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Regulatory mechanism of cold-inducible diapause in Caenorhabditis elegans

Author

Listed:
  • Makoto Horikawa

    (Graduate School of Integrated Sciences for Life, Hiroshima University)

  • Masamitsu Fukuyama

    (Graduate School of Pharmaceutical Sciences, University of Tokyo)

  • Adam Antebi

    (Max Planck Institute for Biology of Ageing
    University of Cologne)

  • Masaki Mizunuma

    (Graduate School of Integrated Sciences for Life, Hiroshima University
    Hiroshima University)

Abstract

Temperature is a critical environmental cue that controls the development and lifespan of many animal species; however, mechanisms underlying low-temperature adaptation are poorly understood. Here, we describe cold-inducible diapause (CID), another type of diapause induced by low temperatures in Caenorhabditis elegans. A premature stop codon in heat shock factor 1 (hsf-1) triggers entry into CID at 9 °C, whereas wild-type animals enter CID at 4 °C. Furthermore, both wild-type and hsf-1(sy441) mutant animals undergoing CID can survive for weeks, and resume growth at 20 °C. Using epistasis analysis, we demonstrate that neural signalling pathways, namely tyraminergic and neuromedin U signalling, regulate entry into CID of the hsf-1 mutant. Overexpression of anti-ageing genes, such as hsf-1, XBP1/xbp-1, FOXO/daf-16, Nrf2/skn-1, and TFEB/hlh-30, also inhibits CID entry of the hsf-1 mutant. Based on these findings, we hypothesise that regulators of the hsf-1 mutant CID may impact longevity, and successfully isolate 16 long-lived mutants among 49 non-CID mutants via genetic screening. Furthermore, we demonstrate that the nonsense mutation of MED23/sur-2 prevents CID entry of the hsf-1(sy441) mutant and extends lifespan. Thus, CID is a powerful model to investigate neural networks involving cold acclimation and to explore new ageing mechanisms.

Suggested Citation

  • Makoto Horikawa & Masamitsu Fukuyama & Adam Antebi & Masaki Mizunuma, 2024. "Regulatory mechanism of cold-inducible diapause in Caenorhabditis elegans," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50111-8
    DOI: 10.1038/s41467-024-50111-8
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    References listed on IDEAS

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    1. Akane Ohta & Tomoyo Ujisawa & Satoru Sonoda & Atsushi Kuhara, 2014. "Light and pheromone-sensing neurons regulates cold habituation through insulin signalling in Caenorhabditis elegans," Nature Communications, Nature, vol. 5(1), pages 1-12, December.
    2. Louis R. Lapierre & C. Daniel De Magalhaes Filho & Philip R. McQuary & Chu-Chiao Chu & Orane Visvikis & Jessica T. Chang & Sara Gelino & Binnan Ong & Andrew E. Davis & Javier E. Irazoqui & Andrew Dill, 2013. "The TFEB orthologue HLH-30 regulates autophagy and modulates longevity in Caenorhabditis elegans," Nature Communications, Nature, vol. 4(1), pages 1-8, October.
    3. Yuan-Li Chen & Jun Tao & Pei-Ji Zhao & Wei Tang & Jian-Ping Xu & Ke-Qin Zhang & Cheng-Gang Zou, 2019. "Adiponectin receptor PAQR-2 signaling senses low temperature to promote C. elegans longevity by regulating autophagy," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
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