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...
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2021
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oai:doaj.org-article:8540a2eb797040a69c7c29bcb73e2db02021-12-02T19:54:26ZNeuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans.1544-91731545-788510.1371/journal.pbio.3001431https://doaj.org/article/8540a2eb797040a69c7c29bcb73e2db02021-11-01T00:00:00Zhttps://doi.org/10.1371/journal.pbio.3001431https://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885To 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.Laetitia ChauveFrancesca HodgeSharlene MurdochFatemeh MasoudzadehHarry-Jack MannAndrea F Lopez-ClavijoHanneke OkkenhaugGreg WestBebiana C SousaAnne Segonds-PichonCheryl LiSteven W WingettHermine KienbergerKarin KleigreweMario de BonoMichael J O WakelamOlivia CasanuevaPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 19, Iss 11, p e3001431 (2021) |
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Biology (General) QH301-705.5 |
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Biology (General) QH301-705.5 Laetitia Chauve Francesca Hodge Sharlene Murdoch Fatemeh Masoudzadeh Harry-Jack Mann Andrea F Lopez-Clavijo Hanneke Okkenhaug Greg West Bebiana C Sousa Anne Segonds-Pichon Cheryl Li Steven W Wingett Hermine Kienberger Karin Kleigrewe Mario de Bono Michael J O Wakelam Olivia Casanueva Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans. |
| 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 |
article |
| author |
Laetitia Chauve Francesca Hodge Sharlene Murdoch Fatemeh Masoudzadeh Harry-Jack Mann Andrea F Lopez-Clavijo Hanneke Okkenhaug Greg West Bebiana C Sousa Anne Segonds-Pichon Cheryl Li Steven W Wingett Hermine Kienberger Karin Kleigrewe Mario de Bono Michael J O Wakelam Olivia Casanueva |
| author_facet |
Laetitia Chauve Francesca Hodge Sharlene Murdoch Fatemeh Masoudzadeh Harry-Jack Mann Andrea F Lopez-Clavijo Hanneke Okkenhaug Greg West Bebiana C Sousa Anne Segonds-Pichon Cheryl Li Steven W Wingett Hermine Kienberger Karin Kleigrewe Mario de Bono Michael J O Wakelam Olivia Casanueva |
| author_sort |
Laetitia Chauve |
| title |
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_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_sort |
neuronal hsf-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in c. elegans. |
| publisher |
Public Library of Science (PLoS) |
| publishDate |
2021 |
| url |
https://doaj.org/article/8540a2eb797040a69c7c29bcb73e2db0 |
| work_keys_str_mv |
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1718375910710706176 |