Thermosensation in Caenorhabditis elegans is linked to ubiquitin-dependent protein turnover via insulin and calcineurin signalling
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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.
| Originalsprog | Engelsk |
|---|---|
| Artikelnummer | 5874 |
| Tidsskrift | Nature Communications |
| Vol/bind | 13 |
| Udgave nummer | 1 |
| Antal sider | 17 |
| ISSN | 2041-1723 |
| DOI | |
| Status | Udgivet - 2022 |
Bibliografisk note
Funding Information:
We thank O. Hobert for valuable advice on the neuronal identity assay, R. Morimoto for strains. S. Greco-Torres and G. Vopper for technical assistance, C. Ahyoud for generating strains, the Cologne Centre for Genomics (CCG) for microarray analysis, H. Nolte (CECAD proteomics facility) for proteomics analysis, SunyBiotech for generating the GFP::C05D11.5 strain, L. Leson for help with setting up the thermotaxis gradient device. C. elegans strains were kindly provided by the Caenorhabditis Genetics Center (funded by the NIH Office of Research Infrastructure Programs (P40 OD010440), and the Mitani lab. We also thank A. Andersen (Life Science Editors), C.E. Kutzner, S. Ravanelli, and D. Vilchez for critical reading of the manuscript. This work was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany´s Excellence Strategy – EXC 2030 – 390661388 and by the European Research Council (ERC-CoG-616499) to T.H. Diese Arbeit wurde von der Deutschen Forschungsgemeinschaft (DFG) im Rahmen der deutschen Exzellenzstrategie – EXC 2030 – 390661388 und vom Europäischen Forschungsrat (ERC-CoG-616499) an T.H. gefördert. K.L.V. received support by the Cologne Graduate School of Aging Research.
Funding Information:
We thank O. Hobert for valuable advice on the neuronal identity assay, R. Morimoto for strains. S. Greco-Torres and G. Vopper for technical assistance, C. Ahyoud for generating strains, the Cologne Centre for Genomics (CCG) for microarray analysis, H. Nolte (CECAD proteomics facility) for proteomics analysis, SunyBiotech for generating the GFP::C05D11.5 strain, L. Leson for help with setting up the thermotaxis gradient device. C. elegans strains were kindly provided by the Caenorhabditis Genetics Center (funded by the NIH Office of Research Infrastructure Programs (P40 OD010440), and the Mitani lab. We also thank A. Andersen (Life Science Editors), C.E. Kutzner, S. Ravanelli, and D. Vilchez for critical reading of the manuscript. This work was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany´s Excellence Strategy – EXC 2030 – 390661388 and by the European Research Council (ERC-CoG-616499) to T.H. Diese Arbeit wurde von der Deutschen Forschungsgemeinschaft (DFG) im Rahmen der deutschen Exzellenzstrategie – EXC 2030 – 390661388 und vom Europäischen Forschungsrat (ERC-CoG-616499) an T.H. gefördert. K.L.V. received support by the Cologne Graduate School of Aging Research.
Publisher Copyright:
© 2022, The Author(s).
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