Histone degradation in response to DNA damage enhances chromatin dynamics and recombination rates

Nature Structural and Molecular Biology

Volumn 24, Issue 2, 2017, Pages 99-107

  Hauer, Michael H ^a,b   Seeber, Andrew ^a,b   Singh, Vijender ^c   Thierry, Raphael ^a   Sack, Ragna ^a   Amitai, Assaf ^d,e   Kryzhanovska, Mariya ^a   Eglinger, Jan ^a   Holcman, David ^d   Owen Hughes, Tom ^c   Gasser, Susan M ^a,b  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

^d ECOLE NORMALE SUPÉRIEURE   (France)

^e Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; HISTONE; CHROMATIN; PROTEASOME; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CHROMATIN; DNA DAMAGE CHECKPOINT; DNA DAMAGE RESPONSE; DNA RECOMBINATION; FLUORESCENCE MICROSCOPY; MASS SPECTROMETRY; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; SACCHAROMYCES CEREVISIAE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYTOLOGY; DNA DAMAGE; DNA REPAIR; GENETIC RECOMBINATION; GENETICS; METABOLISM;

CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA DAMAGE; DNA REPAIR; HISTONES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 85008668741     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3347     Document Type: Article

References (39)

1. Boettiger, A.N. et al. Super-resolution imaging reveals distinct chromatin folding for different epigenetic states. Nature 529, 418-422 (2016).
2. Aze, A., Sannino, V., Soffientini, P., Bachi, A. &Costanzo, V. Centromeric DNA replication reconstitution reveals DNA loops and ATR checkpoint suppression. Nat. Cell Biol. 18, 684-691 (2016).
3. Gerhold, C.B., Hauer, M.H. &Gasser, S.M. INO80-C and SWR-C: guardians of the genome. J. Mol. Biol. 427, 637-651 (2015).
4. Seeber, A., Hauer, M. &Gasser, S.M. Nucleosome remodelers in double-strand break repair. Curr. Opin. Genet. Dev. 23, 174-184 (2013).
5. Soria, G., Polo, S.E. &Almouzni, G. Prime, repair, restore: the active role of chromatin in the DNA damage response. Mol. Cell 46, 722-734 (2012).
6. Chiolo, I. et al. Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 144, 732-744 (2011).
7. Lemaître, C. et al. Nuclear position dictates DNA repair pathway choice. Genes Dev. 28, 2450-2463 (2014).
8. Torres-Rosell, J. et al. The Smc5-Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat. Cell Biol. 9, 923-931 (2007).
9. 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).
10. Miné-Hattab, J. &Rothstein, R. Increased chromosome mobility facilitates homology search during recombination. Nat. Cell Biol. 14, 510-517 (2012).
11. Roukos, V. et al. Spatial dynamics of chromosome translocations in living cells. Science 341, 660-664 (2013).
12. 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).
13. Hu, B. et al. Biological chromodynamics: a general method for measuring protein occupancy across the genome by calibrating ChIP-seq. Nucleic Acids Res. 43, e132 (2015).
14. Povirk, L.F., Wübter, W., Köhnlein, W. &Hutchinson, F. DNA double-strand breaks and alkali-labile bonds produced by bleomycin. Nucleic Acids Res. 4, 3573-3580 (1977).
15. Gunjan, A. &Verreault, A. A Rad53 kinase-dependent surveillance mechanism that regulates histone protein levels in S. cerevisiae. Cell 115, 537-549 (2003).
16. Liang, D., Burkhart, S.L., Singh, R.K., Kabbaj, M.H. &Gunjan, A. Histone dosage regulates DNA damage sensitivity in a checkpoint-independent manner by the homologous recombination pathway. Nucleic Acids Res. 40, 9604-9620 (2012).
17. Heinemeyer, W., Kleinschmidt, J.A., Saidowsky, J., Escher, C. &Wolf, D.H. Proteinase yscE, the yeast proteasome/multicatalytic-multifunctional proteinase: mutants unravel its function in stress induced proteolysis and uncover its necessity for cell survival. EMBO J. 10, 555-562 (1991).
18. Dion, V. &Gasser, S.M. Chromatin movement in the maintenance of genome stability. Cell 152, 1355-1364 (2013).
19. Krawczyk, P.M. et al. Chromatin mobility is increased at sites of DNA double-strand breaks. J. Cell Sci. 125, 2127-2133 (2012).
20. Strecker, J. et al. DNA damage signalling targets the kinetochore to promote chromatin mobility. Nat. Cell Biol. 18, 281-290 (2016).
21. Celona, B. et al. Substantial histone reduction modulates genomewide nucleosomal occupancy and global transcriptional output. PLoS Biol. 9, e1001086 (2011).
22. Sanchez, Y. et al. Regulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science 271, 357-360 (1996).
23. Morrison, A.J. et al. Mec1/Tel1 phosphorylation of the INO80 chromatin remodeling complex influences DNA damage checkpoint responses. Cell 130, 499-511 (2007).
24. Poli, J. et al. Mec1, INO80, and the PAF1 complex cooperate to limit transcription replication conflicts through RNAPII removal during replication stress. Genes Dev. 30, 337-354 (2016).
25. Lafon, A. et al. INO80 chromatin remodeler facilitates release of RNA polymerase II from chromatin for ubiquitin-mediated proteasomal degradation. Mol. Cell 60, 784-796 (2015).
26. Chen, X. et al. The Fun30 nucleosome remodeller promotes resection of DNA double-strand break ends. Nature 489, 576-580 (2012).
27. van Attikum, H., Fritsch, O. &Gasser, S.M. Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J. 26, 4113-4125 (2007).
28. Lisby, M., Barlow, J.H., Burgess, R.C. &Rothstein, R. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118, 699-713 (2004).
29. Verdaasdonk, J.S. et al. Centromere tethering confines chromosome domains. Mol. Cell 52, 819-831 (2013).
30. Haase, S.B. &Lew, D.J. Flow cytometric analysis of DNA content in budding yeast. Methods Enzymol. 283, 322-332 (1997).
31. Liu, C., Apodaca, J., Davis, L.E. &Rao, H. Proteasome inhibition in wild-type yeast Saccharomyces cerevisiae cells. Biotechniques 42, 158-162 (2007).
32. Lee, D.H. &Goldberg, A.L. Selective inhibitors of the proteasome-dependent and vacuolar pathways of protein degradation in Saccharomyces cerevisiae. J. Biol. Chem. 271, 27280-27284 (1996).
33. Wiechens, N. et al. The chromatin remodelling enzymes SNF2H and SNF2L position nucleosomes adjacent to CTCF and other transcription factors. PLoS Genet. 12, e1005940 (2016).
34. Gruhler, A. et al. Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway. Mol. Cell. Proteomics 4, 310-327 (2005).
35. Pasero, P., Duncker, B.P., Schwob, E. &Gasser, S.M. A role for the Cdc7 kinase regulatory subunit Dbf4p in the formation of initiation-competent origins of replication. Genes Dev. 13, 2159-2176 (1999).
36. 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).
37. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682 (2012).
38. Dietz, C. &Berthold, M.R. KNIME for open-source bioimage analysis: a tutorial. Adv. Anat. Embryol. Cell Biol. 219, 179-197 (2016).
39. Sommer, C. &Gerlich, D.W. Machine learning in cell biology-teaching computers to recognize phenotypes. J. Cell Sci. 126, 5529-5539 (2013).