Adaptive plasticity of autophagic proteins to denervation in aging skeletal muscle
Abstract
Aging muscle exhibits a progressive decline in mass and strength, known as sarcopenia, and a decrease in the adaptive response to contractile activity. The molecular mechanisms mediating this reduced plasticity have yet to be elucidated. The purposes of this study were 1) to determine whether denervation-induced muscle disuse would increase the expression of autophagy genes and 2) to examine whether selective autophagy pathways (mitophagy) are altered in aged animals. Denervation reduced muscle mass in young and aged animals by 24 and 16%, respectively. Moreover, young animals showed a 50% decrease in mitochondrial content following denervation, an adaptation that was not matched by aged animals. Basal autophagy protein expression was higher in aged animals, whereas young animals exhibited a greater induction of autophagy proteins following denervation. Localization of LC3II, Parkin, and p62 was significantly increased in the mitochondrial fraction of young and aged animals following denervation. Moreover, the unfolded protein response marker CHOP and the mitochondrial dynamics protein Fis1 were increased by 17- and 2.5-fold, respectively, in aged animals. Lipofuscin granules within lysosomes were evident with aging and denervation. Thus reductions in the adaptive plasticity of aged muscle are associated with decreases in disuse-induced autophagy. These data indicate that the expression of autophagy proteins and their localization to mitochondria are not decreased in aged muscle; however, the induction of autophagy in response to disuse, along with downstream events such as lysosome function, is impaired. This may contribute to an accumulation of dysfunctional mitochondria in aged muscle.
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Our data are congruent with reports of a dysregulated autophagy response in aging muscle, including higher expression of mediators of autophagy.
“Our data are congruent with reports of a dysregulated autophagy response in aging muscle, including higher expression of mediators of autophagy (O'Leary et al., 2013).”
From Autophagy gene expression in skeletal muscle of older individuals is associated with physical performance, muscle volume and mitochondrial function in the study of muscle, mobility and aging ( <scp>SOMMA</scp> ) (2024) · cites this paper as O'Leary et al., 2013
Mitophagy is altered in aged muscle.
“Recent findings suggest that mitophagy, the process in charge of the removal of damaged/dysfunctional mitochondria, is altered in aged muscle.”
From Parkin overexpression protects from ageing‐related loss of muscle mass and strength (2019) · cites this paper as O'Leary et al. 2013
Impaired mitophagy could contribute to the ageing-related loss of muscle mass and function.
“Recent evidence suggests that impaired mitophagy, a process in charge of removing damaged/dysfunctional mitochondria and in part regulated by Parkin, could contribute to the ageing‐related loss of muscle mass and function.”
From Parkin overexpression protects from ageing‐related loss of muscle mass and strength (2019) · cites this paper as O'Leary et al. 2013
Mitophagic processes controlled by the Parkin-Pink1 pathway may be impaired in aged muscles and are probably responsible for the ageing-related accumulation of dysfunctional mitochondria.
“Recent studies have proposed that mitophagic processes controlled by the Parkin–Pink1 pathway may be impaired in aged muscles and are probably responsible for the ageing‐related accumulation of dysfunctional mitochondria (O'Leary et al. 2013; Rana et al. 2013; Gouspillou et al. 2014b).”
From Parkin overexpression protects from ageing‐related loss of muscle mass and strength (2019) · cites this paper as O'Leary et al. 2013
In aged rats, these changes are accompanied by reduced adaptive reserve in response to denervation, with impaired autophagy induction and lower levels of mitophagy compared to young rats.
“These changes are accompanied by reduced adaptive reserve in response to denervation, with impaired autophagy induction and lower levels of mitophagy compared to young rats [496].”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [496]
In aged rats, muscle tissues display elevated basal levels of proteolysis, higher expression of autophagy proteins and accumulation of unfolded protein response elements.
“In aged rats, muscle tissues display elevated basal levels of proteolysis, higher expression of autophagy proteins and the accumulation of unfolded protein response elements.”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [496]
Impaired mitochondrial autophagy (mitophagy) machinery is another primary cause of mitochondrial dysfunction in aging muscle.
“Another primary cause of mitochondrial dysfunction in aging muscle is the impaired mitochondrial autophagy (mitophagy) machinery.”
From From mitochondria to sarcopenia: role of 17β-estradiol and testosterone (2023) · cites this paper as [91]
Aging provokes alterations of several key mitophagy regulators, leading to mitophagy deficiency and subsequent accumulation of dysfunctional mitochondria in skeletal muscle.
“Studies indicate that aging provokes certain alternations of several key mitophagy regulators, leading to mitophagy deficiency and subsequent accumulation of dysfunctional mitochondria in skeletal muscle (91, 92).”
From From mitochondria to sarcopenia: role of 17β-estradiol and testosterone (2023) · cites this paper as [91]
Mfn2 content in aged rodent skeletal muscle is reported as decreased, unchanged, or increased.
“Mfn2 content has been reported as decreased [34,49,55], unchanged [52], or even increased in aged rodent skeletal muscles [47,50,54].”
From Mitochondrial Dynamics and Mitophagy in Skeletal Muscle Health and Aging (2021) · cites this paper as [47]
Studies in rodents have reported increased or unchanged Drp1 content in aged skeletal muscles.
“Indeed, studies in rodents have reported increased [49,50,51] or unchanged [34,47,52,54] Drp1 content in aged skeletal muscles.”
From Mitochondrial Dynamics and Mitophagy in Skeletal Muscle Health and Aging (2021) · cites this paper as [47]
Accumulation of lipofuscin particles in aged muscles from rodents and humans suggests that autophagy-lysosomal function is defective.
“several studies have observed an accumulation of lipofuscin particles in aged muscles from rodents [47] and humans [111,112], suggesting that the autophagy-lysosomal function is defective.”
From Mitochondrial Dynamics and Mitophagy in Skeletal Muscle Health and Aging (2021) · cites this paper as [47]
Accumulation of lipofuscin granules suggests lysosomal failure to remove dysfunctional mitochondria in aging even when Parkin has translocated.
“an accumulation of lipofuscin granules suggests a failure of the lysosome to remove dysfunctional mitochondrial in aging even when Parkin has translocated to the mitochondria (103).”
From Mitochondria initiate and regulate sarcopenia (2017) · cites this paper as [103]
High apoptotic signaling, altered autophagy signaling, and elevated UPS activity occur in muscles after spinal cord injury or denervation.
“High levels of apoptotic signaling (1, 129) and altered autophagy signaling (102, 103) with elevated UPS activity (137) occurs in muscles after spinal cord injury or denervation.”
From Mitochondria initiate and regulate sarcopenia (2017) · cites this paper as [103]
Excessive activation of autophagy aggravates muscle wasting by removing portion of cytoplasm, proteins, and organelles.
“Excessive activation of autophagy aggravates muscle wasting by removing portion of cytoplasm, proteins, and organelles30,50,51”
From Disuse-associated loss of the protease Lonp1 in muscle impairs mitochondrial function and causes reduced skeletal muscle mass and strength (2022) · cites this paper as [50]
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- Authors
- O'Leary, M. F., Vainshtein, A., Iqbal, S., Ostojic, O., & Hood, D. A.
- Affiliations
- School of Kinesiology and Health Science, and Muscle Health Research Centre, York University, Toronto, Ontario, Canada
- York University (CA)
- Corresponding author
- Hood, David A.
- Venue
- American Journal of Physiology-Cell Physiology
- Publisher
- American Physiological Society
- Published
- 2013-03-01
- Volume
- 304
- Issue
- 5
- Pages
- C422-C430
- ISSN
- 0363-6143 (ISSN-L)
- 1522-1563
- OpenAlex
- W2165822680
- Cited by
- 165
- References
- 44
- Citations by year
- 2026: 2 · 2025: 9 · 2024: 10 · 2023: 14 · 2022: 14 · 2021: 17 · 2020: 10 · 2019: 16 · 2018: 23 · 2017: 12 · 2016: 10 · 2015: 12 · 2014: 5 · 2013: 11
- FWCI
- 6.68
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Physiology-Cell Physiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- sarcopenia, muscle aging, denervation, muscle disuse, autophagy, mitophagy, selective autophagy, mitochondrial dysfunction, LC3-II, Parkin, p62, CHOP, unfolded protein response, Fis1, lipofuscin, lysosomes, skeletal muscle
- MeSH terms
- Age Factors, Animals, Autophagy, Lipofuscin, Lysosomes, Male, Mitochondria, Muscle Denervation, Muscle Proteins, Rats, Inbred F344, Muscle, Skeletal, Mitochondrial Proteins, Ubiquitin-Protein Ligases, Rats, Transcription Factor CHOP
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