Mitochondria-associated apoptotic signalling in denervated rat skeletal muscle

Siu, Parco M.; Alway, Stephen E.

doi:10.1113/jphysiol.2004.081083

Cited by 221Cell death mechanisms and regulationMuscle Physiology and DisordersMitochondrial Function and Pathology

Mitochondria-associated apoptotic signalling in denervated rat skeletal muscle

Siu, Parco M., Alway, Stephen E.·2005·The Journal of Physiology

DOI 10.1113/jphysiol.2004.081083

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Abstract

Apoptosis has been implicated in the regulation of denervation-induced muscle atrophy. However, the activation of apoptotic signal transduction during muscle denervation has not been fully elucidated. The present study examined the apoptotic responses to denervation in rat gastrocnemius muscle. Following 14 days of denervation, the extent of apoptotic DNA fragmentation as determined by a cytosolic nucleosome ELISA was increased by 100% in the gastrocnemius muscle. RT-PCR and immunoblot analyses indicated that Bax was dramatically upregulated while Bcl-2 was modestly increased; however, the Bax/Bcl-2 ratio was significantly increased in denervated muscles relative to control muscles. Analyses of ELISA and immunoblots from mitochondria-free cytosol extracts showed a significant increase in mitochondria-associated apoptotic factors, including cytochrome c, Smac/DIABLO and apoptosis-inducing factor (AIF). In addition to the upregulation of caspase-3 and -9 mRNA, pro-/cleaved caspase protein and proteolytic activity levels, the X-linked inhibitor of apoptosis (XIAP) protein level was downregulated. The cleaved product of poly(ADP-ribose) polymerase (PARP) was detected in muscle samples following denervation. Although we did not find a difference in the inhibitor of DNA binding/differentiation-2 (Id2) and c-Myc protein contents between the denervated and control muscles, the protein content of tumour suppressor p53 was significantly increased in both the nuclear and the cytosolic fractions with denervation. Moreover, denervation increased the protein content of HSP70, whereas the MnSOD (a mitochondrial isoform of superoxide dismutase) protein content was diminished, which indicated that denervation might have induced cellular and/or oxidative stress. Our data show that mitochondria-associated apoptotic signalling is upregulated during muscle denervation. We interpret these findings to indicate that apoptosis has a physiologically important role in regulating denervation-induced muscle atrophy.

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In aging, loss of innervation induces profound muscle atrophy.
“In aging, a loss of innervation induces profound muscle atrophy (5, 106, 129).”
From Mitochondria initiate and regulate sarcopenia (2017) · cites this paper as [129]

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Inflammation: Roles in Skeletal Muscle Atrophy
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Effect of denervation on mitochondrially mediated apoptosis in skeletal muscle.
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Limb Immobilization Induces a Coordinate Down-Regulation of Mitochondrial and Other Metabolic Pathways in Men and Women
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Muscle memory and a new cellular model for muscle atrophy and hypertrophy
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Apoptosis in skeletal muscle and its relevance to atrophy
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Denervation drives skeletal muscle atrophy and induces mitochondrial dysfunction, mitophagy and apoptosis via miR-142a-5p/MFN1 axis
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Nuclear apoptosis contributes to sarcopenia
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Nuclear domains during muscle atrophy: nuclei lost or paradigm lost?
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Antioxidant administration attenuates mechanical ventilation‐induced rat diaphragm muscle atrophy independent of protein kinase B (PKB–Akt) signalling
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Mitochondrial Dysfunction Launches Dexamethasone-Induced Skeletal Muscle Atrophy via AMPK/FOXO3 Signaling
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Suppression of Oxidative Stress by Resveratrol After Isometric Contractions in Gastrocnemius Muscles of Aged Mice
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Nuclear translocation of EndoG at the initiation of disuse muscle atrophy and apoptosis is specific to myonuclei
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Active acetylcholine receptors prevent the atrophy of skeletal muscles and favor reinnervation
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p53 and ATF4 mediate distinct and additive pathways to skeletal muscle atrophy during limb immobilization
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β-Hydroxy-β-methylbutyrate (HMB) enhances the proliferation of satellite cells in fast muscles of aged rats during recovery from disuse atrophy
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Modulation of age-induced apoptotic signaling and cellular remodeling by exercise and calorie restriction in skeletal muscle
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Age-related alterations in expression of apoptosis regulatory proteins and heat shock proteins in rat skeletal muscle
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No change in myonuclear number during muscle unloading and reloading
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Age-dependent increase in oxidative stress in gastrocnemius muscle with unloading
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Mediation of endogenous antioxidant enzymes and apoptotic signaling by resveratrol following muscle disuse in the gastrocnemius muscles of young and old rats
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Resistance training increases heat shock protein levels in skeletal muscle of young and old rats
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Molecular events and signalling pathways involved in skeletal muscle disuse‐induced atrophy and the impact of countermeasures
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Denervation-induced mitochondrial dysfunction and autophagy in skeletal muscle of apoptosis-deficient animals
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Inhibition of xanthine oxidase reduces oxidative stress and improves skeletal muscle function in response to electrically stimulated isometric contractions in aged mice
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Statins Trigger Mitochondrial Reactive Oxygen Species-Induced Apoptosis in Glycolytic Skeletal Muscle
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Absence of caspase-3 protects against denervation-induced skeletal muscle atrophy
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Denervation Induces Cytosolic Phospholipase A2-mediated Fatty Acid Hydroperoxide Generation by Muscle Mitochondria
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Denervation effects on myonuclear domain size of rat diaphragm fibers
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Satellite cell proliferation is reduced in muscles of obese Zucker rats but restored with loading
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Tadalafil Increases Akt and Extracellular Signal-Regulated Kinase 1/2 Activation, and Prevents Apoptotic Cell Death in the Penis Following Denervation
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Stress-induced opening of the permeability transition pore in the dystrophin-deficient heart is attenuated by acute treatment with sildenafil
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The Role of Calpains in Skeletal Muscle Remodeling with Exercise and Inactivity-induced Atrophy
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Redox regulation of diaphragm proteolysis during mechanical ventilation
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Response and adaptation of skeletal muscle to denervation stress: the role of apoptosis in muscle loss
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Nutritional and metabolic support in patients with amyotrophic lateral sclerosis
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Muscle denervation promotes opening of the permeability transition pore and increases the expression of cyclophilin D
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Age‐associated mitochondrial dysfunction in skeletal muscle: Contributing factors and suggestions for long‐term interventions
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Nuclear factor-κB signaling contributes to mechanical ventilation-induced diaphragm weakness*
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The angiotensin-(1–7)/Mas axis reduces myonuclear apoptosis during recovery from angiotensin II-induced skeletal muscle atrophy in mice
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Skeletal muscle mitochondrial depletion and dysfunction in chronic kidney disease.
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Deficiency of the Bax gene attenuates denervation-induced apoptosis
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Effects of chronic high-fat feeding on skeletal muscle mass and function in middle-aged mice
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Aging-Dependent Regulation of Antioxidant Enzymes and Redox Status in Chronically Loaded Rat Dorsiflexor Muscles
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Differential apoptosis-related protein expression, mitochondrial properties, proteolytic enzyme activity, and DNA fragmentation between skeletal muscles
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Neuronal involvement in muscular atrophy
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Muscle Apoptotic Response to Denervation, Disuse, and Aging
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Suppressed autophagy flux in skeletal muscle of an amyotrophic lateral sclerosis mouse model during disease progression
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Neurotrophic Factors Improve Motoneuron Survival and Function of Muscle Reinnervated by Embryonic Neurons
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Regenerative cell injection in denervated muscle reduces atrophy and enhances recovery following nerve repair
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Electrical stimulation based on chronaxie reduces atrogin‐1 and myoD gene expressions in denervated rat muscle
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Hindlimb unloading increases muscle content of cytosolic but not nuclear Id2 and p53 proteins in young adult and aged rats
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Induction of mitochondrial biogenesis protects against caspase-dependent and caspase-independent apoptosis in L6 myoblasts
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Muscle apoptosis is induced in pressure-induced deep tissue injury
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Time‐course of changes in the myonuclear domain during denervation in young‐adult and old rat gastrocnemius muscle
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Oxidative stress in the denervated muscle
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Proapoptotic factor Bax is increased in satellite cells in the tibialis anterior muscles of old rats
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Curcumin treatment prevents increased proteasome and apoptosome activities in rat skeletal muscle during reloading and improves subsequent recovery
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The Role of Mitochondria in Mediation of Skeletal Muscle Repair
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Lack of muscle recovery after immobilization in old rats does not result from a defect in normalization of the ubiquitin–proteasome and the caspase‐dependent apoptotic pathways
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Absence of physiological Ca2+ transients is an initial trigger for mitochondrial dysfunction in skeletal muscle following denervation
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Myonuclear permanence in skeletal muscle memory: a systematic review and meta‐analysis of human and animal studies
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Effect of prior chronic contractile activity on mitochondrial function and apoptotic protein expression in denervated muscle
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Bax signaling regulates palmitate-mediated apoptosis in C2C12myotubes
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Protein–DNA array-based identification of transcription factor activities differentially regulated in skeletal muscle of normal and dystrophin-deficient mdx mice
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Self-citation

Authors: Siu, P. M., & Alway, S. E.
Affiliations: West Virginia University (US)
ORCID: Siu, Parco M.
Alway, Stephen E.
Venue: The Journal of Physiology
Publisher: Wiley
Published: 2005-05
Volume: 565
Issue: 1
Pages: 309-323
ISSN: 0022-3751 (ISSN-L)
1469-7793
DOI: 10.1113/jphysiol.2004.081083
OpenAlex: W1484492220
Cited by: 216
References: 85
Citations by year: 2026: 1 · 2025: 5 · 2024: 4 · 2023: 6 · 2022: 8 · 2021: 14 · 2020: 8 · 2019: 3 · 2018: 6 · 2017: 8 · 2016: 7 · 2015: 15 · 2014: 8 · 2013: 8 · 2012: 10
FWCI: 7.15
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 10 d)
Locations: The Journal of Physiology (publishedVersion)
PubMed (publishedVersion)
The HKU Scholars Hub (University of Hong Kong) (submittedVersion)
Funders: National Institute on Aging (R01AG021530)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Keywords: muscle denervation, muscle atrophy, apoptosis, gastrocnemius, Bax/Bcl-2 ratio, cytochrome c, Smac/DIABLO, apoptosis-inducing factor, caspase-3, caspase-9, XIAP, PARP cleavage, p53, HSP70, manganese superoxide dismutase, oxidative stress, skeletal muscle
MeSH terms: Animals, Gene Expression Regulation, Mitochondria, Muscle, Muscle Denervation, Muscle Proteins, Rats, Inbred F344, Signal Transduction, Apoptosis, Muscle, Skeletal, Rats

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Mitochondria-associated apoptotic signalling in denervated rat skeletal muscle

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