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Genome-wide and sister chromatid-resolved profiling of protein occupancy in replicated chromatin with ChOR-seq and SCAR-seq

Nature Protocols volume 16, pages 4446–4493 (2021)Cite this article

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Abstract

Elucidating the mechanisms underlying chromatin maintenance upon genome replication is critical for the understanding of how gene expression programs and cell identity are preserved across cell divisions. Here, we describe two recently developed techniques, chromatin occupancy after replication (ChOR)-seq and sister chromatids after replication (SCAR)-seq, that profile chromatin occupancy on newly replicated DNA in mammalian cells in 5 d of bench work. Both techniques share a common strategy that includes pulse labeling of newly synthesized DNA and chromatin immunoprecipitation (ChIP), followed by purification and high-throughput sequencing. Whereas ChOR-seq quantitatively profiles the post-replicative abundance of histone modifications and chromatin-associated proteins, SCAR-seq distinguishes chromatin occupancy between nascent sister chromatids. Together, these two complementary techniques have unraveled key mechanisms controlling the inheritance of modified histones during replication and revealed locus-specific dynamics of histone modifications across the cell cycle. Here, we provide the experimental protocols and bioinformatic pipelines for these methods.

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Fig. 1: Experimental workflow of ChOR-seq and SCAR-seq.
Fig. 2: Flowchart of the ChOR-seq and SCAR-seq data processing pipelines.
Fig. 3: Representative results for ChOR-seq and SCAR-seq.

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Data availability

Published available sequencing raw and processed datasets analyzed in this work are available in GSE110354 for ChOR-seq and GSE117274 for SCAR-seq. Data analyzed in Fig. 3a,b correspond to GSM2988387, GSM2988389 and GSM2988390 from ref. 15. Data shown in Fig. 3c are GSM3290321, GSM3290334, GSM3290324, GSM3290344 and GSM3290342. Data used in Fig. 3d correspond to the average signal of all replicates described in ref. 11.

Code availability

Code used to analyze SCAR-seq data is available at https://zenodo.org/record/4719235#.YN5p0BNucdU (GitHub: https://github.com/anderssonlab/Replication_SCARseq, release v1.0.0).

References

  1. Zhou, K., Gaullier, G. & Luger, K. Nucleosome structure and dynamics are coming of age. Nat. Struct. Mol. Biol. 26, 3–13 (2019).

    Article  CAS  PubMed  Google Scholar 

  2. Martire, S. & Banaszynski, L. A. The roles of histone variants in fine-tuning chromatin organization and function. Nat. Rev. Mol. Cell Biol. 21, 522–541 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Allis, C. D. & Jenuwein, T. The molecular hallmarks of epigenetic control. Nat. Rev. Genet. 17, 487–500 (2016).

    Article  CAS  PubMed  Google Scholar 

  4. Stillman, B. Histone modifications: insights into their influence on gene expression. Cell 175, 6–9 (2018).

    Article  CAS  PubMed  Google Scholar 

  5. Annunziato, A. T. Assembling chromatin: the long and winding road. Biochim. Biophys. Acta 1819, 196–210 (2013).

    Article  PubMed  CAS  Google Scholar 

  6. Annunziato, A. T. The fork in the road: histone partitioning during DNA replication. Genes 6, 353–371 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Stewart-Morgan, K. R., Petryk, N. & Groth, A. Chromatin replication and epigenetic cell memory. Nat. Cell Biol. 22, 361–371 (2020).

    Article  CAS  PubMed  Google Scholar 

  8. Scharf, A. N., Barth, T. K. & Imhof, A. Establishment of histone modifications after chromatin assembly. Nucleic Acids Res. 37, 5032–5040 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Alabert, C. et al. Two distinct modes for propagation of histone PTMs across the cell cycle. Genes Dev. 29, 585–590 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Yu, C. et al. A mechanism for preventing asymmetric histone segregation onto replicating DNA strands. Science 361, 1386–1389 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Petryk, N. et al. MCM2 promotes symmetric inheritance of modified histones during DNA replication. Science 361, 1389–1392 (2018).

    Article  CAS  PubMed  Google Scholar 

  12. Gan, H. et al. The Mcm2-Ctf4-Polα axis facilitates parental histone H3-H4 transfer to lagging strands. Mol. Cell 72, 140–151.e3 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Li, Z. et al. DNA polymerase alpha interacts with H3-H4 and facilitates the transfer of parental histones to lagging strands. Sci. Adv. 6, eabb5820 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Alabert, C. et al. Domain model explains propagation dynamics and stability of histone H3K27 and H3K36 methylation landscapes. Cell Rep. 30, 1223–1234.e8 (2020).

    Article  CAS  PubMed  Google Scholar 

  15. Reveron-Gomez, N. et al. Accurate recycling of parental histones reproduces the histone modification landscape during DNA replication. Mol. Cell 72, 239–249.e5 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Stewart-Morgan, K. R., Reveron-Gomez, N. & Groth, A. Transcription restart establishes chromatin accessibility after DNA replication. Mol. Cell 75, 284–297.e6 (2019).

    Article  CAS  PubMed  Google Scholar 

  17. Sirbu, B. M. et al. Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev. 25, 1320–1327 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Dungrawala, H. & Cortez, D. Purification of proteins on newly synthesized DNA using iPOND. Methods Mol. Biol. 1228, 123–131 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  19. Alabert, C. et al. Nascent chromatin capture proteomics determines chromatin dynamics during DNA replication and identifies unknown fork components. Nat. Cell Biol. 16, 281–293 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Salic, A. & Mitchison, T. J. A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc. Natl Acad. Sci. USA 105, 2415–2420 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Presolski, S. I., Hong, V. P. & Finn, M. G. Copper-catalyzed azide-alkyne click chemistry for bioconjugation. Curr. Protoc. Chem. Biol. 3, 153–162 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  22. Rostovtsev, V. V., Green, L. G., Fokin, V. V. & Sharpless, K. B. A stepwise huisgen cycloaddition process: copper(I)-catalyzed regioselective “ligation” of azides and terminal alkynes. Angew. Chem. Int. Ed. Engl. 41, 2596–2599 (2002).

    Article  CAS  PubMed  Google Scholar 

  23. Tornoe, C. W., Christensen, C. & Meldal, M. Peptidotriazoles on solid phase: [1,2,3]-triazoles by regiospecific copper(i)-catalyzed 1,3-dipolar cycloadditions of terminal alkynes to azides. J. Org. Chem. 67, 3057–3064 (2002).

    Article  CAS  PubMed  Google Scholar 

  24. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Orlando, D. A. et al. Quantitative ChIP-Seq normalization reveals global modulation of the epigenome. Cell Rep. 9, 1163–1170 (2014).

    Article  CAS  PubMed  Google Scholar 

  26. Fursova, N. A. et al. Synergy between variant PRC1 complexes defines polycomb-mediated gene repression. Mol. Cell 74, 1020–1036.e8 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Tseng, Z., Wu, T., Liu, Y., Zhong, M. & Xiao, A. Using native chromatin immunoprecipitation to interrogate histone variant protein deposition in embryonic stem cells. in Cancer Genomics and Proteomics (ed. Narendra, W.) 11–22 (Springer, 2014).

  28. Brind’Amour, J. et al. An ultra-low-input native ChIP-seq protocol for genome-wide profiling of rare cell populations. Nat. Commun. 6, 6033 (2015).

    Article  PubMed  CAS  Google Scholar 

  29. O’Neill, L. P. & Turner, B. M. Immunoprecipitation of native chromatin: NChIP. Methods 31, 76–82 (2003).

    Article  PubMed  CAS  Google Scholar 

  30. Petryk, N. et al. Replication landscape of the human genome. Nat. Commun. 7, 10208 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Lieberman-Aiden, E. et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289–293 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Bonev, B. et al. Multiscale 3D genome rewiring during mouse neural development. Cell 171, 557–572 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Buratowski, S. Progression through the RNA polymerase II CTD cycle. Mol. Cell 36, 541–546 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Xu, C. & Corces, V. G. Genome-wide mapping of protein-DNA interactions on nascent chromatin. Methods Mol. Biol. 1766, 231–238 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Xu, C. & Corces, V. G. Nascent DNA methylome mapping reveals inheritance of hemimethylation at CTCF/cohesin sites. Science 359, 1166–1170 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Yu, C. et al. Strand-specific analysis shows protein binding at replication forks and PCNA unloading from lagging strands when forks stall. Mol. Cell 56, 551–563 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Kaya-Okur, H. S. et al. CUT&Tag for efficient epigenomic profiling of small samples and single cells. Nat. Commun. 10, 1930 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Kaya-Okur, H. S., Janssens, D. H., Henikoff, J. G., Ahmad, K. & Henikoff, S. Efficient low-cost chromatin profiling with CUT&Tag. Nat. Protoc. 15, 3264–3283 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Carter, B. et al. Mapping histone modifications in low cell number and single cells using antibody-guided chromatin tagmentation (ACT-seq). Nat. Commun. 10, 3747 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Harada, A. et al. A chromatin integration labelling method enables epigenomic profiling with lower input. Nat. Cell Biol. 21, 287–296 (2019).

    Article  CAS  PubMed  Google Scholar 

  41. Wang, Q. et al. CoBATCH for high-throughput single-cell epigenomic profiling. Mol. Cell 76, 206–216.e7 (2019).

    Article  CAS  PubMed  Google Scholar 

  42. Adey, A. & Shendure, J. Ultra-low-input, tagmentation-based whole-genome bisulfite sequencing. Genome Res. 22, 1139–1143 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Wang, Q. et al. Tagmentation-based whole-genome bisulfite sequencing. Nat. Protoc. 8, 2022–2032 (2013).

    Article  CAS  PubMed  Google Scholar 

  44. Xu, M., Wang, W., Chen, S. & Zhu, B. A model for mitotic inheritance of histone lysine methylation. EMBO Rep. 13, 60–67 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Sobel, R. E., Cook, R. G., Perry, C. A., Annunziato, A. T. & Allis, C. D. Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc. Natl Acad. Sci. USA 92, 1237–1241 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. 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).

    Article  CAS  PubMed  Google Scholar 

  47. Jasencakova, Z. et al. Replication stress interferes with histone recycling and predeposition marking of new histones. Mol. Cell 37, 736–743 (2010).

    Article  CAS  PubMed  Google Scholar 

  48. Parthun, M. R. Histone acetyltransferase 1: more than just an enzyme? Biochim. Biophys. Acta 1819, 256–263 (2012).

    Article  CAS  PubMed  Google Scholar 

  49. Saredi, G. et al. H4K20me0 marks post-replicative chromatin and recruits the TONSL-MMS22L DNA repair complex. Nature 534, 714–718 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Pesavento, J. J., Bullock, C. R., LeDuc, R. D., Mizzen, C. A. & Kelleher, N. L. Combinatorial modification of human histone H4 quantitated by two-dimensional liquid chromatography coupled with top down mass spectrometry. J. Biol. Chem. 283, 14927–14937 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Jasencakova, Z. & Groth, A. Restoring chromatin after replication: how new and old histone marks come together. Semin. Cell Dev. Biol. 21, 231–237 (2010).

    Article  CAS  PubMed  Google Scholar 

  53. Bar-Ziv, R., Voichek, Y. & Barkai, N. Chromatin dynamics during DNA replication. Genome Res. 26, 1245–1256 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Vasseur, P. et al. Dynamics of nucleosome positioning maturation following genomic replication. Cell Rep. 16, 2651–2665 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Fennessy, R. T. & Owen-Hughes, T. Establishment of a promoter-based chromatin architecture on recently replicated DNA can accommodate variable inter-nucleosome spacing. Nucleic Acids Res. 44, 7189–7203 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Gutiérrez, M. P., MacAlpine, H. K. & MacAlpine, D. M. Nascent chromatin occupancy profiling reveals locus- and factor-specific chromatin maturation dynamics behind the DNA replication fork. Genome Res. 29, 1123–1133 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Ramachandran, S. & Henikoff, S. Transcriptional regulators compete with nucleosomes post-replication. Cell 165, 580–592 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Julienne, H., Zoufir, A., Audit, B. & Arneodo, A. Human genome replication proceeds through four chromatin states. PLoS Comput. Biol. 9, e1003233 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  59. Grzybowski, A. T., Chen, Z. & Ruthenburg, A. J. Calibrating ChIP-Seq with nucleosomal internal standards to measure histone modification density genome wide. Mol. Cell 58, 886–899 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Minnoye, L. et al. Chromatin accessibility profiling methods. Nat. Rev. Methods Primers 1, 10 (2021).

    Article  Google Scholar 

  61. Klein, D. C. & Hainer, S. J. Genomic methods in profiling DNA accessibility and factor localization. Chromosome Res. 28, 69–85 (2020).

    Article  CAS  PubMed  Google Scholar 

  62. Uttamapinant, C. et al. Fast, cell-compatible click chemistry with copper-chelating azides for biomolecular labeling. Angew. Chem. Int. Ed. Engl. 51, 5852–5856 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Leach, T. J. et al. Histone H2A.Z is widely but nonrandomly distributed in chromosomes of Drosophila melanogaster. J. Biol. Chem. 275, 23267–23272 (2000).

    Article  CAS  PubMed  Google Scholar 

  64. Landt, S. G. et al. ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res. 22, 1813–1831 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Behringer, R., Gertsenstein, M., Nagy, K. V. & Nagy, A. Testing serum batches for mouse embryonic stem cell culture. Cold Spring Harb. Protoc. 2017, pdb.prot092411 (2017).

    Article  PubMed  Google Scholar 

  66. Green, M. R. & Sambrook, J. Molecular Cloning: A Laboratory Manual 4th edn (Cold Spring Harbor Laboratory Press, 2012).

  67. Luhur, A., Klueg, K. M., Roberts, J. & Zelhof, A. C. Thawing, culturing, and cryopreserving Drosophila cell lines. J. Vis. Exp. https://doi.org/10.3791/59459 (2019).

  68. Afgan, E. et al. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res. 46, W537–W544 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. Ying, Q. L. et al. The ground state of embryonic stem cell self-renewal. Nature 453, 519–523 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Amemiya, H. M., Kundaje, A. & Boyle, A. P. The ENCODE blacklist: identification of problematic regions of the genome. Sci. Rep. 9, 9354 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Huang, H. et al. A unique binding mode enables MCM2 to chaperone histones H3-H4 at replication forks. Nat. Struct. Mol. Biol. 22, 618–626 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We are grateful to K. Stewart-Morgan, A. Wenger, S. Graziano and V. Flury for the critical reading of the manuscript. Research in the Groth laboratory was supported by the Independent Research Fund Denmark (7016-00042B and 4092-00404), the European Research Council (CoG no. 724436) and the Lundbeck Foundation (R198-2015-269 and R165-2013-15306). Research at CPR is supported by the Novo Nordisk Foundation (NNF14CC0001). N.P. is supported by LabEx ‘Who Am I?’ #ANR-11-LABX-0071 and the Université de Paris IdEx #ANR-18-IDEX-0001 funded by the French Government through its ‘Investments for the Future’ program and by an INTEGER grant from Agence Nationale de la Recherche (ANR-19-CE12-0030-01). C.G.-A. is the recipient of a Ramón y Cajal Contract RYC2018-025485-I, and her laboratory is supported by grants PID2019-105742GA-100 from the Spanish Government and VIPPIT-2019-IV.2 from the University of Sevilla. M.D. and R.A. were supported by the Independent Research Fund Denmark (6108-00038B) and the European Research Council (StG no. 638173) awarded to R.A.

Author information

Author notes

  1. Maria Dalby

    Present address: H. Lundbeck A/S, Valby, Denmark

  2. These authors contributed equally: Nataliya Petryk, Nazaret Reverón-Gómez, Cristina González-Aguilera.

Authors and Affiliations

  1. Epigenetics and Cell Fate Centre, UMR7216 CNRS, Université de Paris, Paris, France

    Nataliya Petryk

  2. Novo Nordisk Foundation Center for Protein Research (CPR), Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark

    Nazaret Reverón-Gómez & Anja Groth

  3. Biotech Research and Innovation Centre (BRIC), Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark

    Nazaret Reverón-Gómez & Anja Groth

  4. Andalusian Centre for Molecular Biology and Regenerative Medicine (CABIMER), University of Seville–CSIC–University Pablo de Olavide, Andalusian Government, Seville, Spain

    Cristina González-Aguilera

  5. Department of Cellular Biology, University of Seville, Seville, Spain

    Cristina González-Aguilera

  6. The Bioinformatics Centre, Department of Biology, Faculty of Science, University of Copenhagen, Copenhagen, Denmark

    Maria Dalby & Robin Andersson

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Contributions

C.G.-A., N.R-G. and A.G. conceived the ChOR-seq project. C.G.-A. and N.R-G. developed the ChOR-seq method with input from N.P. and supervision from A.G. C.G.-A. and N.R-G. built the ChOR-seq analysis pipeline. N.P. and A.G. conceived the SCAR-seq project. N.P. developed the SCAR-seq method with supervision from A.G. M.D. built the SCAR-seq analysis pipeline, with support from N.P. and supervision from R.A. N.P., N.R.-G. and C.G.-A. wrote the manuscript with input from all authors.

Corresponding author

Correspondence to Anja Groth.

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Competing interests

A.G. is co-inventor on a patent covering the therapeutic targeting of Tonsoku-like protein (TONSL) for cancer therapy. A.G. is a co-founder and chief strategy officer of Ankrin Therapeutics.

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Peer review information Nature Protocols thanks Frederic Berger, Angelika Feldmann, Robert Klose, and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Key references using this protocol

Reveron-Gomez, N. et al. Mol. Cell 72, 239–249.e5 (2018): https://doi.org/10.1016/j.molcel.2018.08.010

Petryk, N. et al. Science 361, 1389–1392 (2018): https://doi.org/10.1126/science.aau0294

Stewart-Morgan, K. et al. Mol. Cell 75, 284–297.e6 (2019): https://doi.org/10.1016/j.molcel.2019.04.033

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Petryk, N., Reverón-Gómez, N., González-Aguilera, C. et al. Genome-wide and sister chromatid-resolved profiling of protein occupancy in replicated chromatin with ChOR-seq and SCAR-seq. Nat Protoc 16, 4446–4493 (2021). https://doi.org/10.1038/s41596-021-00585-3

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