Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans

article Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans published yes Laetitia Chauve author Francesca Hodge author Sharlene Murdoch author Fatemah Masoudzadeh author Harry Jack Mann author Andrea Lopez-Clavijo author Hanneke Okkenhaug author Greg West author Bebiana C. Sousa author Anne Segonds-Pichon author Cheryl Li author Steven Wingett author Hermine Kienberger author Karin Kleigrewe author Mario De Bono author 4E3FF80E-F248-11E8-B48F-1D18A9856A870000-0001-8347-0443 Michael Wakelam author Olivia Casanueva author MaDe department 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. https://research-explorer.ista.ac.at/download/10322/10330/2021_PLoSBio_Chauve.pdf application/pdfno Public Library of Science2021 eng PLoS Biology 1544-9173 1545-7885 34723964 00071581840000110.1371/journal.pbio.3001431 1911 https://research-explorer.ista.ac.at/record/13069 L. Chauve et al., “Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans,” PLoS Biology, vol. 19, no. 11. Public Library of Science, 2021. Chauve, Laetitia, Francesca Hodge, Sharlene Murdoch, Fatemah Masoudzadeh, Harry Jack Mann, Andrea Lopez-Clavijo, Hanneke Okkenhaug, et al. “Neuronal HSF-1 Coordinates the Propagation of Fat Desaturation across Tissues to Enable Adaptation to High Temperatures in C. Elegans.” PLoS Biology. Public Library of Science, 2021. <a href="https://doi.org/10.1371/journal.pbio.3001431">https://doi.org/10.1371/journal.pbio.3001431</a>. Chauve, Laetitia, et al. “Neuronal HSF-1 Coordinates the Propagation of Fat Desaturation across Tissues to Enable Adaptation to High Temperatures in C. Elegans.” PLoS Biology, vol. 19, no. 11, e3001431, Public Library of Science, 2021, doi:<a href="https://doi.org/10.1371/journal.pbio.3001431">10.1371/journal.pbio.3001431</a>. L. Chauve, F. Hodge, S. Murdoch, F. Masoudzadeh, H.J. Mann, A. Lopez-Clavijo, H. Okkenhaug, G. West, B.C. Sousa, A. Segonds-Pichon, C. Li, S. Wingett, H. Kienberger, K. Kleigrewe, M. de Bono, M. Wakelam, O. Casanueva, PLoS Biology 19 (2021). Chauve, L., Hodge, F., Murdoch, S., Masoudzadeh, F., Mann, H. J., Lopez-Clavijo, A., … Casanueva, O. (2021). Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans. PLoS Biology. Public Library of Science. <a href="https://doi.org/10.1371/journal.pbio.3001431">https://doi.org/10.1371/journal.pbio.3001431</a> Chauve L, Hodge F, Murdoch S, et al. Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans. PLoS Biology. 2021;19(11). doi:<a href="https://doi.org/10.1371/journal.pbio.3001431">10.1371/journal.pbio.3001431</a> Chauve L, Hodge F, Murdoch S, Masoudzadeh F, Mann HJ, Lopez-Clavijo A, Okkenhaug H, West G, Sousa BC, Segonds-Pichon A, Li C, Wingett S, Kienberger H, Kleigrewe K, de Bono M, Wakelam M, Casanueva O. 2021. Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans. PLoS Biology. 19(11), e3001431. 103222021-11-21T23:01:28Z2023-08-14T11:53:27Z