Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans |
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Authors: | 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 |
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Affiliation: | 1. Epigenetics Department, Babraham Institute, Cambridge, United Kingdom;2. Babraham Institute, Cambridge, United Kingdom;3. Bavarian Centre for Biomolecular Mass Spectrometry, Freising, Germany;4. Institute of Science and Technology, Klosterneuburg, Austria;5. Signalling Department, Babraham Institute, Cambridge, United Kingdom; Brandeis University, UNITED STATES |
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Abstract: | 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. |
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