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Dense Chromatin Activates Polycomb Repressive Complex 2 to Regulate H3 Lysine 27 Methylation

Maintaining Repression The Polycomb Repressive Complex 2 (PRC2) plays a critical role in gene silencing in metazoans, methylating histone H3 on lysine 27 (H3K27) to generate a repressive chromatin mark. The catalytic subunit E(z)/Ezh2 requires the presence of two other subunits—ESC/EED and Su(z)12—for enzyme activity. Yuan et al. (p. 971; see the Perspective by Pirrotta) show that both a fragment of the histone H3 N-terminal tail, and histone H1 stimulated PRC2 enzyme activity on poor, low-density chromatin substrates, indicating that that PRC2 is regulated by the density and compaction states of chromatin. The histone H3 fragment binds to the Su(z)12 subunit of PRC2 to stimulate E(z)/Ezh2. Local chromatin compaction preceded establishment of histone H3K27 methylation indicating how PRC2 might maintain the repressed state. The density and compaction state of chromatin directly regulates the activity of a transcription repressor protein complex. Polycomb repressive complex 2 (PRC2)–mediated histone H3 lysine 27 (H3K27) methylation is vital for Polycomb gene silencing, a classic epigenetic phenomenon that maintains transcriptional silencing throughout cell divisions. We report that PRC2 activity is regulated by the density of its substrate nucleosome arrays. Neighboring nucleosomes activate the PRC2 complex with a fragment of their H3 histones (Ala31 to Arg42). We also identified mutations on PRC2 subunit Su(z)12, which impair its binding and response to the activating peptide and its ability in establishing H3K27 trimethylation levels in vivo. In mouse embryonic stem cells, local chromatin compaction occurs before the formation of trimethylated H3K27 upon transcription cessation of the retinoic acid–regulated gene CYP26a1. We propose that PRC2 can sense the chromatin environment to exert its role in the maintenance of transcriptional states.