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Thermosensation in Caenorhabditis elegans is linked to ubiquitin-dependent protein turnover via insulin and calcineurin signalling

Author

Listed:
  • Alexandra Segref

    (University of Cologne
    University of Cologne)

  • Kavya L. Vakkayil

    (University of Cologne
    University of Cologne)

  • Tsimafei Padvitski

    (University of Cologne
    University of Cologne)

  • Qiaochu Li

    (University of Cologne
    University of Cologne)

  • Virginia Kroef

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

  • Jakob Lormann

    (University of Cologne
    University of Cologne)

  • Lioba Körner

    (University of Cologne
    University of Cologne)

  • Fabian Finger

    (University of Cologne
    University of Cologne
    University of Copenhagen)

  • Thorsten Hoppe

    (University of Cologne
    University of Cologne
    Faculty of Medicine and University Hospital of Cologne)

Abstract

Organismal physiology and survival are influenced by environmental conditions and linked to protein quality control. Proteome integrity is achieved by maintaining an intricate balance between protein folding and degradation. In Caenorhabditis elegans, acute heat stress determines cell non-autonomous regulation of chaperone levels. However, how the perception of environmental changes, including physiological temperature, affects protein degradation remains largely unexplored. Here, we show that loss-of-function of dyf-1 in Caenorhabditis elegans associated with dysfunctional sensory neurons leads to defects in both temperature perception and thermal adaptation of the ubiquitin/proteasome system centered on thermosensory AFD neurons. Impaired perception of moderate temperature changes worsens ubiquitin-dependent proteolysis in intestinal cells. Brain-gut communication regulating protein turnover is mediated by upregulation of the insulin-like peptide INS-5 and inhibition of the calcineurin-regulated forkhead-box transcription factor DAF-16/FOXO. Our data indicate that perception of ambient temperature and its neuronal integration is important for the control of proteome integrity in complex organisms.

Suggested Citation

  • Alexandra Segref & Kavya L. Vakkayil & Tsimafei Padvitski & Qiaochu Li & Virginia Kroef & Jakob Lormann & Lioba Körner & Fabian Finger & Thorsten Hoppe, 2022. "Thermosensation in Caenorhabditis elegans is linked to ubiquitin-dependent protein turnover via insulin and calcineurin signalling," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33467-7
    DOI: 10.1038/s41467-022-33467-7
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    References listed on IDEAS

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    1. Ayse Sena Mutlu & Shihong Max Gao & Haining Zhang & Meng C. Wang, 2020. "Olfactory specificity regulates lipid metabolism through neuroendocrine signaling in Caenorhabditis elegans," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    2. Javier Apfeld & Cynthia Kenyon, 1999. "Regulation of lifespan by sensory perception in Caenorhabditis elegans," Nature, Nature, vol. 402(6763), pages 804-809, December.
    3. Steven J. Cook & Travis A. Jarrell & Christopher A. Brittin & Yi Wang & Adam E. Bloniarz & Maksim A. Yakovlev & Ken C. Q. Nguyen & Leo T.-H. Tang & Emily A. Bayer & Janet S. Duerr & Hannes E. Bülow & , 2019. "Whole-animal connectomes of both Caenorhabditis elegans sexes," Nature, Nature, vol. 571(7763), pages 63-71, July.
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