Open AccessNeuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans
Author(s) -
Laetitia Chauve,
Francesca Hodge,
Sharlene Murdoch,
Fatemeh Masoudzadeh,
Harry-Jack Mann,
Andrea F. Lopez-Clavijo,
Hanneke Okkenhaug,
Greg West,
Bebiana C. Sousa,
Anne SegondsPichon,
Cheryl Li,
Steven Wingett,
Hermine Kienberger,
Karin Kleigrewe,
Mario de Bono,
Michael J.O. Wakelam,
Olivia Casanueva
Publication year - 2021
Publication title -
plos biology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 4.127
H-Index - 271
eISSN - 1545-7885
pISSN - 1544-9173
DOI - 10.1371/journal.pbio.3001431
Subject(s) - biology , microbiology and biotechnology , caenorhabditis elegans , ectotherm , heat shock , heat shock protein , lipid metabolism , biochemistry , gene , zoology
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.