Alteration of mitochondrial oxidative phosphorylation in aged skeletal muscle involves modification of adenine nucleotide translocator
Open accessAbstract
The process of skeletal muscle aging is characterized by a progressive loss of muscle mass and functionality. The underlying mechanisms are highly complex and remain unclear. This study was designed to further investigate the consequences of aging on mitochondrial oxidative phosphorylation in rat gastrocnemius muscle, by comparing young (6 months) and aged (21 months) rats. Maximal oxidative phosphorylation capacity was clearly reduced in older rats, while mitochondrial efficiency was unaffected. Inner membrane properties were unaffected in aged rats since proton leak kinetics were identical to young rats. Application of top-down control analysis revealed a dysfunction of the phosphorylation module in older rats, responsible for a dysregulation of oxidative phosphorylation under low activities close to in vivo ATP turnover. This dysregulation is responsible for an impaired mitochondrial response toward changes in cellular ATP demand, leading to a decreased membrane potential which may in turn affect ROS production and ion homeostasis. Based on our data, we propose that modification of ANT properties with aging could partly explain these mitochondrial dysfunctions.
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Mitochondrial dysfunctions accumulate with ageing and are critical in the sarcopenic process.
“Solid experimental evidence indicates that mitochondrial dysfunctions accumulate with ageing and are critical in the sarcopenic process.”
From Parkin overexpression protects from ageing‐related loss of muscle mass and strength (2019) · cites this paper as Gouspillou et al. 2010
The Results (§3.2, page unavailable) report reduced oxidative phosphorylation in mitochondria from aged rats, and the Discussion (§4, page unavailable) reports a lower sarcopenic index in those rats. But the Discussion only hypothesizes that age-related mitochondrial dysfunction may contribute to mechanisms associated with muscle loss; it does not establish that dysfunctions accumulate over time or are critical to sarcopenia. (LLM, conf=0.87)
Experimental — accuracy not yet measuredAged skeletal muscles display impaired mitochondrial energetics.
“Notably, aged skeletal muscles display impaired mitochondrial energetics (Trounce et al. 1989; Short et al. 2005; Gouspillou et al. 2010; Lanza et al. 2012; Gouspillou et al. 2014a) and increased mitochondrial‐mediated apoptosis (Selman et al. 2003; Dirks & Leeuwenburgh, 2004; Leeuwenburgh et al. 2005; Chabi et al. 2008; Marzetti et al. 2008; Picard et al. 2010; Picard et al. 2011; Gouspillou et a”
From Parkin overexpression protects from ageing‐related loss of muscle mass and strength (2019) · cites this paper as Gouspillou et al. 2010
Subsequent studies with beetroot juice as the nitrate source, as well as sodium nitrate salt, confirmed and extended these results.
“Subsequent studies have confirmed and extended these results with beetroot juice as the nitrate source, as well as sodium nitrate salt.120,129 -131”
From Nitrate-Nitrite-Nitric Oxide Pathway: Implications for Anesthesiology and Intensive Care (2010) · cites this paper as [129]
The Methods (§2.3) and Results (§3.2; page numbers unavailable) concern oxidative phosphorylation in mitochondria from young and aged rats. Searches for beetroot juice and sodium nitrate found no passage addressing nitrate-source studies or their confirmation of earlier results. (LLM, conf=0.78)
Experimental — accuracy not yet measuredIn these studies, oxygen cost was also reduced during maximal performance, and time-to-exhaustion was significantly extended after beetroot juice.
“In these studies, oxygen cost was also reduced during maximal performance, and time-to-exhaustion was significantly extended after beetroot juice.”
From Nitrate-Nitrite-Nitric Oxide Pathway: Implications for Anesthesiology and Intensive Care (2010) · cites this paper as [129]
The Methods (§2.3) measure oxygen consumption in isolated mitochondria, and the Results (§3.2) compare mitochondria from young and aged rats. Searches for beetroot juice, exercise oxygen cost, maximal performance, and time-to-exhaustion found no passage addressing the claimed effects. (LLM, conf=0.78)
Experimental — accuracy not yet measuredAging is associated with a decline in mitochondrial bioenergetics in rodents and humans.
“Indeed, many studies conducted in both rodents and humans have shown that aging is associated with a decline in mitochondrial bioenergetics [9,10,11].”
From Mitochondrial Dynamics and Mitophagy in Skeletal Muscle Health and Aging (2021) · cites this paper as [10]
Aged skeletal muscles display impaired mitochondrial bioenergetics.
“More specifically, aged skeletal muscles display impaired mitochondrial bioenergetics (Drew and Leeuwenburgh, 2003; Short et al., 2005; Gouspillou et al., 2010) and an increase in mitochondrially mediated apoptosis (Dirks and Leeuwenburgh, 2002; Marzetti et al., 2008; Gouspillou et al., 2014a), which primarily contributes to the aging-related decline in muscle mass and function.”
From Effects of Aging and Caloric Restriction on Fiber Type Composition, Mitochondrial Morphology and Dynamics in Rat Oxidative and Glycolytic Muscles (2019) · cites this paper as Gouspillou et al., 2010
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References 51 · Cited by 62
- Authors
- Gouspillou, G., Bourdel-Marchasson, I., Rouland, R., Calmettes, G., Franconi, J.-M., Deschodt-Arsac, V., & Diolez, P.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Diolez, Philippe
- Venue
- Biochimica et Biophysica Acta (BBA) - Bioenergetics
- Publisher
- Elsevier BV
- Published
- 2010-02
- Volume
- 1797
- Issue
- 2
- Pages
- 143-151
- ISSN
- 0005-2728 (ISSN-L)
- OpenAlex
- W2050147970
- Cited by
- 62
- References
- 51
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 6 · 2023: 1 · 2022: 1 · 2021: 6 · 2020: 1 · 2019: 4 · 2018: 3 · 2017: 2 · 2016: 6 · 2015: 5 · 2014: 2 · 2013: 5 · 2012: 3
- FWCI
- 1.74
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Biochimica et Biophysica Acta (BBA) - Bioenergetics (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › ATP Synthase and ATPases Research
- Keywords
- skeletal muscle aging, mitochondrial oxidative phosphorylation, adenine nucleotide translocase, gastrocnemius, proton leak, mitochondrial efficiency, mitochondrial membrane potential, reactive oxygen species, ATP turnover
- MeSH terms
- Adenosine Triphosphate, Aging, Animals, Kinetics, Male, Mitochondria, Muscle, Oxidative Phosphorylation, Oxygen Consumption, Phosphorylation, Rats, Wistar, Muscle, Skeletal, Adenine Nucleotide Translocator 1, Rats, Membrane Potential, Mitochondrial
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