Coordination of metabolic plasticity in skeletal muscle

Hood, David A.; Irrcher, Isabella; Ljubicic, Vladimir; Joseph, Anna-Maria

doi:10.1242/jeb.02182

Cited by 370Mitochondrial Function and PathologyAdipose Tissue and MetabolismMuscle Physiology and Disorders

Coordination of metabolic plasticity in skeletal muscle

Hood, David A., Irrcher, Isabella, Ljubicic, Vladimir, Joseph, Anna-Maria·2006·Journal of Experimental Biology

DOI 10.1242/jeb.02182

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Abstract

SUMMARY: Skeletal muscle is a highly malleable tissue, capable of pronounced metabolic and morphological adaptations in response to contractile activity(i.e. exercise). Each bout of contractile activity results in a coordinated alteration in the expression of a variety of nuclear DNA and mitochondrial DNA(mtDNA) gene products, leading to phenotypic adaptations. This results in an increase in muscle mitochondrial volume and changes in organelle composition,referred to as mitochondrial biogenesis. The functional consequence of this biogenesis is an improved resistance to fatigue. Signals initiated by the exercise bout involve changes in intracellular Ca2+ as well as alterations in energy status (i.e. ATP/ADP ratio) and the consequent activation of downstream kinases such as AMP kinase and Ca2+-calmodulin-activated kinases. These kinases activate transcription factors that bind DNA to affect the transcription of genes, the most evident manifestation of which occurs during the post-exercise recovery period when energy metabolism is directed toward anabolism, rather than contractile activity. An important protein that is affected by exercise is the transcriptional coactivator PGC-1α, which cooperates with multiple transcription factors to induce the expression of nuclear genes encoding mitochondrial proteins. Once translated in the cytosol, these mitochondrially destined proteins are imported into the mitochondrial outer membrane, inner membrane or matrix space via specific import machinery transport components. Contractile activity affects the expression of the import machinery, as well as the kinetics of import, thus facilitating the entry of newly synthesized proteins into the expanding organelle. An important set of proteins that are imported are the mtDNA transcription factors, which influence the expression and replication of mtDNA. While mtDNA contributes only 13 proteins to the synthesis of the organelle, these proteins are vital for the proper assembly of multi-subunit complexes of the respiratory chain,when combined with nuclear-encoded protein subunits. The expansion of skeletal muscle mitochondria during organelle biogenesis involves the assembly of an interconnected network system (i.e. a mitochondrial reticulum). This expansion of membrane size is influenced by the balance between mitochondrial fusion and fission. Thus, mitochondrial biogenesis is an adaptive process that requires the coordination of multiple cellular events, including the transcription of two genomes, the synthesis of lipids and proteins and the stoichiometric assembly of multisubunit protein complexes into a functional respiratory chain. Impairments at any step can lead to defective electron transport, a subsequent failure of ATP production and an inability to maintain energy homeostasis.

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Skeletal muscles are able to match ATP supply with demand under many different physiological and environmental stimuli, highlighting high metabolic plasticity.
“Remarkably, skeletal muscles are able to match ATP supply with demand under many different physiological and environmental stimuli, highlighting the high metabolic plasticity [6,7,8] of this most abundant tissue in humans [9].”
From Regulation of Energy Substrate Metabolism in Endurance Exercise (2021) · cites this paper as [6]
Improvements from altering health behaviors appear to stem from endocrinological changes that occur with overfatness and following exposure to exercise.
“Where these improvements appear to stem from a number of endocrinological changes that occur with both expression of overfatness and following exposure to exercise that ultimately alters the health status for the individual who is overfat [18,19,26,28,30,32-34].”
From Diet, exercise or diet with exercise: comparing the effectiveness of treatment options for weight-loss and changes in fitness for adults (18–65 years old) who are overfat, or obese; systematic review and meta-analysis (2015) · cites this paper as [30]
Altering any health behaviors leads to a reduction in the risk factors for preventable non-communicable diseases.
“Even if it is well understood that altering any health behaviors leads to a reduction in the risk factors for preventable non-communicable diseases [18,20,26-33].”
From Diet, exercise or diet with exercise: comparing the effectiveness of treatment options for weight-loss and changes in fitness for adults (18–65 years old) who are overfat, or obese; systematic review and meta-analysis (2015) · cites this paper as [30]

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Authors: Hood, D. A., Irrcher, I., Ljubicic, V., & Joseph, A.-M.
Affiliations: York University (CA)
ORCID: Hood, David A.
Ljubicic, Vladimir
Venue: Journal of Experimental Biology
Publisher: The Company of Biologists
Published: 2006-06-15
Volume: 209
Issue: 12
Pages: 2265-2275
ISSN: 0022-0949 (ISSN-L)
1477-9145
DOI: 10.1242/jeb.02182
OpenAlex: W2017268286
Cited by: 370
References: 106
Citations by year: 2026: 5 · 2025: 6 · 2024: 4 · 2023: 12 · 2022: 7 · 2021: 13 · 2020: 14 · 2019: 9 · 2018: 16 · 2017: 14 · 2016: 12 · 2015: 20 · 2014: 15 · 2013: 34 · 2012: 33
FWCI: 2.36
Type: journal article
Language: en
Open access: closed
Locations: Journal of Experimental Biology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Keywords: skeletal muscle, exercise adaptation, mitochondrial biogenesis, metabolic plasticity, PGC-1α, AMP kinase, mitochondrial fission and fusion, mitochondrial reticulum, respiratory chain assembly, energy homeostasis, fatigue resistance, post-exercise recovery
MeSH terms: Adaptation, Physiological, Animals, Gene Expression Regulation, Humans, Transcription Factors, Signal Transduction, Muscle, Skeletal, Mitochondrial Proteins

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Coordination of metabolic plasticity in skeletal muscle

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