Cited by 158Mitochondrial Function and PathologyAdipose Tissue and MetabolismPeroxisome Proliferator-Activated Receptors

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The transcriptional coactivator PGC-1α is essential for maximal and efficient cardiac mitochondrial fatty acid oxidation and lipid homeostasis

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Lehman, John J., Boudina, Sihem, Banke, Natasha Hausler, Sambandam, Nandakumar, Han, Xianlin, Young, Deanna M., Leone, Teresa C., Gross, Richard W., Lewandowski, E. Douglas, Abel, E. Dale, Kelly, Daniel P.·2008·American Journal of Physiology-Heart and Circulatory Physiology

DOI 10.1152/ajpheart.00081.2008PMC PMC2494758

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Abstract

High-capacity mitochondrial ATP production is essential for normal function of the adult heart, and evidence is emerging that mitochondrial derangements occur in common myocardial diseases. Previous overexpression studies have shown that the inducible transcriptional coactivator peroxisome proliferator-activated receptor-gamma coactivator (PGC)-1alpha is capable of activating postnatal cardiac myocyte mitochondrial biogenesis. Recently, we generated mice deficient in PGC-1alpha (PGC-1alpha(-/-) mice), which survive with modestly blunted postnatal cardiac growth. To determine if PGC-1alpha is essential for normal cardiac energy metabolic capacity, mitochondrial function experiments were performed on saponin-permeabilized myocardial fibers from PGC-1alpha(-/-) mice. These experiments demonstrated reduced maximal (state 3) palmitoyl-l-carnitine respiration and increased maximal (state 3) pyruvate respiration in PGC-1alpha(-/-) mice compared with PGC-1alpha(+/+) controls. ATP synthesis rates obtained during maximal (state 3) respiration in permeabilized myocardial fibers were reduced for PGC-1alpha(-/-) mice, whereas ATP produced per oxygen consumed (ATP/O), a measure of metabolic efficiency, was decreased by 58% for PGC-1alpha(-/-) fibers. Ex vivo isolated working heart experiments demonstrated that PGC-1alpha(-/-) mice exhibited lower cardiac power, reduced palmitate oxidation, and increased reliance on glucose oxidation, with the latter likely a compensatory response. (13)C NMR revealed that hearts from PGC-1alpha(-/-) mice exhibited a limited capacity to recruit triglyceride as a source for lipid oxidation during beta-adrenergic challenge. Consistent with reduced mitochondrial fatty acid oxidative enzyme gene expression, the total triglyceride content was greater in hearts of PGC-1alpha(-/-) mice relative to PGC-1alpha(+/+) following a fast. Overall, these results demonstrate that PGC-1alpha is essential for the maintenance of maximal, efficient cardiac mitochondrial fatty acid oxidation, ATP synthesis, and myocardial lipid homeostasis.

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Authors: Lehman, J. J., Boudina, S., Banke, N. H., Sambandam, N., Han, X., Young, D. M., Leone, T. C., Gross, R. W., Lewandowski, E. D., Abel, E. D., & Kelly, D. P.
Affiliations: Washington University in St. Louis (US)
University of Utah (US)
University of Illinois Chicago (US)
ORCID: Boudina, Sihem
Han, Xianlin
Gross, Richard W.
Lewandowski, E. Douglas
Abel, E. Dale
Kelly, Daniel P.
Venue: American Journal of Physiology-Heart and Circulatory Physiology
Publisher: American Physiological Society
Published: 2008-07
Volume: 295
Issue: 1
Pages: H185-H196
ISSN: 0363-6135 (ISSN-L)
1522-1539
DOI: 10.1152/ajpheart.00081.2008
PMC: PMC2494758
OpenAlex: W2099192357
Cited by: 158
References: 64
Citations by year: 2026: 4 · 2025: 2 · 2024: 3 · 2023: 7 · 2022: 6 · 2021: 6 · 2020: 16 · 2019: 4 · 2018: 8 · 2017: 15 · 2016: 6 · 2015: 2 · 2014: 12 · 2013: 6 · 2012: 16
FWCI: 6.16
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: American Journal of Physiology-Heart and Circulatory Physiology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute on Aging (K08AG024844)
National Heart, Lung, and Blood Institute (R01HL073167, R01-HL-73167, R37HL049244, R01HL058493, R01-HL-3749244)
National Institute of Diabetes and Digestive and Kidney Diseases (P30DK056341, P30DK052574)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Peroxisome Proliferator-Activated Receptors
Keywords: PGC-1α, myocardial energy metabolism, mitochondrial biogenesis, palmitate oxidation, triglyceride mobilization, beta-adrenergic stimulation, cardiac power output
MeSH terms: Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha, Adenosine Triphosphate, Adrenergic beta-Agonists, Animals, Energy Metabolism, Fatty Acids, Female, Glucose, Homeostasis, Isoproterenol, Male, Mitochondria, Heart, Myocardial Contraction, Myocardium, Magnetic Resonance Spectroscopy, Oxidation-Reduction, Oxidative Phosphorylation, Oxygen Consumption, Palmitoylcarnitine, Transcription Factors, Triglycerides, Trans-Activators, Mice, Knockout, Pyruvic Acid, Mice, In Vitro Techniques

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The transcriptional coactivator PGC-1α is essential for maximal and efficient cardiac mitochondrial fatty acid oxidation and lipid homeostasis

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