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Homology-directed Fanconi anemia pathway cross-link repair is dependent on DNA replication

Nature Structural & Molecular Biology volume 18, pages 500–503 (2011)Cite this article

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Abstract

Homologous recombination (also termed homology-directed repair, HDR) is a major pathway for the repair of DNA interstrand cross-links (ICLs) in mammalian cells. Cells from individuals with Fanconi anemia (FA) are characterized by extreme ICL sensitivity, but their reported defect in HDR is mild. Here we examined ICL-induced HDR using a GFP reporter and observed a profound defect in ICL-induced HDR in FA cells, but only when the reporter could replicate.

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Figure 1: ICL induction of HDR in mammalian cells.
Figure 2: ICL- and DSB-induced HDR in mouse ES cell mutants.
Figure 3: FANCA-dependent, replication-coupled ICL-induced HDR.

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References

  1. Auerbach, A.D. Mutat. Res. 668, 4–10 (2009).

    Article  CAS  Google Scholar 

  2. Wang, W. Nat. Rev. Genet. 8, 735–748 (2007).

    Article  CAS  Google Scholar 

  3. Räschle, M. et al. Cell 134, 969–980 (2008).

    Article  Google Scholar 

  4. Knipscheer, P. et al. Science 326, 1698–1701 (2009).

    Article  CAS  Google Scholar 

  5. Nakanishi, K. et al. Proc. Natl. Acad. Sci. USA 102, 1110–1115 (2005).

    Article  CAS  Google Scholar 

  6. Moynahan, M.E. & Jasin, M. Nat. Rev. Mol. Cell Biol. 11, 196–207 (2010).

    Article  CAS  Google Scholar 

  7. Pierce, A.J., Johnson, R.D., Thompson, L.H. & Jasin, M. Genes Dev. 13, 2633–2638 (1999).

    Article  CAS  Google Scholar 

  8. Faruqi, A.F., Seidman, M.M., Segal, D.J., Carroll, D. & Glazer, P.M. Mol. Cell. Biol. 16, 6820–6828 (1996).

    Article  CAS  Google Scholar 

  9. Chin, J.Y. & Glazer, P.M. Mol. Carcinog. 48, 389–399 (2009).

    Article  CAS  Google Scholar 

  10. Vasquez, K.M. Environ. Mol. Mutagen. 51, 527–539 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Brunet, E., Corgnali, M., Cannata, F., Perrouault, L. & Giovannangeli, C. Nucleic Acids Res. 34, 4546–4553 (2006).

    Article  CAS  Google Scholar 

  12. Giovannangéli, C., Thuong, N.T. & Helene, C. Nucleic Acids Res. 20, 4275–4281 (1992).

    Article  Google Scholar 

  13. Kalish, J.M., Seidman, M.M., Weeks, D.L. & Glazer, P.M. Nucleic Acids Res. 33, 3492–3502 (2005).

    Article  CAS  Google Scholar 

  14. Liu, Y., Nairn, R.S. & Vasquez, K.M. Nucleic Acids Res. 36, 4680–4688 (2008).

    Article  CAS  Google Scholar 

  15. Zhang, N., Liu, X., Li, L. & Legerski, R. DNA Repair (Amst.) 6, 1670–1678 (2007).

    Article  CAS  Google Scholar 

  16. Kraakman-van der Zwet, M. et al. Mol. Cell. Biol. 22, 669–679 (2002).

    Article  CAS  Google Scholar 

  17. Saeki, H. et al. Proc. Natl. Acad. Sci. USA 103, 8768–8773 (2006).

    Article  CAS  Google Scholar 

  18. Pierce, A.J., Hu, P., Han, M., Ellis, N. & Jasin, M. Genes Dev. 15, 3237–3242 (2001).

    Article  CAS  Google Scholar 

  19. Kass, E.M. & Jasin, M. FEBS Lett. 584, 3703–3708 (2010).

    Article  CAS  Google Scholar 

  20. Adamo, A. et al. Mol. Cell 39, 25–35 (2010).

    Article  CAS  Google Scholar 

  21. Pace, P. et al. Science 329, 219–223 (2010).

    Article  CAS  Google Scholar 

  22. Hinz, J.M. Environ. Mol. Mutagen. 51, 582–603 (2010).

    CAS  PubMed  Google Scholar 

  23. Stark, J.M., Pierce, A.J., Oh, J., Pastink, A. & Jasin, M. Mol. Cell. Biol. 24, 9305–9316 (2004).

    Article  CAS  Google Scholar 

  24. D'Andrea, A.D. & Grompe, M. Nat. Rev. Cancer 3, 23–34 (2003).

    Article  CAS  Google Scholar 

  25. Reisman, D., Yates, J. & Sugden, B. Mol. Cell. Biol. 5, 1822–1832 (1985).

    Article  CAS  Google Scholar 

  26. Guillonneau, F., Guieysse, A.L., Nocentini, S., Giovannangeli, C. & Praseuth, D. Nucleic Acids Res. 32, 1143–1153 (2004).

    Article  CAS  Google Scholar 

  27. Garcia-Higuera, I. et al. Mol. Cell 7, 249–262 (2001).

    Article  CAS  Google Scholar 

  28. Taniguchi, T. et al. Blood 100, 2414–2420 (2002).

    Article  CAS  Google Scholar 

  29. Lindner, S.E. & Sugden, B. Plasmid 58, 1–12 (2007).

    Article  CAS  Google Scholar 

  30. Havre, P.A., Gunther, E.J., Gasparro, F.P. & Glazer, P.M. Proc. Natl. Acad. Sci. USA 90, 7879–7883 (1993).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank K. Schlacher, J. LaRocque and L. Kass from the Jasin laboratory for comments on the manuscript. This work was supported by MFAG (My First AIRC Grant) 4765 from the Associazione Italiana per la Ricerca sul Cancro (M.B.), the Hecksher Foundation for Children (M.E.M.), the Byrne Fund (M.J.), and US National Institutes for Health grants P01CA94060 (M.E.M. and M.J.) and R01GM54668 (M.J.).

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Authors and Affiliations

  1. Developmental Biology Program, Memorial Sloan-Kettering Cancer Center, New York, New York, USA

    Koji Nakanishi, Erika Brunet & Maria Jasin

  2. Department of Public Health and Cell Biology, Section of Anatomy, University of Rome Tor Vergata, Rome, Italy

    Francesca Cavallo & Marco Barchi

  3. Muséum National d'Histoire Naturelle, Paris, France

    Loïc Perrouault, Carine Giovannangeli & Erika Brunet

  4. Centre National de la Recherche Scientifique UMR7196, Paris, France

    Loïc Perrouault, Carine Giovannangeli & Erika Brunet

  5. INSERM U565, Paris, France

    Loïc Perrouault, Carine Giovannangeli & Erika Brunet

  6. Department of Medicine, Memorial Sloan-Kettering Cancer Center, New York, New York, USA

    Mary Ellen Moynahan

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  1. Koji Nakanishi
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  2. Francesca Cavallo
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  8. Maria Jasin
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Contributions

K.N. designed and performed experiments, analyzed data and assisted in manuscript preparation; F.C. performed experiments and analyzed data; L.P. prepared the ICL-only substrates; C.G. supervised L.P. and assisted in manuscript preparation; M.E.M. provide supervision, analyzed data and assisted in manuscript preparation; M.B. supervised F.C. and contributed to data analysis; E.B. designed experiments and assisted in manuscript preparation; M.J. designed the experiments, supervised the project and wrote the manuscript.

Corresponding author

Correspondence to Maria Jasin.

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The authors declare no competing financial interests.

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Supplementary Methods, Supplementary Figures 1–4 and Supplementary Table 1 (PDF 756 kb)

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Nakanishi, K., Cavallo, F., Perrouault, L. et al. Homology-directed Fanconi anemia pathway cross-link repair is dependent on DNA replication. Nat Struct Mol Biol 18, 500–503 (2011). https://doi.org/10.1038/nsmb.2029

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