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Signal Transduction

AMP-Activated Protein Kinase α2 Deficiency Affects Cardiac Cardiolipin Homeostasis and Mitochondrial Function

  1. Yoni Athéa123,
  2. Benoît Viollet4567,
  3. Philippe Mateo123,
  4. Delphine Rousseau238,
  5. Marta Novotova9,
  6. Anne Garnier123,
  7. Sophie Vaulont4567,
  8. James R. Wilding123,
  9. Alain Grynberg238,
  10. Vladimir Veksler123,
  11. Jacqueline Hoerter123 and
  12. Renée Ventura-Clapier123
  1. 1Institut National de la Santé et de la Recherche Médicale U769, Châtenay-Malabry, France
  2. 2Université Paris-Sud 11, Châtenay-Malabry, France
  3. 3Institut Fédératif de Recherche 141, Châtenay-Malabry, France
  4. 4Institut Cochin, Département Endocrinologie Métabolisme et Cancer, Paris, France
  5. 5Institut National de la Santé et de la Recherche Médicale U567, Paris, France
  6. 6Centre National de la Recherche Scientifique, Unité Mixte de Recherche 8104, Paris, France
  7. 7Université Paris 5, Faculté de Médecine René Descartes, Unité mixte 3, Paris, France
  8. 8Institut National de la Recherche Agronomique-Unité Mixte de Recherche 1154, Châtenay-Malabry, France
  9. 9Institute of Molecular Physiology and Genetics, Slovak Academy of Sciences, Bratislava, Slovak Republic
  1. Address correspondence and reprint requests to Renée Ventura-Clapier, INSERM U-769, Université Paris-Sud, 5 rue J6B Clément, F-92296 Châtenay-Malabry, France. E-mail: renee.ventura{at}u-psud.fr
Diabetes 2007 Mar; 56(3): 786-794. https://doi.org/10.2337/db06-0187
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Abstract

AMP-activated protein kinase (AMPK) plays an important role in controlling energy homeostasis and is envisioned as a promising target to treat metabolic disorders. In the heart, AMPK is involved in short-term regulation and in transcriptional control of proteins involved in energy metabolism. Here, we investigated whether deletion of AMPKα2, the main cardiac catalytic isoform, alters mitochondrial function and biogenesis. Body weight, heart weight, and AMPKα1 expression were similar in control littermate and AMPKα2−/− mice. Despite normal oxygen consumption in perfused hearts, maximal oxidative capacity, measured using saponin permeabilized cardiac fibers, was ∼30% lower in AMPKα2−/− mice with octanoate, pyruvate, or glutamate plus malate but not with succinate as substrates, showing an impairment at complex I of the respiratory chain. This effect was associated with a 25% decrease in mitochondrial cardiolipin content, the main mitochondrial membrane phospholipid that is crucial for complex I activity, and with a 13% decrease in mitochondrial content of linoleic acid, the main fatty acid of cardiolipins. The decrease in cardiolipin content could be explained by mRNA downregulation of rate-limiting enzymes of both cardiolipin synthesis (CTP:PA cytidylyltransferase) and remodeling (acyl-CoA:lysocardiolipin acyltransferase 1). These data reveal a new role for AMPKα2 subunit in the regulation of cardiac muscle oxidative capacity via cardiolipin homeostasis.

  • ALCAT1, acyl-CoA:lysocardiolipin acyltransferase 1
  • AMPK, AMP-activated protein kinase
  • CDS2, CTP:PA cytidylyltransferase
  • CK, creatine kinase
  • COX, cytochrome c oxidase
  • CPT-1, carnitine palmitoyl transferase 1
  • FADH2, reduced flavine adenine dinucleotide
  • G3P, glycerol-3-phosphate
  • MDH, malate dehydrogenase
  • mi-CK, mitochondrial creatine kinase
  • NAO, 10N-nonyl acridine orange
  • OMC, oxoglutarate/malate carrier
  • PGC-1α, peroxisome proliferator–activated receptor-γ coactivator-1α

Footnotes

  • The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

    • Accepted November 27, 2006.
    • Received February 9, 2006.
  • DIABETES
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AMP-Activated Protein Kinase α2 Deficiency Affects Cardiac Cardiolipin Homeostasis and Mitochondrial Function
Yoni Athéa, Benoît Viollet, Philippe Mateo, Delphine Rousseau, Marta Novotova, Anne Garnier, Sophie Vaulont, James R. Wilding, Alain Grynberg, Vladimir Veksler, Jacqueline Hoerter, Renée Ventura-Clapier
Diabetes Mar 2007, 56 (3) 786-794; DOI: 10.2337/db06-0187

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AMP-Activated Protein Kinase α2 Deficiency Affects Cardiac Cardiolipin Homeostasis and Mitochondrial Function
Yoni Athéa, Benoît Viollet, Philippe Mateo, Delphine Rousseau, Marta Novotova, Anne Garnier, Sophie Vaulont, James R. Wilding, Alain Grynberg, Vladimir Veksler, Jacqueline Hoerter, Renée Ventura-Clapier
Diabetes Mar 2007, 56 (3) 786-794; DOI: 10.2337/db06-0187
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