Changes in PRC1 activity during interphase modulate lineage transition in pluripotent cells

Helena G. Asenjo, María Alcazar-Fabra, Mencía Espinosa-Martínez, Lourdes Lopez-Onieva, Amador Gallardo, Emilia Dimitrova, Angelika Feldmann, Tomas Pachano, Jordi Martorell-Marugán, Pedro Carmona-Sáez, Antonio Sanchez-Pozo, Álvaro Rada-Iglesias, Robert J. Klose and David Landeira ()
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Helena G. Asenjo: Centre for Genomics and Oncological Research (GENYO)
María Alcazar-Fabra: Centre for Genomics and Oncological Research (GENYO)
Mencía Espinosa-Martínez: Centre for Genomics and Oncological Research (GENYO)
Lourdes Lopez-Onieva: Centre for Genomics and Oncological Research (GENYO)
Amador Gallardo: Centre for Genomics and Oncological Research (GENYO)
Emilia Dimitrova: University of Oxford
Angelika Feldmann: University of Oxford
Tomas Pachano: CSIC/Universidad de Cantabria
Jordi Martorell-Marugán: Centre for Genomics and Oncological Research (GENYO)
Pedro Carmona-Sáez: Centre for Genomics and Oncological Research (GENYO)
Antonio Sanchez-Pozo: Centre for Genomics and Oncological Research (GENYO)
Álvaro Rada-Iglesias: CSIC/Universidad de Cantabria
Robert J. Klose: University of Oxford
David Landeira: Centre for Genomics and Oncological Research (GENYO)

Nature Communications, 2023, vol. 14, issue 1, 1-16

Abstract: Abstract The potential of pluripotent cells to respond to developmental cues and trigger cell differentiation is enhanced during the G1 phase of the cell cycle, but the molecular mechanisms involved are poorly understood. Variations in polycomb activity during interphase progression have been hypothesized to regulate the cell-cycle-phase-dependent transcriptional activation of differentiation genes during lineage transition in pluripotent cells. Here, we show that recruitment of Polycomb Repressive Complex 1 (PRC1) and associated molecular functions, ubiquitination of H2AK119 and three-dimensional chromatin interactions, are enhanced during S and G2 phases compared to the G1 phase. In agreement with the accumulation of PRC1 at target promoters upon G1 phase exit, cells in S and G2 phases show firmer transcriptional repression of developmental regulator genes that is drastically perturbed upon genetic ablation of the PRC1 catalytic subunit RING1B. Importantly, depletion of RING1B during retinoic acid stimulation interferes with the preference of mouse embryonic stem cells (mESCs) to induce the transcriptional activation of differentiation genes in G1 phase. We propose that incremental enrolment of polycomb repressive activity during interphase progression reduces the tendency of cells to respond to developmental cues during S and G2 phases, facilitating activation of cell differentiation in the G1 phase of the pluripotent cell cycle.

Date: 2023
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DOI: 10.1038/s41467-023-35859-9

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