PARP1- and CTCF-Mediated Interactions between Active and Repressed Chromatin at the Lamina Promote Oscillating Transcription

Honglei Zhao, Emmanouil G. Sifakis, Noriyuki Sumida, Lluís Millán-Ariño, Barbara A. Scholz, J. Peter Svensson, Xingqi Chen, Anna L. Ronnegren, Carolina Diettrich Mallet de Lima, Farzaneh Shahin Varnoosfaderani, Chengxi Shi, Olga Loseva, Samer Yammine, Maria Israelsson, Li Sophie Rathje, Balázs Németi, Erik Fredlund, Thomas Helleday, Márta P. Imreh, Anita Göndör

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66 Citations (Scopus)

Abstract

Transcriptionally active and inactive chromatin domains tend to segregate into separate sub-nuclear compartments to maintain stable expression patterns. However, here we uncovered an inter-chromosomal network connecting active loci enriched in circadian genes to repressed lamina-associated domains (LADs). The interactome is regulated by PARP1 and its co-factor CTCF. They not only mediate chromatin fiber interactions but also promote the recruitment of circadian genes to the lamina. Synchronization of the circadian rhythm by serum shock induces oscillations in PARP1-CTCF interactions, which is accompanied by oscillating recruitment of circadian loci to the lamina, followed by the acquisition of repressive H3K9me2 marks and transcriptional attenuation. Furthermore, depletion of H3K9me2/3, inhibition of PARP activity by olaparib, or downregulation of PARP1 or CTCF expression counteracts both recruitment to the envelope and circadian transcription. PARP1- and CTCF-regulated contacts between circadian loci and the repressive chromatin environment at the lamina therefore mediate circadian transcriptional plasticity. Zhao et al. show that entrainment of the circadian rhythm by serum shock induces the circadian recruitment of clock-controlled genes to the repressive environment of the nuclear periphery, leading to diurnal transcriptional attenuation. PARP1 and CTCF regulate the contacts between clock-controlled genes and lamina-associated chromatin as well as oscillating transcription.

Original languageEnglish
Pages (from-to)984-997
Number of pages14
JournalMolecular Cell
Volume59
Issue number6
DOIs
Publication statusPublished - Sep 17 2015

ASJC Scopus subject areas

  • Molecular Biology
  • Cell Biology

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    Zhao, H., Sifakis, E. G., Sumida, N., Millán-Ariño, L., Scholz, B. A., Svensson, J. P., Chen, X., Ronnegren, A. L., Mallet de Lima, C. D., Varnoosfaderani, F. S., Shi, C., Loseva, O., Yammine, S., Israelsson, M., Rathje, L. S., Németi, B., Fredlund, E., Helleday, T., Imreh, M. P., & Göndör, A. (2015). PARP1- and CTCF-Mediated Interactions between Active and Repressed Chromatin at the Lamina Promote Oscillating Transcription. Molecular Cell, 59(6), 984-997. https://doi.org/10.1016/j.molcel.2015.07.019