharomyces cerevisiae histone H2A in DNA repair.
    Nature. 2000 Dec 21-28;408(6815):1001-4 PMID: 11140636
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
2006-01-00
Epub
2005-00-11
Pages
67-76
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1456192
Subset
IM
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