Chaperone-mediated autophagy in fish: A key function amid a changing environment

Chaperone-Mediated Autophagy (CMA) is a major pathway of lysosomal proteolysis critical for cellular homoeostasis and metabolism. While extensively studied in mammals, CMA’s existence in fish has only been confirmed recently, offering exciting insights into its role in species facing environmental s...

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Main Authors: Simon Schnebert, Emilio J Vélez, Maxime Goguet, Karine Dias, Vincent Véron, Isabel García-Pérez, Lisa M Radler, Emilie Cardona, Stéphanie Fontagné-Dicharry, Pierre Van Delft, Franziska Dittrich-Domergue, Amélie Bernard, Florian Beaumatin, Amaury Herpin, Beth Cleveland, Iban Seiliez
Format: Article
Language:English
Published: Taylor & Francis Group 2024-12-01
Series:Autophagy Reports
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Online Access:https://www.tandfonline.com/doi/10.1080/27694127.2024.2403956
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author Simon Schnebert
Emilio J Vélez
Maxime Goguet
Karine Dias
Vincent Véron
Isabel García-Pérez
Lisa M Radler
Emilie Cardona
Stéphanie Fontagné-Dicharry
Pierre Van Delft
Franziska Dittrich-Domergue
Amélie Bernard
Florian Beaumatin
Amaury Herpin
Beth Cleveland
Iban Seiliez
author_facet Simon Schnebert
Emilio J Vélez
Maxime Goguet
Karine Dias
Vincent Véron
Isabel García-Pérez
Lisa M Radler
Emilie Cardona
Stéphanie Fontagné-Dicharry
Pierre Van Delft
Franziska Dittrich-Domergue
Amélie Bernard
Florian Beaumatin
Amaury Herpin
Beth Cleveland
Iban Seiliez
author_sort Simon Schnebert
collection DOAJ
description Chaperone-Mediated Autophagy (CMA) is a major pathway of lysosomal proteolysis critical for cellular homoeostasis and metabolism. While extensively studied in mammals, CMA’s existence in fish has only been confirmed recently, offering exciting insights into its role in species facing environmental stress. Here, we shed light on the existence of 2 genes encoding the CMA-limiting factor Lamp2A (lysosomal associated membrane protein 2A) in rainbow trout (RT, Oncorhynchus mykiss), revealing distinct expression patterns across various tissues. Notably, RT lacking the most expressed Lamp2A exhibit profound hepatic proteome disturbances during acute nutritional stress, underscoring its pivotal role as a guardian of hepatic proteostasis. Building upon these findings, we introduce and validate the CMA activation score as a reliable indicator of CMA status, providing a valuable tool for detecting cellular stress in fish under environmental threats. Overall, our study offers new perspectives into understanding CMA from evolutionary and environmental contexts.
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series Autophagy Reports
spelling doaj-art-0eae5580c50f4e10ad5ee5490cf103512025-08-20T02:30:42ZengTaylor & Francis GroupAutophagy Reports2769-41272024-12-013110.1080/27694127.2024.2403956Chaperone-mediated autophagy in fish: A key function amid a changing environmentSimon Schnebert0Emilio J Vélez1Maxime Goguet2Karine Dias3Vincent Véron4Isabel García-Pérez5Lisa M Radler6Emilie Cardona7Stéphanie Fontagné-Dicharry8Pierre Van Delft9Franziska Dittrich-Domergue10Amélie Bernard11Florian Beaumatin12Amaury Herpin13Beth Cleveland14Iban Seiliez15Université de Pau et des Pays de l’Adour, E2S UPPA, INRAE, Nutrition Métabolisme et Aquaculture, NuMeA, Saint-Pée-sur Nivelle, FranceUniversité de Pau et des Pays de l’Adour, E2S UPPA, INRAE, Nutrition Métabolisme et Aquaculture, NuMeA, Saint-Pée-sur Nivelle, FranceUniversité de Pau et des Pays de l’Adour, E2S UPPA, INRAE, Nutrition Métabolisme et Aquaculture, NuMeA, Saint-Pée-sur Nivelle, FranceUniversité de Pau et des Pays de l’Adour, E2S UPPA, INRAE, Nutrition Métabolisme et Aquaculture, NuMeA, Saint-Pée-sur Nivelle, FranceUniversité de Pau et des Pays de l’Adour, E2S UPPA, INRAE, Nutrition Métabolisme et Aquaculture, NuMeA, Saint-Pée-sur Nivelle, FranceUniversité de Pau et des Pays de l’Adour, E2S UPPA, INRAE, Nutrition Métabolisme et Aquaculture, NuMeA, Saint-Pée-sur Nivelle, FranceNational Center for Cool and Cold Water Aquaculture, ARS/USDA, Kearneysville, WV, USAUniversité de Pau et des Pays de l’Adour, E2S UPPA, INRAE, Nutrition Métabolisme et Aquaculture, NuMeA, Saint-Pée-sur Nivelle, FranceUniversité de Pau et des Pays de l’Adour, E2S UPPA, INRAE, Nutrition Métabolisme et Aquaculture, NuMeA, Saint-Pée-sur Nivelle, FranceLaboratoire de Biogenèse Membranaire, UMR, CNRS, Univ. Bordeaux, Villenave d’Ornon, FranceLaboratoire de Biogenèse Membranaire, UMR, CNRS, Univ. Bordeaux, Villenave d’Ornon, FranceLaboratoire de Biogenèse Membranaire, UMR, CNRS, Univ. Bordeaux, Villenave d’Ornon, FranceUniversité de Pau et des Pays de l’Adour, E2S UPPA, INRAE, Nutrition Métabolisme et Aquaculture, NuMeA, Saint-Pée-sur Nivelle, FranceINRAE, UR Laboratory of Fish Physiology and Genomics, Campus de Beaulieu, Rennes, FranceNational Center for Cool and Cold Water Aquaculture, ARS/USDA, Kearneysville, WV, USAUniversité de Pau et des Pays de l’Adour, E2S UPPA, INRAE, Nutrition Métabolisme et Aquaculture, NuMeA, Saint-Pée-sur Nivelle, FranceChaperone-Mediated Autophagy (CMA) is a major pathway of lysosomal proteolysis critical for cellular homoeostasis and metabolism. While extensively studied in mammals, CMA’s existence in fish has only been confirmed recently, offering exciting insights into its role in species facing environmental stress. Here, we shed light on the existence of 2 genes encoding the CMA-limiting factor Lamp2A (lysosomal associated membrane protein 2A) in rainbow trout (RT, Oncorhynchus mykiss), revealing distinct expression patterns across various tissues. Notably, RT lacking the most expressed Lamp2A exhibit profound hepatic proteome disturbances during acute nutritional stress, underscoring its pivotal role as a guardian of hepatic proteostasis. Building upon these findings, we introduce and validate the CMA activation score as a reliable indicator of CMA status, providing a valuable tool for detecting cellular stress in fish under environmental threats. Overall, our study offers new perspectives into understanding CMA from evolutionary and environmental contexts.https://www.tandfonline.com/doi/10.1080/27694127.2024.2403956Chaperone-mediated autophagyfishrainbow troutmetabolismstressenvironment
spellingShingle Simon Schnebert
Emilio J Vélez
Maxime Goguet
Karine Dias
Vincent Véron
Isabel García-Pérez
Lisa M Radler
Emilie Cardona
Stéphanie Fontagné-Dicharry
Pierre Van Delft
Franziska Dittrich-Domergue
Amélie Bernard
Florian Beaumatin
Amaury Herpin
Beth Cleveland
Iban Seiliez
Chaperone-mediated autophagy in fish: A key function amid a changing environment
Autophagy Reports
Chaperone-mediated autophagy
fish
rainbow trout
metabolism
stress
environment
title Chaperone-mediated autophagy in fish: A key function amid a changing environment
title_full Chaperone-mediated autophagy in fish: A key function amid a changing environment
title_fullStr Chaperone-mediated autophagy in fish: A key function amid a changing environment
title_full_unstemmed Chaperone-mediated autophagy in fish: A key function amid a changing environment
title_short Chaperone-mediated autophagy in fish: A key function amid a changing environment
title_sort chaperone mediated autophagy in fish a key function amid a changing environment
topic Chaperone-mediated autophagy
fish
rainbow trout
metabolism
stress
environment
url https://www.tandfonline.com/doi/10.1080/27694127.2024.2403956
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