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Somatic PMK-1/p38 signaling links environmental stress to germ cell apoptosis and heritable euploidy

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  • Najmeh Soltanmohammadi

    (University Hospital and University of Cologne
    University of Cologne)

  • Siyao Wang

    (University Hospital and University of Cologne
    University of Cologne)

  • Björn Schumacher

    (University Hospital and University of Cologne
    University of Cologne)

Abstract

Inheritance of stable and euploid genomes is a prerequisite for species maintenance. The DNA damage response in germ cells controls the integrity of heritable genomes. Whether and how somatic stress responses impact the quality control of germline genomes has remained unclear. Here, we show that PMK-1/p38-mediated stress signaling in intestinal cells is required for germ cell apoptosis amid ionizing radiation (IR)-induced or meiotic DNA double strand breaks (DSBs) in C. elegans. We demonstrate that intestinal PMK-1/p38 signaling regulates the germ cell death in response to environmental stress. The PMK-1/p38 target SYSM-1 is secreted from the intestine into the germline to trigger apoptosis of meiotic pachytene cells. Compromised PMK-1/p38 signaling in intestinal cells leads to stress-induced aneuploidy in the consequent generation. Our data suggest that somatic stress surveillance controls heritable genome integrity and euploidy.

Suggested Citation

  • Najmeh Soltanmohammadi & Siyao Wang & Björn Schumacher, 2022. "Somatic PMK-1/p38 signaling links environmental stress to germ cell apoptosis and heritable euploidy," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28225-8
    DOI: 10.1038/s41467-022-28225-8
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    References listed on IDEAS

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    1. Ataman Sendoel & Ines Kohler & Christof Fellmann & Scott W. Lowe & Michael O. Hengartner, 2010. "HIF-1 antagonizes p53-mediated apoptosis through a secreted neuronal tyrosinase," Nature, Nature, vol. 465(7298), pages 577-583, June.
    2. Ding Xue & H. Robert Horvitz, 1997. "Caenorhabditis elegans CED-9 protein is a bifunctional cell-death inhibitor," Nature, Nature, vol. 390(6657), pages 305-308, November.
    3. Maria A. Ermolaeva & Alexandra Segref & Alexander Dakhovnik & Hui-Ling Ou & Jennifer I. Schneider & Olaf Utermöhlen & Thorsten Hoppe & Björn Schumacher, 2013. "DNA damage in germ cells induces an innate immune response that triggers systemic stress resistance," Nature, Nature, vol. 501(7467), pages 416-420, September.
    4. Stephen P. Jackson & Jiri Bartek, 2009. "The DNA-damage response in human biology and disease," Nature, Nature, vol. 461(7267), pages 1071-1078, October.
    5. Shawn Ahmed & Jonathan Hodgkin, 2000. "MRT-2 checkpoint protein is required for germline immortality and telomere replication in C. elegans," Nature, Nature, vol. 403(6766), pages 159-164, January.
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