Cell Chemical Biology
Volume 26, Issue 10, 17 October 2019, Pages 1436-1449.e5
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Article
Neutralization of the Positive Charges on Histone Tails by RNA Promotes an Open Chromatin Structure

https://doi.org/10.1016/j.chembiol.2019.08.002Get rights and content
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Highlights

  • RNA regulates opening and closure of chromatin via charge

  • RNA neutralizes histone tails and attenuates electrostatic compaction of chromatin

  • Histones precipitate following removal of single-stranded RNA

  • RNA facilitates formation of nucleosomes in vitro

Summary

RNA associates extensively with chromatin and can influence its structure; however, the potential role of the negative charges of RNA on chromatin structure remains unknown. Here, we demonstrate that RNA prevents precipitation of histones and can attenuate electrostatic interactions between histones and DNA, thereby loosening up the chromatin structure. This effect is independent of the sequence of RNA but dependent on its single-stranded nature, length, concentration, and negative charge. Opening and closure of chromatin by RNA occurs rapidly (within minutes) and passively (in permeabilized cells), in agreement with electrostatics. Accordingly, chromatin compaction following removal of RNA can be prevented by high ionic strength or neutralization of the positively charged histone tails by hyperacetylation. Finally, LINE1 repeat RNAs bind histone H2B and can decondense chromatin. We propose that RNA regulates chromatin opening and closure by neutralizing the positively charged tails of histones, reducing their electrostatic interactions with DNA.

Keywords

chromatin structure
electrostatic interactions
RNA
LINE1 repeat
neutralization
histone tails
precipitation
negative charge
charge-mechanism
chaperone

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