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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.

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).

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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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Related links

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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