A methylation-phosphorylation switch controls EZH2 stability and hematopoiesis.

Guo, Pengfei; Lim, Rebecca C; Rajawasam, Keshari; Trinh, Tiffany; Sun, Hong; Zhang, Hui · Elife · 2024

basic_science · Level V

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Abstract

The Polycomb Repressive Complex 2 (PRC2) methylates H3K27 to regulate development and cell fate by transcriptional silencing. Alteration of PRC2 is associated with various cancers. Here, we show that mouse <i>Kdm1a</i> deletion causes a dramatic reduction of PRC2 proteins, whereas mouse null mutation of <i>L3mbtl3</i> or <i>Dcaf5</i> results in PRC2 accumulation and increased H3K27 trimethylation. The catalytic subunit of PRC2, EZH2, is methylated at lysine 20 (K20), promoting EZH2 proteolysis by L3MBTL3 and the CLR4<sup>DCAF5</sup> ubiquitin ligase. KDM1A (LSD1) demethylates the methylated K20 to stabilize EZH2. K20 methylation is inhibited by AKT-mediated phosphorylation of serine 21 in EZH2. Mouse <i>Ezh2</i><sup>K20R/K20R</sup> mutants develop hepatosplenomegaly associated with high GFI1B expression, and <i>Ezh2</i><sup>K20R/K20R</sup> mutant bone marrows expand hematopoietic stem cells and downstream hematopoietic populations. Our studies reveal that EZH2 is regulated by methylation-dependent proteolysis, which is negatively controlled by AKT-mediated S21 phosphorylation to establish a methylation-phosphorylation switch to regulate the PRC2 activity and hematopoiesis.

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