Decoding chromatin states by proteomic profiling of nucleosome readers

Saulius Lukauskas, Andrey Tvardovskiy, Nhuong V. Nguyen, Mara Stadler, Peter Faull, Tina Ravnsborg, Bihter Özdemir Aygenli, Scarlett Dornauer, Helen Flynn, Rik G. H. Lindeboom, Teresa K. Barth, Kevin Brockers, Stefanie M. Hauck, Michiel Vermeulen, Ambrosius P. Snijders, Christian L. Müller, Peter A. DiMaggio, Ole N. Jensen, Robert Schneider and Till Bartke ()
Additional contact information
Saulius Lukauskas: Helmholtz Zentrum München
Andrey Tvardovskiy: Helmholtz Zentrum München
Nhuong V. Nguyen: MRC Laboratory of Medical Sciences (LMS)
Mara Stadler: Helmholtz Zentrum München
Peter Faull: MRC Laboratory of Medical Sciences (LMS)
Tina Ravnsborg: University of Southern Denmark
Bihter Özdemir Aygenli: Helmholtz Zentrum München
Scarlett Dornauer: Helmholtz Zentrum München
Helen Flynn: The Francis Crick Institute
Rik G. H. Lindeboom: Radboud University Nijmegen
Teresa K. Barth: Helmholtz Zentrum München
Kevin Brockers: Helmholtz Zentrum München
Stefanie M. Hauck: Helmholtz Zentrum München
Michiel Vermeulen: Radboud University Nijmegen
Ambrosius P. Snijders: The Francis Crick Institute
Christian L. Müller: Helmholtz Zentrum München
Peter A. DiMaggio: Imperial College London
Ole N. Jensen: University of Southern Denmark
Robert Schneider: Helmholtz Zentrum München
Till Bartke: Helmholtz Zentrum München

Nature, 2024, vol. 627, issue 8004, 671-679

Abstract: Abstract DNA and histone modifications combine into characteristic patterns that demarcate functional regions of the genome1,2. While many ‘readers’ of individual modifications have been described3–5, how chromatin states comprising composite modification signatures, histone variants and internucleosomal linker DNA are interpreted is a major open question. Here we use a multidimensional proteomics strategy to systematically examine the interaction of around 2,000 nuclear proteins with over 80 modified dinucleosomes representing promoter, enhancer and heterochromatin states. By deconvoluting complex nucleosome-binding profiles into networks of co-regulated proteins and distinct nucleosomal features driving protein recruitment or exclusion, we show comprehensively how chromatin states are decoded by chromatin readers. We find highly distinctive binding responses to different features, many factors that recognize multiple features, and that nucleosomal modifications and linker DNA operate largely independently in regulating protein binding to chromatin. Our online resource, the Modification Atlas of Regulation by Chromatin States (MARCS), provides in-depth analysis tools to engage with our results and advance the discovery of fundamental principles of genome regulation by chromatin states.

Date: 2024
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DOI: 10.1038/s41586-024-07141-5

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