Higher activation of autophagy in skeletal muscle of mice during endurance exercise in the fasted state

Jamart, Cécile; Naslain, Damien; Gilson, Hélène; Francaux, Marc

doi:10.1152/ajpendo.00270.2013

Cited by 148Autophagy in Disease and TherapyMuscle Physiology and DisordersExercise and Physiological Responses

Higher activation of autophagy in skeletal muscle of mice during endurance exercise in the fasted state

Jamart, Cécile, Naslain, Damien, Gilson, Hélène, Francaux, Marc·2013·American Journal of Physiology-Endocrinology and Metabolism

DOI 10.1152/ajpendo.00270.2013

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Abstract

Activation of autophagy in skeletal muscle has been reported in response to endurance exercise and food deprivation independently. The purpose of this study was to evaluate whether autophagy was more activated when both stimuli were combined, namely when endurance exercise was performed in a fasted rather than a fed state. Mice performed a low-intensity running exercise (10 m/min for 90min) in both dietary states after which the gastrocnemius muscles were removed. LC3b-II, a marker of autophagosome presence, increased in both conditions, but the increase was higher in the fasted state. Other protein markers of autophagy, like Gabarapl1-II and Atg12 conjugated form as well as mRNA of Lc3b, Gabarapl1, and p62/Sqstm1 were increased only when exercise was performed in a fasted state. The larger activation of autophagy by exercise in a fasted state was associated with a larger decrease in plasma insulin and phosphorylation of Akt Ser473, Akt Thr308, FoxO3a Thr32, and ULK1 Ser757. AMPKα Thr172, ULK1 Ser317, and ULK1 Ser555 remained unchanged in both conditions, whereas p38 Thr180/Tyr182 increased during exercise to a similar extent in the fasted and fed conditions. The marker of mitochondrial fission DRP1 Ser616 was increased by exercise independently of the nutritional status. Changes in mitophagy markers BNIP3 and Parkin suggest that mitophagy was increased during exercise in the fasted state. In conclusion, our results highlight a major implication of the insulin-Akt-mTOR pathway and its downstream targets FoxO3a and ULK1 in the larger activation of autophagy observed when exercise is performed in a fasted state compared with a fed state.

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Autophagy is regulated by distinct mechanisms in different cell types, and these cell type-specific mechanisms underlie the differential vulnerability of separate tissues to autophagy mutations, resulting in heterogeneous manifestations of disease.
“Furthermore, mounting evidence shows that autophagy is regulated by distinct mechanisms in different cell types [11–26], and these cell type-specific mechanisms underlie the differential vulnerability of separate tissues to autophagy mutations, resulting in heterogenous manifestations of disease.”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [16]
Exercise potentiates autophagy activation due to starvation and the resulting reduction in plasma insulin, which downregulates AKT and FOXO3 signaling.
“Exercise also potentiates autophagy activation due to starvation and the resulting reduction in plasma insulin, which in turn downregulates AKT and FOXO3 signaling [16,18].”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [16]
Studies in rodents show increased abundance of autophagy proteins including Drp1, Bcl-2, and Bnip3 after exercise.
“Studies in rodents have shown an increased abundance of autophagy proteins including Drp1 and Bcl-2 and 19 kDa interacting protein-3 (Bnip3) after exercise (60, 65, 71, 78).”
From Mitochondria initiate and regulate sarcopenia (2017) · cites this paper as [60]

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Background
Exercise and the control of muscle mass in human
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High mTORC1 signaling is maintained, while protein degradation pathways are perturbed in old murine skeletal muscles in the fasted state
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Activation of autophagy in human skeletal muscle is dependent on exercise intensity and AMPK activation
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Regulation of (Macro)-Autophagy in Response to Exercise
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A single bout of exhaustive treadmill exercise increased AMPK activation associated with enhanced autophagy in mice skeletal muscle
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Regulation of autophagy in human skeletal muscle: effects of exercise, exercise training and insulin stimulation
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Exercise‐mediated modulation of autophagy in skeletal muscle
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Authors: Jamart, C., Naslain, D., Gilson, H., & Francaux, M.
Affiliations: UCLouvain (BE)
Corresponding author: Francaux, Marc
ORCID: Francaux, Marc
Venue: American Journal of Physiology-Endocrinology and Metabolism
Publisher: American Physiological Society
Published: 2013-10-15
Volume: 305
Issue: 8
Pages: E964-E974
ISSN: 0193-1849 (ISSN-L)
1522-1555
DOI: 10.1152/ajpendo.00270.2013
OpenAlex: W2158565718
Cited by: 148
References: 55
Citations by year: 2026: 1 · 2025: 4 · 2024: 7 · 2023: 5 · 2022: 19 · 2021: 16 · 2020: 12 · 2019: 10 · 2018: 17 · 2017: 17 · 2016: 15 · 2015: 17 · 2014: 6 · 2013: 2
FWCI: 9.72
Type: journal article
Language: en
Open access: closed
Locations: American Journal of Physiology-Endocrinology and Metabolism (publishedVersion)
PubMed (publishedVersion)
Digital Access to Libraries (Université catholique de Louvain (UCL), l'Université de Namur (UNamur) and the Université Saint-Louis (USL-B)) (submittedVersion)
Funders: Fondation Louvain
Topics: Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
Keywords: autophagy, endurance exercise, fasting, skeletal muscle, gastrocnemius, FOXO3, ULK1, mitophagy, Drp1, AMPK, p38 MAPK, GABARAPL1, LC3B, p62, food deprivation
MeSH terms: Sequestosome-1 Protein, Animals, Autophagy, Fasting, Female, Heat-Shock Proteins, Membrane Proteins, Mice, Inbred C57BL, Microtubule-Associated Proteins, Motor Activity, Physical Endurance, RNA, Messenger, Signal Transduction, Biomarkers, Up-Regulation, Muscle, Skeletal, Cytoplasmic Vesicles, Mitochondrial Proteins, Dynamins, Adaptor Proteins, Signal Transducing, Mice, Mitochondrial Dynamics

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Higher activation of autophagy in skeletal muscle of mice during endurance exercise in the fasted state

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