RRC ID 75924
Author Chauve L, Hodge F, Murdoch S, Masoudzadeh F, Mann HJ, Lopez-Clavijo AF, Okkenhaug H, West G, Sousa BC, Segonds-Pichon A, Li C, Wingett SW, Kienberger H, Kleigrewe K, de Bono M, Wakelam MJO, Casanueva O.
Title Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans.
Journal PLoS Biol
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.
Volume 19(11)
Pages e3001431
Published 2021-11-1
DOI 10.1371/journal.pbio.3001431
PMID 34723964
PMC PMC8585009
MeSH Adaptation, Physiological* Animals Bone Morphogenetic Proteins / metabolism Caenorhabditis elegans / genetics Caenorhabditis elegans / growth & development Caenorhabditis elegans / physiology* Caenorhabditis elegans Proteins / metabolism* Cold Temperature Cyclic GMP / metabolism Glycerophospholipids / metabolism Hot Temperature* Lipids / chemistry* Neurons / metabolism* Phenotype Signal Transduction Stress, Physiological Transcription Factors / metabolism* Transcription, Genetic Transforming Growth Factor beta / metabolism
C.elegans tm331