Home LiteratureArticle Details
PMID: 19465393 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The Walker B motif in avian FANCM is required to limit sister chromatid exchanges but is dispensable for DNA crosslink repair.

Nucleic acids research ·Vol. 37 ·No. 13 ·2009-07-00 ·Pages 4360-70

Rosado IV, Niedzwiedz W, Alpi AF, Patel KJ

Abstract

FANCM, the most highly conserved component of the Fanconi Anaemia (FA) pathway can resolve recombination intermediates and remodel synthetic replication forks. However, it is not known if these activities are relevant to how this conserved protein activates the FA pathway and promotes DNA crosslink repair. Here we use chicken DT40 cells to systematically dissect the function of the helicase and nuclease domains of FANCM. Our studies reveal that these domains contribute distinct roles in the tolerance of crosslinker, UV light and camptothecin-induced DNA damage. Although the complete helicase domain is critical for crosslink repair, a predicted inactivating mutation of the Walker B box domain has no impact on FA pathway associated functions. However, this mutation does result in elevated sister chromatid exchanges (SCE). Furthermore, our genetic dissection indicates that FANCM functions with the Blm helicase to suppress spontaneous SCE events. Overall our results lead us to reappraise the role of helicase domain associated activities of FANCM with respect to the activation of the FA pathway, crosslink repair and in the resolution of recombination intermediates.

MeSH Terms
Alleles Amino Acid Motifs Animals Avian Proteins/chemistry,genetics,metabolism Cell Line Chickens DNA Helicases/chemistry,genetics,metabolism DNA Repair Fanconi Anemia Complementation Group Proteins/chemistry,genetics,metabolism Genetic Complementation Test Phenotype Point Mutation Protein Structure, Tertiary Sister Chromatid Exchange
Chemicals
Avian Proteins Fanconi Anemia Complementation Group Proteins DNA Helicases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Rosado Ivan V
MRC Laboratory of Molecular Biology, Hills Rd, Cambridge CB20QH, UK.
Niedzwiedz Wojciech
Alpi Arno F
Patel Ketan J
References (33)
33 references, click to expand
  1. The FANCM ortholog Fml1 promotes recombination at stalled replication forks and limits crossing over during DNA double-strand break repair.
    Mol Cell. 2008 Oct 10;32(1):118-28 PMID: 18851838
  2. Bloom helicase is involved in DNA surveillance in early S phase in vertebrate cells.
    Oncogene. 2001 Mar 8;20(10):1143-51 PMID: 11313858
  3. Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins.
    Nat Rev Genet. 2007 Oct;8(10):735-48 PMID: 17768402
  4. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast.
    Cell. 2003 Nov 14;115(4):401-11 PMID: 14622595
  5. A multiprotein nuclear complex connects Fanconi anemia and Bloom syndrome.
    Mol Cell Biol. 2003 May;23(10):3417-26 PMID: 12724401
  6. The Bloom's syndrome helicase suppresses crossing over during homologous recombination.
    Nature. 2003 Dec 18;426(6968):870-4 PMID: 14685245
  7. The vertebrate Hef ortholog is a component of the Fanconi anemia tumor-suppressor pathway.
    Nat Struct Mol Biol. 2005 Sep;12(9):763-71 PMID: 16116434
  8. Phosphorylation of BLM, dissociation from topoisomerase IIIalpha, and colocalization with gamma-H2AX after topoisomerase I-induced replication damage.
    Mol Cell Biol. 2005 Oct;25(20):8925-37 PMID: 16199871
  9. UBE2T is the E2 in the Fanconi anemia pathway and undergoes negative autoregulation.
    Mol Cell. 2006 Aug;23(4):589-96 PMID: 16916645
  10. A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M.
    Nat Genet. 2005 Sep;37(9):958-63 PMID: 16116422
  11. Possible association of BLM in decreasing DNA double strand breaks during DNA replication.
    EMBO J. 2000 Jul 3;19(13):3428-35 PMID: 10880455
  12. Fanconi anemia and DNA replication repair.
    DNA Repair (Amst). 2007 Jul 1;6(7):885-90 PMID: 17481966
  13. Cell cycle-dependent chromatin loading of the Fanconi anemia core complex by FANCM/FAAP24.
    Blood. 2008 May 15;111(10):5215-22 PMID: 18174376
  14. FANCM and FAAP24 function in ATR-mediated checkpoint signaling independently of the Fanconi anemia core complex.
    Mol Cell. 2008 Nov 7;32(3):313-24 PMID: 18995830
  15. Saccharomyces cerevisiae MPH1 gene, required for homologous recombination-mediated mutation avoidance, encodes a 3' to 5' DNA helicase.
    J Biol Chem. 2005 Mar 4;280(9):7854-60 PMID: 15634678
  16. The BRIP1 helicase functions independently of BRCA1 in the Fanconi anemia pathway for DNA crosslink repair.
    Nat Genet. 2005 Sep;37(9):953-7 PMID: 16116421
  17. FANCI phosphorylation functions as a molecular switch to turn on the Fanconi anemia pathway.
    Nat Struct Mol Biol. 2008 Nov;15(11):1138-46 PMID: 18931676
  18. A major switch for the Fanconi anemia DNA damage-response pathway.
    Nat Struct Mol Biol. 2008 Nov;15(11):1128-30 PMID: 18985065
  19. Fanconi anemia protein FANCD2 promotes immunoglobulin gene conversion and DNA repair through a mechanism related to homologous recombination.
    Mol Cell Biol. 2005 Jan;25(1):34-43 PMID: 15601828
  20. Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM.
    Mol Cell. 2007 Feb 9;25(3):331-43 PMID: 17289582
  21. Remodeling of DNA replication structures by the branch point translocase FANCM.
    Proc Natl Acad Sci U S A. 2008 Oct 21;105(42):16107-12 PMID: 18843105
  22. New insights into the Fanconi anemia pathway from an isogenic FancG hamster CHO mutant.
    DNA Repair (Amst). 2005 Jan 2;4(1):11-22 PMID: 15533833
  23. Cooperation of the N-terminal Helicase and C-terminal endonuclease activities of Archaeal Hef protein in processing stalled replication forks.
    J Biol Chem. 2004 Dec 17;279(51):53175-85 PMID: 15485882
  24. Mrc1 and Srs2 are major actors in the regulation of spontaneous crossover.
    EMBO J. 2006 Jun 21;25(12):2837-46 PMID: 16724109
  25. Recql5 and Blm RecQ DNA helicases have nonredundant roles in suppressing crossovers.
    Mol Cell Biol. 2005 May;25(9):3431-42 PMID: 15831450
  26. The Fanconi anaemia gene FANCC promotes homologous recombination and error-prone DNA repair.
    Mol Cell. 2004 Aug 27;15(4):607-20 PMID: 15327776
  27. The Fanconi anemia protein FANCM can promote branch migration of Holliday junctions and replication forks.
    Mol Cell. 2008 Jan 18;29(1):141-8 PMID: 18206976
  28. Mechanism of replication-coupled DNA interstrand crosslink repair.
    Cell. 2008 Sep 19;134(6):969-80 PMID: 18805090
  29. UBE2T, the Fanconi anemia core complex, and FANCD2 are recruited independently to chromatin: a basis for the regulation of FANCD2 monoubiquitination.
    Mol Cell Biol. 2007 Dec;27(24):8421-30 PMID: 17938197
  30. Functional relation among RecQ family helicases RecQL1, RecQL5, and BLM in cell growth and sister chromatid exchange formation.
    Mol Cell Biol. 2003 May;23(10):3527-35 PMID: 12724411
  31. FAAP100 is essential for activation of the Fanconi anemia-associated DNA damage response pathway.
    EMBO J. 2007 Apr 18;26(8):2104-14 PMID: 17396147
  32. FANCM of the Fanconi anemia core complex is required for both monoubiquitination and DNA repair.
    Hum Mol Genet. 2008 Jun 1;17(11):1641-52 PMID: 18285517
  33. Yeast Mph1 helicase dissociates Rad51-made D-loops: implications for crossover control in mitotic recombination.
    Genes Dev. 2009 Jan 1;23(1):67-79 PMID: 19136626
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
1362-4962
Published
2009-07-00
Epub
2009-00-21
Pages
4360-70
Language
English
Region
England
NLM ID
0411011
PMCID
PMC2715236
Subset
IM
Grants
Medical Research Council · MC_U105178811 · United Kingdom
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]