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Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans
To survive elevated temperatures, ectotherms adjust the fluidity of membranes by fine-tuning lipid desaturation levels in a process previously described to be cell autonomous. We have discovered that, in Caenorhabditis elegans, neuronal heat shock factor 1 (HSF-1), the conserved master regulator of...
Autores principales: | , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8585009/ https://www.ncbi.nlm.nih.gov/pubmed/34723964 http://dx.doi.org/10.1371/journal.pbio.3001431 |
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author | Chauve, Laetitia Hodge, Francesca Murdoch, Sharlene Masoudzadeh, Fatemeh Mann, Harry-Jack Lopez-Clavijo, Andrea F. Okkenhaug, Hanneke West, Greg Sousa, Bebiana C. Segonds-Pichon, Anne Li, Cheryl Wingett, Steven W. Kienberger, Hermine Kleigrewe, Karin de Bono, Mario Wakelam, Michael J. O. Casanueva, Olivia |
author_facet | Chauve, Laetitia Hodge, Francesca Murdoch, Sharlene Masoudzadeh, Fatemeh Mann, Harry-Jack Lopez-Clavijo, Andrea F. Okkenhaug, Hanneke West, Greg Sousa, Bebiana C. Segonds-Pichon, Anne Li, Cheryl Wingett, Steven W. Kienberger, Hermine Kleigrewe, Karin de Bono, Mario Wakelam, Michael J. O. Casanueva, Olivia |
author_sort | Chauve, Laetitia |
collection | PubMed |
description | To survive elevated temperatures, ectotherms adjust the fluidity of membranes by fine-tuning lipid desaturation levels in a process previously described to be cell autonomous. We have discovered that, in Caenorhabditis elegans, neuronal heat shock factor 1 (HSF-1), the conserved master regulator of the heat shock response (HSR), causes extensive fat remodeling in peripheral tissues. These changes include a decrease in fat desaturase and acid lipase expression in the intestine and a global shift in the saturation levels of plasma membrane’s phospholipids. The observed remodeling of plasma membrane is in line with ectothermic adaptive responses and gives worms a cumulative advantage to warm temperatures. We have determined that at least 6 TAX-2/TAX-4 cyclic guanosine monophosphate (cGMP) gated channel expressing sensory neurons, and transforming growth factor ß (TGF-β)/bone morphogenetic protein (BMP) are required for signaling across tissues to modulate fat desaturation. We also find neuronal hsf-1 is not only sufficient but also partially necessary to control the fat remodeling response and for survival at warm temperatures. This is the first study to show that a thermostat-based mechanism can cell nonautonomously coordinate membrane saturation and composition across tissues in a multicellular animal. |
format | Online Article Text |
id | pubmed-8585009 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-85850092021-11-12 Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans Chauve, Laetitia Hodge, Francesca Murdoch, Sharlene Masoudzadeh, Fatemeh Mann, Harry-Jack Lopez-Clavijo, Andrea F. Okkenhaug, Hanneke West, Greg Sousa, Bebiana C. Segonds-Pichon, Anne Li, Cheryl Wingett, Steven W. Kienberger, Hermine Kleigrewe, Karin de Bono, Mario Wakelam, Michael J. O. Casanueva, Olivia PLoS Biol Research Article To survive elevated temperatures, ectotherms adjust the fluidity of membranes by fine-tuning lipid desaturation levels in a process previously described to be cell autonomous. We have discovered that, in Caenorhabditis elegans, neuronal heat shock factor 1 (HSF-1), the conserved master regulator of the heat shock response (HSR), causes extensive fat remodeling in peripheral tissues. These changes include a decrease in fat desaturase and acid lipase expression in the intestine and a global shift in the saturation levels of plasma membrane’s phospholipids. The observed remodeling of plasma membrane is in line with ectothermic adaptive responses and gives worms a cumulative advantage to warm temperatures. We have determined that at least 6 TAX-2/TAX-4 cyclic guanosine monophosphate (cGMP) gated channel expressing sensory neurons, and transforming growth factor ß (TGF-β)/bone morphogenetic protein (BMP) are required for signaling across tissues to modulate fat desaturation. We also find neuronal hsf-1 is not only sufficient but also partially necessary to control the fat remodeling response and for survival at warm temperatures. This is the first study to show that a thermostat-based mechanism can cell nonautonomously coordinate membrane saturation and composition across tissues in a multicellular animal. Public Library of Science 2021-11-01 /pmc/articles/PMC8585009/ /pubmed/34723964 http://dx.doi.org/10.1371/journal.pbio.3001431 Text en © 2021 Chauve et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Chauve, Laetitia Hodge, Francesca Murdoch, Sharlene Masoudzadeh, Fatemeh Mann, Harry-Jack Lopez-Clavijo, Andrea F. Okkenhaug, Hanneke West, Greg Sousa, Bebiana C. Segonds-Pichon, Anne Li, Cheryl Wingett, Steven W. Kienberger, Hermine Kleigrewe, Karin de Bono, Mario Wakelam, Michael J. O. Casanueva, Olivia Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans |
title | Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans |
title_full | Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans |
title_fullStr | Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans |
title_full_unstemmed | Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans |
title_short | Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans |
title_sort | neuronal hsf-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in c. elegans |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8585009/ https://www.ncbi.nlm.nih.gov/pubmed/34723964 http://dx.doi.org/10.1371/journal.pbio.3001431 |
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