Oral Presentation 45th Lorne Genome Conference 2024

The apparent loss of PRC2 chromatin occupancy as an artefact of RNA depletion (#19)

Evan Healy 1 , Qi Zhang 1 , Emma H Gail 1 , Samuel C Agius 1 , Guizhi Sun 2 , Michael Bullen 3 , Varun Pandey 3 , Partha P Das 2 3 , Jose M Polo 2 3 , Chen Davidovich 1 4
  1. Department of Biochemistry and Molecular Biology, Biomedicine Discovery Institute, Faculty of Medicine, Nursing and Health Sciences, Monash University, Clayton, VIC, Australia
  2. Development and Stem Cells Program, Monash Biomedicine Discovery Institute, Wellington Road, Clayton, VIC, Australia
  3. Department of Anatomy and Developmental Biology, Monash University, Wellington Road, Clayton, VIC, Australia
  4. EMBL-Australia, Clayton, VIC, Australia

The histone methyltransferase Polycomb repressive complex 2 (PRC2) interacts with RNAs, but there is ongoing debate as to the functional consequences of this interaction. RNase A treatment during chromatin immunoprecipitation (rChIP) reduces chromatin occupancy of PRC2, with this data supporting a model whereby RNA ‘bridges’ PRC2 to chromatin [1]. A separation-of-function PRC2 mutant, defective in RNA binding but active in methyltransferase, was defective in H3K27me3 deposition in cells, which further supported a function for the RNA binding activity of PRC2 [1].

Here we show that RNase A treatment during chromatin immunoprecipitation leads to the apparent loss of all facultative heterochromatin, including PRC2 and its H3K27me3 mark genome-wide [2]. We track this artificial displacement of PRC2 to a gain of DNA from non-targeted chromatin following RNA degradation. This DNA is then sequenced at the expense of specific DNA, thereby reducing specific ChIP-seq signals. Furthermore, part of the RNA-binding surface in a previously studied PRC2 mutant [1] is required for chromatin modification, yet this activity is independent of RNA. Instead, a portion of the RNA-binding surface is required for chromatin modification through interactions with nucleosomal DNA. Conversely, another RNA-binding defective mutant [3] exhibited normal chromatin modification activity in cells. Collectively, we uncover a critical role for RNA in maintaining the solubility of chromatin while also showing that part of the RNA-binding surface of PRC2, rather than its RNA-binding activity, is required for the methylation of chromatin in vitro and in cells. 

References

  1. Long et al. "RNA is essential for PRC2 chromatin occupancy and function in human pluripotent stem cellsNat Genet2020.
  2. Healy, E. et al.The apparent loss of PRC2 chromatin occupancy as an artefact of RNA depletion”. BioRxiv 2023.
  3. Zhang et al. “RNA exploits an exposed regulatory site to inhibit the enzymatic activity of PRC2” 2019.