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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Autores principales: 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
Formato: article
Lenguaje:EN
Publicado: Public Library of Science (PLoS) 2021
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Acceso en línea:https://doaj.org/article/a78b7a74d13c459bbb5c8c7072758ce4
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Sumario: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. In response to heat, ectotherms exhibit an adaptive response characterized by changes in membrane fluidity. This study in the nematode Caenorhabditis elegans shows that neuronal HSF-1 is critical for this remodeling, suggesting a neuronal thermostat-based mechanism that can non-cell-autonomously coordinate the animal’s response to heat.