Homeostatic control of stearoyl desaturase expression via patched-like receptor PTR-23 ensures the survival of C. elegans during heat stress

Venkatesh, SR and Siddiqui, R and Sandhu, A and Ramani, M and Houston, IR and Watts, JL and Singh, V (2023) Homeostatic control of stearoyl desaturase expression via patched-like receptor PTR-23 ensures the survival of C. elegans during heat stress. In: PLoS Genetics, 19 (12).

PDF plo_gen_19_12_2023 - Published Version Download (3MB)

Abstract

Organismal responses to temperature fluctuations include an evolutionarily conserved cytosolic chaperone machinery as well as adaptive alterations in lipid constituents of cellular membranes. Using C. elegans as a model system, we asked whether adaptable lipid homeostasis is required for survival during physiologically relevant heat stress. By systematic analyses of lipid composition in worms during and before heat stress, we found that unsaturated fatty acids are reduced in heat-stressed animals. This is accompanied by the transcriptional downregulation of fatty acid desaturase enzymes encoded by fat-1, fat-3, fat-4, fat-5, fat-6, and fat-7 genes. Conversely, overexpression of the �9 desaturase FAT-7, responsible for the synthesis of PUFA precursor oleic acid, and supplementation of oleic acid causes accelerated death of worms during heat stress. Interestingly, heat stress causes permeability defects in the worm�s cuticle. We show that fat-7 expression is reduced in the permeability defective collagen (PDC) mutant, dpy-10, known to have enhanced heat stress resistance (HSR). Further, we show that the HSR of dpy-10 animals is dependent on the upregulation of PTR-23, a patched-like receptor in the epidermis, and that PTR-23 downregulates the expression of fat-7. Consequently, abrogation of ptr-23 in wild type animals affects its survival during heat stress. This study provides evidence for the negative regulation of fatty acid desaturase expression in the soma of C. elegans via the non-canonical role of a patched receptor signaling component. Taken together, this constitutes a skin-gut axis for the regulation of lipid desaturation to promote the survival of worms during heat stress. © 2023 Venkatesh et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Item Type:	Journal Article
Publication:	PLoS Genetics
Publisher:	Public Library of Science
Additional Information:	The copyright for this article belongs to the authors.
Keywords:	acyl coenzyme A desaturase; oleic acid; patched like receptor 23; stearoyl desaturase; unclassified drug; unsaturated fatty acid; acyl coenzyme A desaturase; Caenorhabditis elegans protein, Article; Caenorhabditis elegans; down regulation; epidermis; fatty acid desaturation; fatty acid metabolism; fatty acid synthesis; feedback system; gene overexpression; genotype; heat stress; homeostasis; imaging; lipid composition; lipid homeostasis; lipogenesis; mass fragmentography; nonhuman; paralysis; physiological stress; protein expression; real time polymerase chain reaction; RNAi therapeutics; survival; upregulation; animal; genetics; heat shock response; homeostasis; metabolism; physiology, Animals; Caenorhabditis elegans; Caenorhabditis elegans Proteins; Fatty Acid Desaturases; Fatty Acids, Unsaturated; Heat-Shock Response; Homeostasis; Oleic Acids; Stearoyl-CoA Desaturase
Department/Centre:	Division of Biological Sciences > Molecular Reproduction, Development & Genetics
Date Deposited:	02 Aug 2024 05:53
Last Modified:	02 Aug 2024 05:53
URI:	http://eprints.iisc.ac.in/id/eprint/85302

Actions (login required)

View Item