H4K20me0 marks post-replicative chromatin and recruits the TONSL-MMS22L DNA repair complex

Nature

Volumn 534, Issue 7609, 2016, Pages 714-718

  Saredi, Giulia ^a   Huang, Hongda ^b   Hammond, Colin M ^a   Alabert, Constance ^a   Bekker Jensen, Simon ^c   Forne, Ignasi ^d   Reverón Gómez, Nazaret ^a   Foster, Benjamin M ^e   Mlejnkova, Lucie ^f   Bartke, Till ^e   Cejka, Petr ^f   Mailand, Niels ^c   Imhof, Axel ^d   Patel, Dinshaw J ^b   Groth, Anja ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c University of Copenhagen   (Denmark)

^d UNIVERSITY OF MUNICH   (Germany)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ARD PROTEIN; DNA; DNA BINDING PROTEIN; HISTONE H3; HISTONE H4; MMS22L PROTEIN; REGULATOR PROTEIN; TONSL PROTEIN; UNCLASSIFIED DRUG; CHAPERONE; CHROMATIN; HISTONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LYSINE; MMS22L PROTEIN, HUMAN; NUCLEAR PROTEIN; PROTEIN BINDING; TONSL PROTEIN, HUMAN;

CANCER; COMPLEXITY; CYTOLOGY; DNA; GENE; HOMOLOGY; LESION; PIGMENT; PROTEIN; RECOMBINATION;

ARTICLE; BINDING SITE; CANCER THERAPY; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL STRESS; CELL VIABILITY; CHROMATIN; DNA REPAIR; DNA REPLICATION; DNA STRUCTURE; DRUG TARGETING; GENOMIC INSTABILITY; HISTONE METHYLATION; HOMOLOGOUS RECOMBINATION; HUMAN; NUCLEOSOME; PRIORITY JOURNAL; REPLICATION FORK; CHEMISTRY; GENETICS; METABOLISM; METHYLATION; MOLECULAR MODEL; PROTEIN TERTIARY STRUCTURE;

CHROMATIN; DNA REPAIR; DNA REPLICATION; DNA-BINDING PROTEINS; GENOMIC INSTABILITY; HISTONES; HOMOLOGOUS RECOMBINATION; HUMANS; LYSINE; METHYLATION; MODELS, MOLECULAR; MOLECULAR CHAPERONES; NF-KAPPA B; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 85011377139     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature18312     Document Type: Article

References (41)

1. Duro, E. et al. Identification of the MMS22L-TONSL complex that promotes homologous recombination. Mol. Cell 40, 632-644 (2010).
2. O'Donnell, L. et al. The MMS22L-TONSL complex mediates recovery from replication stress and homologous recombination. Mol. Cell 40, 619-631 (2010).
3. O'Connell, B. C. et al. A genome-wide camptothecin sensitivity screen identifies a mammalian MMS22L-NFKBIL2 complex required for genomic stability. Mol. Cell 40, 645-657 (2010).
4. Piwko, W. et al. RNAi-based screening identifies the Mms22L-Nfkbil2 complex as a novel regulator of DNA replication in human cells. EMBO J. 29, 4210-4222 (2010).
5. Campos, E. I. et al. Analysis of the histone H3.1 interactome: a suitable chaperone for the right event. Mol. Cell 60, 697-709 (2015).
6. Groth, A. et al. Regulation of replication fork progression through histone supply and demand. Science 318, 1928-1931 (2007).
7. Huang, H. et al. A unique binding mode enables MCM2 to chaperone histones H3-H4 at replication forks. Nature Struct. Mol. Biol. 22, 618-626 (2015).
8. Richet, N. et al. Structural insight into how the human helicase subunit MCM2 may act as a histone chaperone together with ASF1 at the replication fork. Nucleic Acids Res. 43, 1905-1917 (2015).
9. Kalashnikova, A. A., Porter-Goff, M. E., Muthurajan, U. M., Luger, K. & Hansen, J. C. The role of the nucleosome acidic patch in modulating higher order chromatin structure. J. R. Soc. Interface 10, 20121022 (2013).
10. Collins, R. E. et al. The ankyrin repeats of G9a and GLP histone methyltransferases are mono- and dimethyllysine binding modules. Nature Struct. Mol. Biol. 15, 245-250 (2008).
11. Jasencakova, Z. et al. Replication stress interferes with histone recycling and predeposition marking of new histones. Mol. Cell 37, 736-743 (2010).
12. Taipale, M. et al. hMOF histone acetyltransferase is required for histone H4 lysine 16 acetylation in mammalian cells. Mol. Cell. Biol. 25, 6798-6810 (2005).
13. Rice, J. C. et al. Mitotic-specific methylation of histone H4 Lys 20 follows increased PR-Set7 expression and its localization to mitotic chromosomes. Genes Dev. 16, 2225-2230 (2002).
14. Pesavento, J. J., Yang, H. & Kelleher, N. L. & Mizzen, C. A. Certain and progressive methylation of histone H4 at lysine 20 during the cell cycle. Mol. Cell. Biol. 28, 468-486 (2008).
15. Beck, D. B., Oda, H., Shen, S. S. & Reinberg, D. PR-Set7 and H4K20me1: at the crossroads of genome integrity, cell cycle, chromosome condensation, and transcription. Genes Dev. 26, 325-337 (2012).
16. Jørgensen, S., Schotta, G. & Sørensen, C. S. Histone H4 lysine 20 methylation: key player in epigenetic regulation of genomic integrity. Nucleic Acids Res. 41, 2797-2806 (2013).
17. Loyola, A., Bonaldi, T., Roche, D., Imhof, A. & Almouzni, G. PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol. Cell 24, 309-316 (2006).
18. Alabert, C. et al. Two distinct modes for propagation of histone PTMs across the cell cycle. Genes Dev. 29, 585-590 (2015).
19. Alabert, C. et al. Nascent chromatin capture proteomics determines chromatin dynamics during DNA replication and identifies unknown fork components. Nature Cell Biol. 16, 281-293 (2014).
20. Prasanth, S. G., Méndez, J., Prasanth, K. V. & Stillman, B. Dynamics of pre-replication complex proteins during the cell division cycle. Phil. Trans. R. Soc. B 359, 7-16 (2004).
21. Takahashi, T. S., Wigley, D. B. & Walter, J. C. Pumps, paradoxes and ploughshares: mechanism of the MCM2-7 DNA helicase. Trends Biochem. Sci. 30, 437-444 (2005).
22. Seeber, A., Hauer, M. & Gasser, S. M. Nucleosome remodelers in double-strand break repair. Curr. Opin. Genet. Dev. 23, 174-184 (2013).
23. Burgess, R. J. & Zhang, Z. Histone chaperones in nucleosome assembly and human disease. Nature Struct. Mol. Biol. 20, 14-22 (2013).
24. Botuyan, M. V. et al. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127, 1361-1373 (2006).
25. Panier, S. & Boulton, S. J. Double-strand break repair: 53BP1 comes into focus. Nature Rev. Mol. Cell Biol. 15, 7-18 (2014).
26. Fox, D., III et al. Crystal structure of the BARD1 ankyrin repeat domain and its functional consequences. J. Biol. Chem. 283, 21179-21186 (2008).
27. Laufer, M. et al. Structural requirements for the BARD1 tumor suppressor in chromosomal stability and homology-directed DNA repair. J. Biol. Chem. 282, 34325-34333 (2007).
28. Ishitobi, M. et al. Mutational analysis of BARD1 in familial breast cancer patients in Japan. Cancer Lett. 200, 1-7 (2003).
29. Iacovoni, J. S. et al. High-resolution profiling of γH2AX around DNA double strand breaks in the mammalian genome. EMBO J. 29, 1446-1457 (2010).
30. Cejka, P. & Kowalczykowski, S. C. The full-length Saccharomyces cerevisiae Sgs1 protein is a vigorous DNA helicase that preferentially unwinds holliday junctions. J. Biol. Chem. 285, 8290-8301 (2010).
31. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
32. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
33. Adams, P. D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D 58, 1948-1954 (2002).
34. Dyer, P. N. et al. Reconstitution of nucleosome core particles from recombinant histones and DNA. Methods Enzymol. 375, 23-44 (2004).
35. Bartke, T. et al. Nucleosome-interacting proteins regulated by DNA and histone methylation. Cell 143, 470-484 (2010).
36. Bodor, D. L., Valente, L. P., Mata, J. F., Black, B. E. & Jansen, L. E. Assembly in G1 phase and long-term stability are unique intrinsic features of CENP-A nucleosomes. Mol. Biol. Cell 24, 923-932 (2013).
37. Jørgensen, S. et al. The histone methyltransferase SET8 is required for S-phase progression. J. Cell Biol. 179, 1337-1345 (2007).
38. Mosbech, A., Lukas, C., Bekker-Jensen, S. & Mailand, N. The deubiquitylating enzyme USP44 counteracts the DNA double-strand break response mediated by the RNF8 and RNF168 ubiquitin ligases. J. Biol. Chem. 288, 16579-16587 (2013).
39. Nakamura, K. et al. Regulation of homologous recombination by RNF20- dependent H2B ubiquitination. Mol. Cell 41, 515-528 (2011).
40. Jakobsen, J. S. et al. Temporal mapping of CEBPA and CEBPB binding during liver regeneration reveals dynamic occupancy and specific regulatory codes for homeostatic and cell cycle gene batteries. Genome Res. 23, 592-603 (2013).
41. Aymard, F. et al. Transcriptionally active chromatin recruits homologous recombination at DNA double-strand breaks. Nature Struct. Mol. Biol. 21, 366-374 (2014).