Histone deposition promotes recombination-dependent replication at arrested forks
Autoři:
Julien Hardy aff001; Dingli Dai aff001; Anissia Ait Saada aff001; Ana Teixeira-Silva aff001; Louise Dupoiron aff001; Fatemeh Mojallali aff001; Karine Fréon aff001; Francoise Ochsenbein aff004; Brigitte Hartmann aff005; Sarah Lambert aff001
Působiště autorů:
Institut Curie, PSL Research University, UMR3348, Orsay, France
aff001; University Paris Sud, Paris-Saclay University, UMR3348, Orsay, France
aff002; CNRS, UMR3348, Orsay France
aff003; CEA, DRF, SB2SM, Laboratoire de Biologie Structurale et Radiobiologie, Gif-sur-Yvette, France
aff004; Laboratoire de Biologie et Pharmacologie Appliquée (LBPA) UMR 8113, CNRS / ENS de Cachan, Cachan cedex, France
aff005
Vyšlo v časopise:
Histone deposition promotes recombination-dependent replication at arrested forks. PLoS Genet 15(10): e32767. doi:10.1371/journal.pgen.1008441
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008441
Souhrn
Replication stress poses a serious threat to genome stability. Recombination-Dependent-Replication (RDR) promotes DNA synthesis resumption from arrested forks. Despite the identification of chromatin restoration pathways after DNA repair, crosstalk coupling RDR and chromatin assembly is largely unexplored. The fission yeast Chromatin Assembly Factor-1, CAF-1, is known to promote RDR. Here, we addressed the contribution of histone deposition to RDR. We expressed a mutated histone, H3-H113D, to genetically alter replication-dependent chromatin assembly by destabilizing (H3-H4)2 tetramer. We established that DNA synthesis-dependent histone deposition, by CAF-1 and Asf1, promotes RDR by preventing Rqh1-mediated disassembly of joint-molecules. The recombination factor Rad52 promotes CAF-1 binding to sites of recombination-dependent DNA synthesis, indicating that histone deposition occurs downstream Rad52. Histone deposition and Rqh1 activity act synergistically to promote cell resistance to camptothecin, a topoisomerase I inhibitor that induces replication stress. Moreover, histone deposition favors non conservative recombination events occurring spontaneously in the absence of Rqh1, indicating that the stabilization of joint-molecules by histone deposition also occurs independently of Rqh1 activity. These results indicate that histone deposition plays an active role in promoting RDR, a benefit counterbalanced by stabilizing at-risk joint-molecules for genome stability.
Klíčová slova:
DNA repair – DNA replication – DNA synthesis – Histones – Chromatin – Saccharomyces cerevisiae – Schizosaccharomyces pombe – Nucleosomes
Zdroje
1. Soria G, Polo SE, Almouzni G (2012) Prime, repair, restore: the active role of chromatin in the DNA damage response. Mol Cell 46: 722–734. doi: 10.1016/j.molcel.2012.06.002 22749398
2. Svikovic S, Sale JE (2017) The Effects of Replication Stress on S Phase Histone Management and Epigenetic Memory. J Mol Biol 429: 2011–2029. doi: 10.1016/j.jmb.2016.11.011 27876548
3. Dabin J, Fortuny A, Polo SE (2016) Epigenome Maintenance in Response to DNA Damage. Mol Cell 62: 712–727. doi: 10.1016/j.molcel.2016.04.006 27259203
4. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251–260. doi: 10.1038/38444 9305837
5. Smith S, Stillman B (1991) Stepwise assembly of chromatin during DNA replication in vitro. EMBO J 10: 971–980. 1849080
6. Hatakeyama A, Hartmann B, Travers A, Nogues C, Buckle M (2016) High-resolution biophysical analysis of the dynamics of nucleosome formation. Sci Rep 6: 27337. doi: 10.1038/srep27337 27263658
7. Burgess RJ, Zhang Z (2013) Histone chaperones in nucleosome assembly and human disease. Nat Struct Mol Biol 20: 14–22. doi: 10.1038/nsmb.2461 23288364
8. Moggs JG, Grandi P, Quivy JP, Jonsson ZO, Hubscher U, et al. (2000) A CAF-1-PCNA-mediated chromatin assembly pathway triggered by sensing DNA damage. Mol Cell Biol 20: 1206–1218. doi: 10.1128/mcb.20.4.1206-1218.2000 10648606
9. Shibahara K, Stillman B (1999) Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 96: 575–585. doi: 10.1016/s0092-8674(00)80661-3 10052459
10. Mattiroli F, Gu Y, Balsbaugh JL, Ahn NG, Luger K (2017) The Cac2 subunit is essential for productive histone binding and nucleosome assembly in CAF-1. Sci Rep 7: 46274. doi: 10.1038/srep46274 28418026
11. Zhang K, Gao Y, Li J, Burgess R, Han J, et al. (2016) A DNA binding winged helix domain in CAF-1 functions with PCNA to stabilize CAF-1 at replication forks. Nucleic Acids Res 44: 5083–5094. doi: 10.1093/nar/gkw106 26908650
12. Sauer PV, Timm J, Liu D, Sitbon D, Boeri-Erba E, et al. (2017) Insights into the molecular architecture and histone H3-H4 deposition mechanism of yeast Chromatin assembly factor 1. Elife 6.
13. Mattiroli F, Gu Y, Yadav T, Balsbaugh JL, Harris MR, et al. (2017) DNA-mediated association of two histone-bound complexes of yeast Chromatin Assembly Factor-1 (CAF-1) drives tetrasome assembly in the wake of DNA replication. Elife 6.
14. Liu WH, Roemer SC, Zhou Y, Shen ZJ, Dennehey BK, et al. (2016) The Cac1 subunit of histone chaperone CAF-1 organizes CAF-1-H3/H4 architecture and tetramerizes histones. Elife 5.
15. English CM, Adkins MW, Carson JJ, Churchill ME, Tyler JK (2006) Structural basis for the histone chaperone activity of Asf1. Cell 127: 495–508. doi: 10.1016/j.cell.2006.08.047 17081973
16. Han J, Zhou H, Li Z, Xu RM, Zhang Z (2007) Acetylation of lysine 56 of histone H3 catalyzed by RTT109 and regulated by ASF1 is required for replisome integrity. J Biol Chem 282: 28587–28596. doi: 10.1074/jbc.M702496200 17690098
17. Xhemalce B, Miller KM, Driscoll R, Masumoto H, Jackson SP, et al. (2007) Regulation of histone H3 lysine 56 acetylation in Schizosaccharomyces pombe. J Biol Chem 282: 15040–15047. doi: 10.1074/jbc.M701197200 17369611
18. Franco AA, Lam WM, Burgers PM, Kaufman PD (2005) Histone deposition protein Asf1 maintains DNA replisome integrity and interacts with replication factor C. Genes Dev 19: 1365–1375. doi: 10.1101/gad.1305005 15901673
19. Lambert S, Carr AM (2013) Replication stress and genome rearrangements: lessons from yeast models. Curr Opin Genet Dev 23: 132–139. doi: 10.1016/j.gde.2012.11.009 23267817
20. Alabert C, Groth A (2012) Chromatin replication and epigenome maintenance. Nat Rev Mol Cell Biol 13: 153–167. doi: 10.1038/nrm3288 22358331
21. Prado F, Maya D (2017) Regulation of Replication Fork Advance and Stability by Nucleosome Assembly. Genes (Basel) 8.
22. Mejlvang J, Feng Y, Alabert C, Neelsen KJ, Jasencakova Z, et al. (2014) New histone supply regulates replication fork speed and PCNA unloading. J Cell Biol 204: 29–43. doi: 10.1083/jcb.201305017 24379417
23. Jasencakova Z, Scharf AN, Ask K, Corpet A, Imhof A, et al. (2010) Replication stress interferes with histone recycling and predeposition marking of new histones. Mol Cell 37: 736–743. doi: 10.1016/j.molcel.2010.01.033 20227376
24. Carr AM, Lambert S (2013) Replication stress-induced genome instability: the dark side of replication maintenance by homologous recombination. J Mol Biol 425: 4733–4744. doi: 10.1016/j.jmb.2013.04.023 23643490
25. Ait Saada A, Lambert SAE, Carr AM (2018) Preserving replication fork integrity and competence via the homologous recombination pathway. DNA Repair (Amst) 71: 135–147.
26. Mimitou EP, Symington LS (2009) Nucleases and helicases take center stage in homologous recombination. Trends Biochem Sci 34: 264–272. doi: 10.1016/j.tibs.2009.01.010 19375328
27. Lambert S, Mizuno K, Blaisonneau J, Martineau S, Chanet R, et al. (2010) Homologous recombination restarts blocked replication forks at the expense of genome rearrangements by template exchange. Mol Cell 39: 346–359. doi: 10.1016/j.molcel.2010.07.015 20705238
28. Hu L, Kim TM, Son MY, Kim SA, Holland CL, et al. (2013) Two replication fork maintenance pathways fuse inverted repeats to rearrange chromosomes. Nature 501: 569–572. doi: 10.1038/nature12500 24013173
29. Adam S, Polo SE, Almouzni G (2013) Transcription recovery after DNA damage requires chromatin priming by the H3.3 histone chaperone HIRA. Cell 155: 94–106. doi: 10.1016/j.cell.2013.08.029 24074863
30. Chen CC, Carson JJ, Feser J, Tamburini B, Zabaronick S, et al. (2008) Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134: 231–243. doi: 10.1016/j.cell.2008.06.035 18662539
31. Jalan M, Oehler J, Morrow CA, Osman F, Whitby MC (2019) Factors affecting template switch recombination associated with restarted DNA replication. Elife 8.
32. Nguyen MO, Jalan M, Morrow CA, Osman F, Whitby MC (2015) Recombination occurs within minutes of replication blockage by RTS1 producing restarted forks that are prone to collapse. Elife 4: e04539. doi: 10.7554/eLife.04539 25806683
33. Iraqui I, Chekkal Y, Jmari N, Pietrobon V, Freon K, et al. (2012) Recovery of arrested replication forks by homologous recombination is error-prone. PLoS Genet 8: e1002976. doi: 10.1371/journal.pgen.1002976 23093942
34. Pietrobon V, Freon K, Hardy J, Costes A, Iraqui I, et al. (2014) The chromatin assembly factor 1 promotes Rad51-dependent template switches at replication forks by counteracting D-loop disassembly by the RecQ-type helicase Rqh1. PLoS Biol 12: e1001968. doi: 10.1371/journal.pbio.1001968 25313826
35. Tanae K, Horiuchi T, Matsuo Y, Katayama S, Kawamukai M (2012) Histone chaperone Asf1 plays an essential role in maintaining genomic stability in fission yeast. PLoS One 7: e30472. doi: 10.1371/journal.pone.0030472 22291963
36. Nakano S, Stillman B, Horvitz HR (2011) Replication-coupled chromatin assembly generates a neuronal bilateral asymmetry in C. elegans. Cell 147: 1525–1536. doi: 10.1016/j.cell.2011.11.053 22177093
37. Davey CA, Sargent DF, Luger K, Maeder AW, Richmond TJ (2002) Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution. J Mol Biol 319: 1097–1113. doi: 10.1016/S0022-2836(02)00386-8 12079350
38. Banks DD, Gloss LM (2004) Folding mechanism of the (H3-H4)2 histone tetramer of the core nucleosome. Protein Sci 13: 1304–1316. doi: 10.1110/ps.03535504 15096635
39. Ramachandran S, Vogel L, Strahl BD, Dokholyan NV (2011) Thermodynamic stability of histone H3 is a necessary but not sufficient driving force for its evolutionary conservation. PLoS Comput Biol 7: e1001042. doi: 10.1371/journal.pcbi.1001042 21253558
40. Mellone BG, Ball L, Suka N, Grunstein MR, Partridge JF, et al. (2003) Centromere silencing and function in fission yeast is governed by the amino terminus of histone H3. Curr Biol 13: 1748–1757. doi: 10.1016/j.cub.2003.09.031 14561399
41. Takayama Y, Takahashi K (2007) Differential regulation of repeated histone genes during the fission yeast cell cycle. Nucleic Acids Res 35: 3223–3237. doi: 10.1093/nar/gkm213 17452352
42. Yadav RK, Jablonowski CM, Fernandez AG, Lowe BR, Henry RA, et al. (2017) Histone H3G34R mutation causes replication stress, homologous recombination defects and genomic instability in S. pombe. Elife 6.
43. Lim KK, Ong TY, Tan YR, Yang EG, Ren B, et al. (2015) Mutation of histone H3 serine 86 disrupts GATA factor Ams2 expression and precise chromosome segregation in fission yeast. Sci Rep 5: 14064. doi: 10.1038/srep14064 26369364
44. Fleck O, Fahnoe U, Lovschal KV, Gasasira MU, Marinova IN, et al. (2017) Deoxynucleoside Salvage in Fission Yeast Allows Rescue of Ribonucleotide Reductase Deficiency but Not Spd1-Mediated Inhibition of Replication. Genes (Basel) 8.
45. Takami Y, Ono T, Fukagawa T, Shibahara K, Nakayama T (2007) Essential role of chromatin assembly factor-1-mediated rapid nucleosome assembly for DNA replication and cell division in vertebrate cells. Mol Biol Cell 18: 129–141. doi: 10.1091/mbc.E06-05-0426 17065558
46. Quivy JP, Gerard A, Cook AJ, Roche D, Almouzni G (2008) The HP1-p150/CAF-1 interaction is required for pericentric heterochromatin replication and S-phase progression in mouse cells. Nat Struct Mol Biol 15: 972–979. 19172751
47. Klapholz B, Dietrich BH, Schaffner C, Heredia F, Quivy JP, et al. (2009) CAF-1 is required for efficient replication of euchromatic DNA in Drosophila larval endocycling cells. Chromosoma 118: 235–248. doi: 10.1007/s00412-008-0192-2 19066929
48. Ray-Gallet D, Woolfe A, Vassias I, Pellentz C, Lacoste N, et al. (2011) Dynamics of histone H3 deposition in vivo reveal a nucleosome gap-filling mechanism for H3.3 to maintain chromatin integrity. Mol Cell 44: 928–941. doi: 10.1016/j.molcel.2011.12.006 22195966
49. Driscoll R, Hudson A, Jackson SP (2007) Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315: 649–652. doi: 10.1126/science.1135862 17272722
50. Doe CL, Dixon J, Osman F, Whitby MC (2000) Partial suppression of the fission yeast rqh1(-) phenotype by expression of a bacterial Holliday junction resolvase. EMBO J 19: 2751–2762. doi: 10.1093/emboj/19.11.2751 10835372
51. Hartsuiker E, Vaessen E, Carr AM, Kohli J (2001) Fission yeast Rad50 stimulates sister chromatid recombination and links cohesion with repair. EMBO J 20: 6660–6671. doi: 10.1093/emboj/20.23.6660 11726502
52. Adkins NL, Swygert SG, Kaur P, Niu H, Grigoryev SA, et al. (2017) Nucleosome-like, Single-stranded DNA (ssDNA)-Histone Octamer Complexes and the Implication for DNA Double Strand Break Repair. J Biol Chem 292: 5271–5281. doi: 10.1074/jbc.M117.776369 28202543
53. Fasching CL, Cejka P, Kowalczykowski SC, Heyer WD (2015) Top3-Rmi1 dissolve Rad51-mediated D loops by a topoisomerase-based mechanism. Mol Cell 57: 595–606. doi: 10.1016/j.molcel.2015.01.022 25699708
54. Miyabe I, Mizuno K, Keszthelyi A, Daigaku Y, Skouteri M, et al. (2015) Polymerase delta replicates both strands after homologous recombination-dependent fork restart. Nat Struct Mol Biol 22: 932–938. doi: 10.1038/nsmb.3100 26436826
55. Mizuno K, Miyabe I, Schalbetter SA, Carr AM, Murray JM (2013) Recombination-restarted replication makes inverted chromosome fusions at inverted repeats. Nature 493: 246–249. doi: 10.1038/nature11676 23178809
56. Sarkies P, Reams C, Simpson LJ, Sale JE (2010) Epigenetic instability due to defective replication of structured DNA. Mol Cell 40: 703–713. doi: 10.1016/j.molcel.2010.11.009 21145480
57. Li W, Yi J, Agbu P, Zhou Z, Kelley RL, et al. (2017) Replication stress affects the fidelity of nucleosome-mediated epigenetic inheritance. PLoS Genet 13: e1006900. doi: 10.1371/journal.pgen.1006900 28749973
58. Schiavone D, Jozwiakowski SK, Romanello M, Guilbaud G, Guilliam TA, et al. (2016) PrimPol Is Required for Replicative Tolerance of G Quadruplexes in Vertebrate Cells. Mol Cell 61: 161–169. doi: 10.1016/j.molcel.2015.10.038 26626482
59. Moreno S, Klar A, Nurse P (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194: 795–823. doi: 10.1016/0076-6879(91)94059-l 2005825
60. Kai M, Tanaka H, Wang TS (2001) Fission yeast Rad17 associates with chromatin in response to aberrant genomic structures. Mol Cell Biol 21: 3289–3301. doi: 10.1128/MCB.21.10.3289-3301.2001 11313455
61. Ait Saada A, Teixeira-Silva A, Iraqui I, Costes A, Hardy J, et al. (2017) Unprotected Replication Forks Are Converted into Mitotic Sister Chromatid Bridges. Mol Cell 66: 398–410 e394. doi: 10.1016/j.molcel.2017.04.002 28475874
62. Audry J, Maestroni L, Delagoutte E, Gauthier T, Nakamura TM, et al. (2015) RPA prevents G-rich structure formation at lagging-strand telomeres to allow maintenance of chromosome ends. EMBO J 34: 1942–1958. doi: 10.15252/embj.201490773 26041456
63. Wu PY, Nurse P (2009) Establishing the program of origin firing during S phase in fission Yeast. Cell 136: 852–864. doi: 10.1016/j.cell.2009.01.017 19269364
64. Pai CC, Deegan RS, Subramanian L, Gal C, Sarkar S, et al. (2014) A histone H3K36 chromatin switch coordinates DNA double-strand break repair pathway choice. Nat Commun 5: 4091. doi: 10.1038/ncomms5091 24909977
65. Lea DE, Coulson CA (1949) The distribution of the numbers of mutants in bacterial populations. J Genet 49: 264–285. doi: 10.1007/bf02986080 24536673
66. de Beer TA, Berka K, Thornton JM, Laskowski RA (2014) PDBsum additions. Nucleic Acids Res 42: D292–296. doi: 10.1093/nar/gkt940 24153109
Štítky
Genetika Reprodukční medicínaČlánek vyšel v časopise
PLOS Genetics
2019 Číslo 10
Nejčtenější v tomto čísle
- Spatiotemporal cytoskeleton organizations determine morphogenesis of multicellular trichomes in tomato
- Loss of thymidine kinase 1 inhibits lung cancer growth and metastatic attributes by reducing GDF15 expression
- TSEN54 missense variant in Standard Schnauzers with leukodystrophy
- Viral quasispecies