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
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/a78b7a74d13c459bbb5c8c7072758ce4
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spelling	oai:doaj.org-article:a78b7a74d13c459bbb5c8c7072758ce42021-11-18T05:36:59ZNeuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans1544-91731545-7885https://doaj.org/article/a78b7a74d13c459bbb5c8c7072758ce42021-11-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8585009/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885To 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.Laetitia ChauveFrancesca HodgeSharlene MurdochFatemeh MasoudzadehHarry-Jack MannAndrea F. Lopez-ClavijoHanneke OkkenhaugGreg WestBebiana C. SousaAnne Segonds-PichonCheryl LiSteven W. WingettHermine KienbergerKarin KleigreweMario de BonoMichael J. O. WakelamOlivia CasanuevaPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 19, Iss 11 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 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 Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans
description	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.
format	article
author	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
author_facet	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
author_sort	Laetitia Chauve
title	Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans
title_short	Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans
title_full	Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans
title_fullStr	Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans
title_full_unstemmed	Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans
title_sort	neuronal hsf-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in c. elegans
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/a78b7a74d13c459bbb5c8c7072758ce4
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Neuronal HSF-1 coordinates the propagation of fat desaturation across tissues to enable adaptation to high temperatures in C. elegans

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