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AGO1 regulates major satellite transcripts and H3K9me3 distribution at pericentromeric regions in mESCs

Madlen Müller, Tara Fäh, Moritz Schäfer, Janina Luitz, Patrick Stalder, Rajika Arora, View ORCID ProfileRichard Patryk Ngondo, View ORCID ProfileConstance Ciaudo
doi: https://doi.org/10.1101/2021.07.26.453733
Madlen Müller
1Swiss Federal Institute of Technology Zurich, IMHS, Chair of RNAi and Genome Integrity, Zurich, Switzerland
2Life Science Zurich Graduate School, University of Zürich, Switzerland
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Tara Fäh
1Swiss Federal Institute of Technology Zurich, IMHS, Chair of RNAi and Genome Integrity, Zurich, Switzerland
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Moritz Schäfer
1Swiss Federal Institute of Technology Zurich, IMHS, Chair of RNAi and Genome Integrity, Zurich, Switzerland
2Life Science Zurich Graduate School, University of Zürich, Switzerland
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Janina Luitz
1Swiss Federal Institute of Technology Zurich, IMHS, Chair of RNAi and Genome Integrity, Zurich, Switzerland
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Patrick Stalder
1Swiss Federal Institute of Technology Zurich, IMHS, Chair of RNAi and Genome Integrity, Zurich, Switzerland
2Life Science Zurich Graduate School, University of Zürich, Switzerland
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Rajika Arora
1Swiss Federal Institute of Technology Zurich, IMHS, Chair of RNAi and Genome Integrity, Zurich, Switzerland
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Richard Patryk Ngondo
1Swiss Federal Institute of Technology Zurich, IMHS, Chair of RNAi and Genome Integrity, Zurich, Switzerland
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  • ORCID record for Richard Patryk Ngondo
Constance Ciaudo
1Swiss Federal Institute of Technology Zurich, IMHS, Chair of RNAi and Genome Integrity, Zurich, Switzerland
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  • ORCID record for Constance Ciaudo
  • For correspondence: cciaudo@ethz.ch
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SUMMARY

In the past years, several studies reported nuclear roles for the Argonaute (AGO) proteins associating them with transcriptional activation or repression, alternative splicing and, chromatin organization. However, as most of these experiments have been conducted in human cancer cell lines, the nuclear functions of the AGO proteins in mouse early embryonic development still remains elusive. In this study, we investigated possible nuclear functions of the AGO proteins in mouse Embryonic Stem Cells (mESCs). By biochemical assays, we observed that AGO1 and AGO2 are present in a small fraction in the nucleus and even less on chromatin in mESCs. To profile the nuclear interactome of the AGO proteins, we performed immunoprecipitation followed by Mass Spectrometry and identified three novel nuclear interactors for AGO1, namely DNMT3a, HP1α, and ATRX. These interactors are well-known proteins involved in the establishment and maintenance of heterochromatin at pericentromeric regions. Indeed, upon depletion of Ago1, we observed a specific redistribution of the heterochromatin protein HP1α and the repressive histone mark H3K9me3, away from pericentromeric regions. Furthermore, these regions are characterized by AT-rich tandem repeats known as major satellite sequences. We demonstrated that major satellite transcripts are strongly upregulated in Ago1_KO mESCs. Interestingly, this phenotype was not caused by the loss of genome integrity at pericentromeres, as these could still form normally in Ago1_KO mESCs. Lastly, we showed that specific microRNAs loaded in AGO1, regulate the expression of the major satellite transcripts. Overall, our results demonstrate for the first time a novel role for AGO1 in regulating major satellite transcripts and localization of HP1α and H3K9me3 at pericentromeres in mESCs.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted July 26, 2021.
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AGO1 regulates major satellite transcripts and H3K9me3 distribution at pericentromeric regions in mESCs
Madlen Müller, Tara Fäh, Moritz Schäfer, Janina Luitz, Patrick Stalder, Rajika Arora, Richard Patryk Ngondo, Constance Ciaudo
bioRxiv 2021.07.26.453733; doi: https://doi.org/10.1101/2021.07.26.453733
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AGO1 regulates major satellite transcripts and H3K9me3 distribution at pericentromeric regions in mESCs
Madlen Müller, Tara Fäh, Moritz Schäfer, Janina Luitz, Patrick Stalder, Rajika Arora, Richard Patryk Ngondo, Constance Ciaudo
bioRxiv 2021.07.26.453733; doi: https://doi.org/10.1101/2021.07.26.453733

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