DNA damage signalling targets the kinetochore to promote chromatin mobility (original) (raw)

References

  1. Marshall, W. F. et al. Interphase chromosomes undergo constrained diffusional motion in living cells. Curr. Biol. 7, 930–939 (1997).
    CAS PubMed Google Scholar
  2. Chubb, J. R., Boyle, S., Perry, P. & Bickmore, W. A. Chromatin motion is constrained by association with nuclear compartments in human cells. Curr. Biol. 12, 439–445 (2002).
    CAS PubMed Google Scholar
  3. Vazquez, J., Belmont, A. S. & Sedat, J. W. Multiple regimes of constrained chromosome motion are regulated in the interphase Drosophila nucleus. Curr. Biol. 11, 1227–1239 (2001).
    CAS PubMed Google Scholar
  4. Heun, P., Laroche, T., Shimada, K., Furrer, P. & Gasser, S. M. Chromosome dynamics in the yeast interphase nucleus. Science 294, 2181–2186 (2001).
    CAS PubMed Google Scholar
  5. Seeber, A., Dion, V. & Gasser, S. M. Checkpoint kinases and the INO80 nucleosome remodeling complex enhance global chromatin mobility in response to DNA damage. Genes Dev. 27, 1999–2008 (2013).
    CAS PubMed PubMed Central Google Scholar
  6. Chung, D. K. et al. Perinuclear tethers license telomeric DSBs for a broad kinesin- and NPC-dependent DNA repair process. Nat. Commun. 6, 7742 (2015).
    CAS PubMed Google Scholar
  7. Dion, V. & Gasser, S. M. Chromatin movement in the maintenance of genome stability. Cell 152, 1355–1364 (2013).
    CAS PubMed Google Scholar
  8. Krawczyk, P. M. et al. Chromatin mobility is increased at sites of DNA double-strand breaks. J. Cell Sci. 125, 2127–2133 (2012).
    CAS PubMed Google Scholar
  9. Lottersberger, F., Karssemeijer, R. A., Dimitrova, N. & de Lange, T. 53BP1 and the LINC complex promote microtubule-dependent DSB mobility and DNA repair. Cell 163, 880–893 (2015).
    CAS PubMed PubMed Central Google Scholar
  10. Dimitrova, N., Chen, Y. C., Spector, D. L. & de Lange, T. 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature 456, 524–528 (2008).
    CAS PubMed PubMed Central Google Scholar
  11. Cho, N. W., Dilley, R. L., Lampson, M. A. & Greenberg, R. A. Interchromosomal homology searches drive directional ALT telomere movement and synapsis. Cell 159, 108–121 (2014).
    CAS PubMed PubMed Central Google Scholar
  12. Kruhlak, M. J. et al. Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J. Cell Biol. 172, 823–834 (2006).
    CAS PubMed PubMed Central Google Scholar
  13. Soutoglou, E. et al. Positional stability of single double-strand breaks in mammalian cells. Nat. Cell Biol. 9, 675–682 (2007).
    CAS PubMed PubMed Central Google Scholar
  14. Roukos, V. et al. Spatial dynamics of chromosome translocations in living cells. Science 341, 660–664 (2013).
    CAS PubMed PubMed Central Google Scholar
  15. Dion, V., Kalck, V., Horigome, C., Towbin, B. D. & Gasser, S. M. Increased mobility of double-strand breaks requires Mec1, Rad9 and the homologous recombination machinery. Nat. Cell Biol. 14, 502–509 (2012).
    CAS PubMed Google Scholar
  16. Mine-Hattab, J. & Rothstein, R. Increased chromosome mobility facilitates homology search during recombination. Nat. Cell Biol. 14, 510–517 (2012).
    CAS PubMed Google Scholar
  17. Aylon, Y. & Kupiec, M. DSB repair: the yeast paradigm. DNA Repair 3, 797–815 (2004).
    CAS PubMed Google Scholar
  18. Renkawitz, J., Lademann, C. A. & Jentsch, S. Mechanisms and principles of homology search during recombination. Nat. Rev. Mol. Cell Biol. 15, 369–383 (2014).
    CAS PubMed Google Scholar
  19. Horigome, C. et al. SWR1 and INO80 chromatin remodelers contribute to DNA double-strand break perinuclear anchorage site choice. Mol. Cell 55, 626–639 (2014).
    CAS PubMed Google Scholar
  20. Gasser, S. M. Visualizing chromatin dynamics in interphase nuclei. Science 296, 1412–1416 (2002).
    CAS PubMed Google Scholar
  21. Verdaasdonk, J. S. et al. Centromere tethering confines chromosome domains. Mol. Cell 52, 819–831 (2013).
    CAS PubMed Google Scholar
  22. Hediger, F., Neumann, F. R., Van Houwe, G., Dubrana, K. & Gasser, S. M. Live imaging of telomeres: yKu and Sir proteins define redundant telomere-anchoring pathways in yeast. Curr. Biol. 12, 2076–2089 (2002).
    CAS PubMed Google Scholar
  23. Gartenberg, M. R., Neumann, F. R., Laroche, T., Blaszczyk, M. & Gasser, S. M. Sir-mediated repression can occur independently of chromosomal and subnuclear contexts. Cell 119, 955–967 (2004).
    CAS PubMed Google Scholar
  24. Hill, A. & Bloom, K. Genetic manipulation of centromere function. Mol. Cell. Biol. 7, 2397–2405 (1987).
    CAS PubMed PubMed Central Google Scholar
  25. Smolka, M. B., Albuquerque, C. P., Chen, S. H. & Zhou, H. Proteome-wide identification of in vivo targets of DNA damage checkpoint kinases. Proc. Natl Acad. Sci. USA 104, 10364–10369 (2007).
    CAS PubMed PubMed Central Google Scholar
  26. Chen, S. H., Albuquerque, C. P., Liang, J., Suhandynata, R. T. & Zhou, H. A proteome-wide analysis of kinase-substrate network in the DNA damage response. J. Biol. Chem. 285, 12803–12812 (2010).
    CAS PubMed PubMed Central Google Scholar
  27. Lisby, M., Rothstein, R. & Mortensen, U. H. Rad52 forms DNA repair and recombination centers during S phase. Proc. Natl Acad. Sci. USA 98, 8276–8282 (2001).
    CAS PubMed PubMed Central Google Scholar
  28. Lisby, M., Mortensen, U. H. & Rothstein, R. Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat. Cell Biol. 5, 572–577 (2003).
    CAS PubMed Google Scholar
  29. Lechner, J. & Carbon, J. A 240 kd multisubunit protein complex, CBF3, is a major component of the budding yeast centromere. Cell 64, 717–725 (1991).
    CAS PubMed Google Scholar
  30. Lechner, J. A zinc finger protein, essential for chromosome segregation, constitutes a putative DNA binding subunit of the Saccharomyces cerevisiae kinetochore complex, Cbf3. EMBO J. 13, 5203–5211 (1994).
    CAS PubMed PubMed Central Google Scholar
  31. Purvis, A. & Singleton, M. R. Insights into kinetochore–DNA interactions from the structure of Cep3Delta. EMBO Rep. 9, 56–62 (2008).
    CAS PubMed Google Scholar
  32. Pinsky, B. A., Kung, C., Shokat, K. M. & Biggins, S. The Ipl1-Aurora protein kinase activates the spindle checkpoint by creating unattached kinetochores. Nat. Cell Biol. 8, 78–83 (2006).
    CAS PubMed Google Scholar
  33. Dorn, J. F. et al. Yeast kinetochore microtubule dynamics analyzed by high-resolution three-dimensional microscopy. Biophys. J. 89, 2835–2854 (2005).
    CAS PubMed PubMed Central Google Scholar
  34. Jeggo, P. A. & Downs, J. A. Roles of chromatin remodellers in DNA double strand break repair. Exp. Cell Res. 329, 69–77 (2014).
    CAS PubMed Google Scholar
  35. Agmon, N., Liefshitz, B., Zimmer, C., Fabre, E. & Kupiec, M. Effect of nuclear architecture on the efficiency of double-strand break repair. Nat. Cell Biol. 15, 694–699 (2013).
    CAS PubMed Google Scholar
  36. Rieder, C. L., Cole, R. W., Khodjakov, A. & Sluder, G. The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores. J. Cell Biol. 130, 941–948 (1995).
    CAS PubMed Google Scholar
  37. Sanchez, Y. et al. Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. Science 286, 1166–1171 (1999).
    CAS PubMed Google Scholar
  38. Wang, H., Liu, D., Wang, Y., Qin, J. & Elledge, S. J. Pds1 phosphorylation in response to DNA damage is essential for its DNA damage checkpoint function. Genes Dev. 15, 1361–1372 (2001).
    CAS PubMed PubMed Central Google Scholar
  39. Dotiwala, F., Harrison, J. C., Jain, S., Sugawara, N. & Haber, J. E. Mad2 prolongs DNA damage checkpoint arrest caused by a double-strand break via a centromere-dependent mechanism. Curr. Biol. 20, 328–332 (2010).
    CAS PubMed Google Scholar
  40. Musacchio, A. & Salmon, E. D. The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 8, 379–393 (2007).
    CAS PubMed Google Scholar
  41. Yuen, K. W. et al. Systematic genome instability screens in yeast and their potential relevance to cancer. Proc. Natl Acad. Sci. USA 104, 3925–3930 (2007).
    CAS PubMed PubMed Central Google Scholar
  42. Warren, C. D. et al. S-phase checkpoint genes safeguard high-fidelity sister chromatid cohesion. Mol. Biol. Cell 15, 1724–1735 (2004).
    CAS PubMed PubMed Central Google Scholar
  43. Renkawitz, J., Lademann, C. A., Kalocsay, M. & Jentsch, S. Monitoring homology search during DNA double-strand break repair in vivo. Mol. Cell 50, 261–272 (2013).
    CAS PubMed Google Scholar
  44. Neumann, F. R. et al. Targeted INO80 enhances subnuclear chromatin movement and ectopic homologous recombination. Genes Dev. 26, 369–383 (2012).
    CAS PubMed PubMed Central Google Scholar
  45. Chambers, A. L. et al. The INO80 chromatin remodeling complex prevents polyploidy and maintains normal chromatin structure at centromeres. Genes Dev. 26, 2590–2603 (2012).
    CAS PubMed PubMed Central Google Scholar
  46. Lee, C.-S. et al. Chromosome position determines the success of double-strand break repair. Proc. Natl Acad. Sci. USA 113, E146–E154 (2015).
    PubMed PubMed Central Google Scholar
  47. Dick, A. E. & Gerlich, D. W. Kinetic framework of spindle assembly checkpoint signalling. Nat. Cell Biol. 15, 1370–1377 (2013).
    CAS PubMed PubMed Central Google Scholar
  48. Collin, P., Nashchekina, O., Walker, R. & Pines, J. The spindle assembly checkpoint works like a rheostat rather than a toggle switch. Nat. Cell Biol. 15, 1378–1385 (2013).
    CAS PubMed Google Scholar
  49. Rohner, S., Gasser, S. M. & Meister, P. Modules for cloning-free chromatin tagging in Saccharomyces cerevisae. Yeast 25, 235–239 (2008).
    CAS PubMed Google Scholar
  50. Sage, D., Neumann, F. R., Hediger, F., Gasser, S. M. & Unser, M. Automatic tracking of individual fluorescence particles: application to the study of chromosome dynamics. IEEE Trans. Image Process. 14, 1372–1383 (2005).
    PubMed Google Scholar
  51. Wybenga-Groot, L. E. et al. Structural basis of Rad53 kinase activation by dimerization and activation segment exchange. Cell Signal. 26, 1825–1836 (2014).
    CAS PubMed Google Scholar

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