Histone H4 lysine 20 mono-methylation directly facilitates chromatin openness and promotes transcription of housekeeping genes

Muhammad Shoaib, Qinming Chen, Xiangyan Shi, Nidhi Nair, Chinmayi Prasanna, Renliang Yang, David Walter, Klaus S. Frederiksen, Hjorleifur Einarsson, J. Peter Svensson, Chuan Fa Liu, Karl Ekwall, Mads Lerdrup (), Lars Nordenskiöld () and Claus S. Sørensen ()
Additional contact information
Muhammad Shoaib: University of Copenhagen
Qinming Chen: Nanyang Technological University
Xiangyan Shi: Nanyang Technological University
Nidhi Nair: University of Copenhagen
Chinmayi Prasanna: Nanyang Technological University
Renliang Yang: Nanyang Technological University
David Walter: University of Copenhagen
Klaus S. Frederiksen: Global Drug Discovery, Novo Nordisk A/S
Hjorleifur Einarsson: University of Copenhagen
J. Peter Svensson: Karolinska Institute
Chuan Fa Liu: Nanyang Technological University
Karl Ekwall: Karolinska Institute
Mads Lerdrup: University of Copenhagen
Lars Nordenskiöld: Nanyang Technological University
Claus S. Sørensen: University of Copenhagen

Nature Communications, 2021, vol. 12, issue 1, 1-16

Abstract: Abstract Histone lysine methylations have primarily been linked to selective recruitment of reader or effector proteins that subsequently modify chromatin regions and mediate genome functions. Here, we describe a divergent role for histone H4 lysine 20 mono-methylation (H4K20me1) and demonstrate that it directly facilitates chromatin openness and accessibility by disrupting chromatin folding. Thus, accumulation of H4K20me1 demarcates highly accessible chromatin at genes, and this is maintained throughout the cell cycle. In vitro, H4K20me1-containing nucleosomal arrays with nucleosome repeat lengths (NRL) of 187 and 197 are less compact than unmethylated (H4K20me0) or trimethylated (H4K20me3) arrays. Concordantly, and in contrast to trimethylated and unmethylated tails, solid-state NMR data shows that H4K20 mono-methylation changes the H4 conformational state and leads to more dynamic histone H4-tails. Notably, the increased chromatin accessibility mediated by H4K20me1 facilitates gene expression, particularly of housekeeping genes. Altogether, we show how the methylation state of a single histone H4 residue operates as a focal point in chromatin structure control. While H4K20me1 directly promotes chromatin openness at highly transcribed genes, it also serves as a stepping-stone for H4K20me3-dependent chromatin compaction.

Date: 2021
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DOI: 10.1038/s41467-021-25051-2

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