HPF1-dependent histone ADP-ribosylation triggers chromatin relaxation to promote the recruitment of repair factors at sites of DNA damage.
Journal
Nature structural & molecular biology
ISSN: 1545-9985
Titre abrégé: Nat Struct Mol Biol
Pays: United States
ID NLM: 101186374
Informations de publication
Date de publication:
05 2023
05 2023
Historique:
received:
27
08
2021
accepted:
28
03
2023
medline:
19
5
2023
pubmed:
28
4
2023
entrez:
27
4
2023
Statut:
ppublish
Résumé
Poly(ADP-ribose) polymerase 1 (PARP1) activity is regulated by its co-factor histone poly(ADP-ribosylation) factor 1 (HPF1). The complex formed by HPF1 and PARP1 catalyzes ADP-ribosylation of serine residues of proteins near DNA breaks, mainly PARP1 and histones. However, the effect of HPF1 on DNA repair regulated by PARP1 remains unclear. Here, we show that HPF1 controls prolonged histone ADP-ribosylation in the vicinity of the DNA breaks by regulating both the number and length of ADP-ribose chains. Furthermore, we demonstrate that HPF1-dependent histone ADP-ribosylation triggers the rapid unfolding of chromatin, facilitating access to DNA at sites of damage. This process promotes the assembly of both the homologous recombination and non-homologous end joining repair machineries. Altogether, our data highlight the key roles played by the PARP1/HPF1 complex in regulating ADP-ribosylation signaling as well as the conformation of damaged chromatin at early stages of the DNA damage response.
Identifiants
pubmed: 37106138
doi: 10.1038/s41594-023-00977-x
pii: 10.1038/s41594-023-00977-x
doi:
Substances chimiques
Histones
0
Chromatin
0
Poly(ADP-ribose) Polymerases
EC 2.4.2.30
Poly (ADP-Ribose) Polymerase-1
EC 2.4.2.30
DNA
9007-49-2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
678-691Subventions
Organisme : Wellcome Trust
ID : 210634
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 223107
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/R007195/1
Pays : United Kingdom
Organisme : Cancer Research UK
ID : C35050/A22284
Pays : United Kingdom
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature America, Inc.
Références
Kraus, W. L. & Hottiger, M. O. PARP-1 and gene regulation: progress and puzzles. Mol. Aspects Med. 34, 1109–1123 (2013).
pubmed: 23357755
doi: 10.1016/j.mam.2013.01.005
Chaudhuri, A. R. & Nussenzweig, A. The multifaceted roles of PARP1 in DNA repair and chromatin remodelling. Nat. Rev. Mol. Cell Biol. 18, 610–621 (2017).
doi: 10.1038/nrm.2017.53
Eustermann, S. et al. Structural basis of detection and signaling of DNA single-strand breaks by human PARP-1. Mol. Cell 60, 742–754 (2015).
pubmed: 26626479
pmcid: 4678113
doi: 10.1016/j.molcel.2015.10.032
Ali, A. A. E. et al. The zinc-finger domains of PARP1 cooperate to recognize DNA strand breaks. Nat. Struct. Mol. Biol. 19, 685–692 (2012).
pubmed: 22683995
pmcid: 4826610
doi: 10.1038/nsmb.2335
Langelier, M.-F., Planck, J. L., Roy, S. & Pascal, J. M. Structural basis for DNA damage–dependent poly(ADP-ribosyl)ation by human PARP-1. Science 336, 728–732 (2012).
pubmed: 22582261
pmcid: 3532513
doi: 10.1126/science.1216338
Leidecker, O. et al. Serine is a new target residue for endogenous ADP-ribosylation on histones. Nat. Chem. Biol. 12, 998–1000 (2016).
pubmed: 27723750
pmcid: 5113755
doi: 10.1038/nchembio.2180
Buch-Larsen, S. C. et al. Mapping physiological ADP-ribosylation using activated ion electron transfer dissociation. Cell Rep. 32, 108176 (2020).
pubmed: 32966781
pmcid: 7508052
doi: 10.1016/j.celrep.2020.108176
Gibbs-Seymour, I., Fontana, P., Rack, J. G. M. & Ahel, I. HPF1/C4orf27 Is a PARP-1-interacting protein that regulates PARP-1 ADP-ribosylation activity. Mol. Cell 62, 432–442 (2016).
pubmed: 27067600
pmcid: 4858568
doi: 10.1016/j.molcel.2016.03.008
Suskiewicz, M. J. et al. HPF1 completes the PARP active site for DNA damage-induced ADP-ribosylation. Nature 579, 598–602 (2020).
pubmed: 32028527
pmcid: 7104379
doi: 10.1038/s41586-020-2013-6
Palazzo, L. et al. Serine is the major residue for ADP-ribosylation upon DNA damage. eLife 7, e34334 (2018).
pubmed: 29480802
pmcid: 5837557
doi: 10.7554/eLife.34334
Bonfiglio, J. J. et al. Serine ADP-ribosylation depends on HPF1. Mol. Cell 65, 932–940.e6 (2017).
pubmed: 28190768
pmcid: 5344681
doi: 10.1016/j.molcel.2017.01.003
Hendriks, I. A. et al. The regulatory landscape of the human HPF1- and ARH3-dependent ADP-ribosylome. Nat. Commun. 12, 5893 (2021).
pubmed: 34625544
pmcid: 8501107
doi: 10.1038/s41467-021-26172-4
Rudolph, J., Roberts, G., Muthurajan, U. M. & Luger, K. HPF1 and nucleosomes mediate a dramatic switch in activity of PARP1 from polymerase to hydrolase. eLife 10, e65773 (2021).
pubmed: 33683197
pmcid: 8012059
doi: 10.7554/eLife.65773
Sun, F.-H. et al. HPF1 remodels the active site of PARP1 to enable the serine ADP-ribosylation of histones. Nat. Commun. 12, 1028 (2021).
pubmed: 33589610
pmcid: 7884425
doi: 10.1038/s41467-021-21302-4
Mahadevan, J. et al. Q-FADD: a mechanistic approach for modeling the accumulation of proteins at sites of DNA damage. Biophys. J. 116, 2224–2233 (2019).
pubmed: 31109734
pmcid: 6554667
doi: 10.1016/j.bpj.2019.04.032
Langelier, M.-F., Billur, R., Sverzhinsky, A., Black, B. E. & Pascal, J. M. HPF1 dynamically controls the PARP1/2 balance between initiating and elongating ADP-ribose modifications. Nat. Commun. 12, 6675 (2021).
pubmed: 34795260
pmcid: 8602370
doi: 10.1038/s41467-021-27043-8
Prokhorova, E. et al. Serine-linked PARP1 auto-modification controls PARP inhibitor response. Nat. Commun. 12, 4055 (2021).
pubmed: 34210965
pmcid: 8249464
doi: 10.1038/s41467-021-24361-9
Juhász, S. et al. The chromatin remodeler ALC1 underlies resistance to PARP inhibitor treatment. Sci. Adv. 6, eabb8626 (2020).
pubmed: 33355125
doi: 10.1126/sciadv.abb8626
Shao, Z. et al. Clinical PARP inhibitors do not abrogate PARP1 exchange at DNA damage sites in vivo. Nucleic Acids Res. 48, 9694–9709 (2020).
pubmed: 32890402
pmcid: 7515702
doi: 10.1093/nar/gkaa718
Gibson, B. A., Conrad, L. B., Huang, D. & Kraus, W. L. Generation and characterization of recombinant antibody-like ADP-ribose binding proteins. Biochemistry 56, 6305–6316 (2017).
pubmed: 29053245
doi: 10.1021/acs.biochem.7b00670
Timinszky, G. et al. A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat. Struct. Mol. Biol. 16, 923–929 (2009).
pubmed: 19680243
doi: 10.1038/nsmb.1664
Wang, Z. et al. Recognition of the iso-ADP-ribose moiety in poly(ADP-ribose) by WWE domains suggests a general mechanism for poly(ADP-ribosyl)ation-dependent ubiquitination. Genes Dev. 26, 235–240 (2012).
pubmed: 22267412
pmcid: 3278890
doi: 10.1101/gad.182618.111
Smith, R. et al. Poly(ADP-ribose)-dependent chromatin unfolding facilitates the association of DNA-binding proteins with DNA at sites of damage. Nucleic Acids Res. 47, 11250–11267 (2019).
pubmed: 31566235
pmcid: 6868358
doi: 10.1093/nar/gkz820
Sellou, H. et al. The poly(ADP-ribose)-dependent chromatin remodeler Alc1 induces local chromatin relaxation upon DNA damage. Mol. Biol. Cell 27, 3791–3799 (2016).
pubmed: 27733626
pmcid: 5170603
doi: 10.1091/mbc.E16-05-0269
Rother, M. B. et al. CHD7 and 53BP1 regulate distinct pathways for the re-ligation of DNA double-strand breaks. Nat. Commun. 11, 5775 (2020).
pubmed: 33188175
pmcid: 7666215
doi: 10.1038/s41467-020-19502-5
Smith, R., Sellou, H., Chapuis, C., Huet, S. & Timinszky, G. CHD3 and CHD4 recruitment and chromatin remodeling activity at DNA breaks is promoted by early poly(ADP-ribose)-dependent chromatin relaxation. Nucleic Acids Res. 46, 6087–6098 (2018).
pubmed: 29733391
pmcid: 6158744
doi: 10.1093/nar/gky334
Prokhorova, E. et al. Unrestrained poly-ADP-ribosylation provides insights into chromatin regulation and human disease. Mol. Cell 81, 2640–2655.e8 (2021).
pubmed: 34019811
pmcid: 8221567
doi: 10.1016/j.molcel.2021.04.028
Singh, J. K. et al. Zinc finger protein ZNF384 is an adaptor of Ku to DNA during classical non-homologous end-joining. Nat. Commun. 12, 6560 (2021).
pubmed: 34772923
pmcid: 8589989
doi: 10.1038/s41467-021-26691-0
Leung, J. W. C. et al. ZMYM3 regulates BRCA1 localization at damaged chromatin to promote DNA repair. Genes Dev. 31, 260–274 (2017).
pubmed: 28242625
pmcid: 5358723
doi: 10.1101/gad.292516.116
Moison, C. et al. Zinc finger protein E4F1 cooperates with PARP-1 and BRG1 to promote DNA double-strand break repair. Proc. Natl Acad. Sci. USA 118, e2019408118 (2021).
pubmed: 33692124
pmcid: 7980444
doi: 10.1073/pnas.2019408118
Grundy, G. J. et al. APLF promotes the assembly and activity of non-homologous end joining protein complexes. EMBO J. 32, 112–125 (2013).
pubmed: 23178593
doi: 10.1038/emboj.2012.304
Liu, C., Vyas, A., Kassab, M. A., Singh, A. K. & Yu, X. The role of poly ADP-ribosylation in the first wave of DNA damage response. Nucleic Acids Res. 45, 8129–8141 (2017).
pubmed: 28854736
pmcid: 5737498
doi: 10.1093/nar/gkx565
Kurgina, T. A. et al. Dual function of HPF1 in the modulation of PARP1 and PARP2 activities. Commun. Biol. 4, 1259 (2021).
pubmed: 34732825
pmcid: 8566583
doi: 10.1038/s42003-021-02780-0
Bonfiglio, J. J. et al. An HPF1/PARP1-based chemical biology strategy for exploring ADP-ribosylation. Cell 183, 1086–1102.e23 (2020).
pubmed: 33186521
doi: 10.1016/j.cell.2020.09.055
Barkauskaite, E., Jankevicius, G., Ladurner, A. G., Ahel, I. & Timinszky, G. The recognition and removal of cellular poly(ADP-ribose) signals. FEBS J. 280, 3491–3507 (2013).
pubmed: 23711178
doi: 10.1111/febs.12358
Murai, J. et al. Trapping of PARP1 and PARP2 by clinical PARP inhibitors. Cancer Res. 72, 5588–5599 (2012).
pubmed: 23118055
pmcid: 3528345
doi: 10.1158/0008-5472.CAN-12-2753
Poirier, G. G., de Murcia, G., Jongstra-Bilen, J., Niedergang, C. & Mandel, P. Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure. Proc. Natl Acad. Sci. USA 79, 3423–3427 (1982).
pubmed: 6808510
pmcid: 346432
doi: 10.1073/pnas.79.11.3423
Hananya, N., Daley, S. K., Bagert, J. D. & Muir, T. W. Synthesis of ADP-ribosylated histones reveals site-specific impacts on chromatin structure and function. J. Am. Chem. Soc. 143, 10847–10852 (2021).
pubmed: 34264659
doi: 10.1021/jacs.1c05429
de Murcia, G. et al. Modulation of chromatin superstructure induced by poly(ADP-ribose) synthesis and degradation. J. Biol. Chem. 261, 7011–7017 (1986).
pubmed: 3084493
doi: 10.1016/S0021-9258(19)62715-8
Luijsterburg, M. S. et al. PARP1 links CHD2-mediated chromatin expansion and H3.3 deposition to DNA repair by non-homologous end-joining. Mol. Cell 61, 547–562 (2016).
pubmed: 26895424
pmcid: 4769320
doi: 10.1016/j.molcel.2016.01.019
Bacic, L. et al. Structure and dynamics of the chromatin remodeler ALC1 bound to a PARylated nucleosome. eLife 10, e71420 (2021).
pubmed: 34486521
pmcid: 8463071
doi: 10.7554/eLife.71420
Mohapatra, J. et al. Serine ADP-ribosylation marks nucleosomes for ALC1-dependent chromatin remodeling. eLife 10, e71502 (2021).
pubmed: 34874266
pmcid: 8683085
doi: 10.7554/eLife.71502
Tulin, A. & Spradling, A. Chromatin loosening by poly(ADP)-ribose polymerase (PARP) at Drosophila puff loci. Science 299, 560–562 (2003).
pubmed: 12543974
doi: 10.1126/science.1078764
Mehrotra, P. V. et al. DNA repair factor APLF is a histone chaperone. Mol. Cell 41, 46–55 (2011).
pubmed: 21211722
pmcid: 3443741
doi: 10.1016/j.molcel.2010.12.008
Beaudouin, J., Mora-Bermúdez, F., Klee, T., Daigle, N. & Ellenberg, J. Dissecting the contribution of diffusion and interactions to the mobility of nuclear proteins. Biophys. J. 90, 1878–1894 (2006).
pubmed: 16387760
doi: 10.1529/biophysj.105.071241
Polo, S. E., Kaidi, A., Baskcomb, L., Galanty, Y. & Jackson, S. P. Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4. EMBO J. 29, 3130–3139 (2010).
pubmed: 20693977
pmcid: 2944064
doi: 10.1038/emboj.2010.188
Richardson, C., Moynahan, M. E. & Jasin, M. Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev. 12, 3831–3842 (1998).
pubmed: 9869637
pmcid: 317271
doi: 10.1101/gad.12.24.3831
Densham, R. M. et al. Human BRCA1–BARD1 ubiquitin ligase activity counteracts chromatin barriers to DNA resection. Nat. Struct. Mol. Biol. 23, 647–655 (2016).
pubmed: 27239795
pmcid: 6522385
doi: 10.1038/nsmb.3236
Britton, S., Coates, J. & Jackson, S. P. A new method for high-resolution imaging of Ku foci to decipher mechanisms of DNA double-strand break repair. J. Cell Biol. 202, 579–595 (2013).
pubmed: 23897892
pmcid: 3734090
doi: 10.1083/jcb.201303073
Czarna, A. et al. Structures of Drosophila cryptochrome and mouse cryptochrome1 provide insight into circadian function. Cell 153, 1394–1405 (2013).
pubmed: 23746849
doi: 10.1016/j.cell.2013.05.011
Gunn, A. & Stark, J. M. I-SceI-based assays to examine distinct repair outcomes of mammalian chromosomal double strand breaks. Methods Mol. Biol. 920, 379–391 (2012).
pubmed: 22941618
doi: 10.1007/978-1-61779-998-3_27
Tang, J. et al. Acetylation limits 53BP1 association with damaged chromatin to promote homologous recombination. Nat. Struct. Mol. Biol. 20, 317–325 (2013).
pubmed: 23377543
pmcid: 3594358
doi: 10.1038/nsmb.2499
Platani, M., Goldberg, I., Lamond, A. I. & Swedlow, J. R. Cajal body dynamics and association with chromatin are ATP-dependent. Nat. Cell Biol. 4, 502–508 (2002).
pubmed: 12068306
doi: 10.1038/ncb809
Wachsmuth, M. et al. High-throughput fluorescence correlation spectroscopy enables analysis of proteome dynamics in living cells. Nat. Biotechnol. 33, 384–389 (2015).
pubmed: 25774713
doi: 10.1038/nbt.3146
Haralick, R. M., Shanmugam, K. & Dinstein, I. Textural features for image classification. IEEE Trans. Syst. Man Cybern. SMC-3, 610–621 (1973).
doi: 10.1109/TSMC.1973.4309314