Skeletal muscle fuel selection occurs at the mitochondrial level

Kuzmiak-Glancy, Sarah; Willis, Wayne T.

doi:10.1242/jeb.098863

Cited by 33Mitochondrial Function and PathologyAdipose Tissue and MetabolismCardiovascular and exercise physiology

Skeletal muscle fuel selection occurs at the mitochondrial level

Kuzmiak-Glancy, Sarah, Willis, Wayne T.·2014·Journal of Experimental Biology

DOI 10.1242/jeb.098863

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Abstract

Mammals exponentially increase the rate of carbohydrate oxidation as exercise intensity rises, while birds combust lipid almost exclusively while flying at high percentages of aerobic capacity. The fuel oxidized by contracting muscle depends on many factors: whole-body fuel storage mass, mobilization, blood transport, cellular uptake, and substrate selection at the level of the mitochondrion. We examined the fuel preferences of mitochondria isolated from mammalian and avian locomotory muscles using two approaches. First, the influence of substrates on the kinetics of respiration (Km,ADP and Vmax) was evaluated. For all substrates and combinations, Km,ADP was generally twofold higher in avian mitochondria. Second, fuel competition between pyruvate, glutamate and/or palmitoyl-l-carnitine at three levels of ATP free energy was determined using the principle of mass balance and the measured rates of O2 consumption and metabolite accumulation/utilization. Avian mitochondria strongly spared pyruvate from oxidation when another substrate was available and fatty acid was the dominant substrate, regardless of energy state. Mammalian mitochondria exhibited some preference for fatty acid over pyruvate at lower flux (higher energy state), but exhibited a much greater tendency to select pyruvate and glutamate when available. Studies in sonicated mitochondria revealed twofold higher electron transport chain electron conductance in avian mitochondria. We conclude that substantial fuel selection occurs at the level of the mitochondrial matrix and that avian flight muscle mitochondria are particularly biased toward the selection of fatty acid, possibly by facilitating high β-oxidation flux by maintaining a more oxidized matrix.

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Isolated skeletal muscle mitochondria from rats fed high-sugar or high-fat diets show reduced metabolic flexibility.
“Recently, isolated skeletal muscle mitochondria from rats fed high-sugar or high-fat diets showed reduced metabolic flexibility, indicating that substrate preference is independent of cytosolic-mitochondrial communication and in fact a consequence of inherent mitochondrial biochemical network interactions (92, 93).”
From Metabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease (2018) · cites this paper as [93]
Substrate preference is independent of cytosolic-mitochondrial communication and is a consequence of inherent mitochondrial biochemical network interactions.
“Recently, isolated skeletal muscle mitochondria from rats fed high-sugar or high-fat diets showed reduced metabolic flexibility, indicating that substrate preference is independent of cytosolic-mitochondrial communication and in fact a consequence of inherent mitochondrial biochemical network interactions (92, 93).”
From Metabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease (2018) · cites this paper as [93]

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Authors: Kuzmiak-Glancy, S., & Willis, W. T.
Affiliations: Arizona State University, United States
Mayo Clinic in Arizona (US)
Corresponding author: Willis, Wayne T.
ORCID: Willis, Wayne T.
Venue: Journal of Experimental Biology
Publisher: The Company of Biologists
Published: 2014-01-01
Volume: 217
Issue: Pt 11
Pages: 1993-2003
ISSN: 0022-0949 (ISSN-L)
1477-9145
DOI: 10.1242/jeb.098863
OpenAlex: W2140573109
Cited by: 33
References: 74
Citations by year: 2026: 1 · 2024: 1 · 2023: 4 · 2022: 5 · 2021: 7 · 2020: 4 · 2019: 2 · 2018: 3 · 2017: 2 · 2016: 2 · 2015: 2
FWCI: 0.82
Type: journal article
Language: en
Open access: closed
Locations: Journal of Experimental Biology (publishedVersion)
PubMed (publishedVersion)
HighWire Press Open Archive (submittedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
Keywords: pyruvate oxidation, fatty acid oxidation, palmitoyl-L-carnitine, glutamate oxidation, mammalian muscle, fatty acid beta-oxidation, respiration kinetics, mass balance
MeSH terms: Animals, Energy Metabolism, Physical Exertion, Locomotion, Mitochondria, Muscle, Muscle Contraction, Oxygen Consumption, Muscle, Skeletal, Passeriformes, Rats

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Skeletal muscle fuel selection occurs at the mitochondrial level

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