• Open Access

Mitochondrial energetics is impaired in vivo in aged skeletal muscle

Authors

  • Gilles Gouspillou,

    Corresponding author
    1. Résonance Magnétique des Systèmes Biologiques, UMR 5536 CNRS - Bordeaux Segalen University, Bordeaux, France
    2. Département de Kinanthropologie, Université du Québec à Montréal, Montreal, Quebec, Canada
    • Correspondence

      Gilles Gouspillou, Université du Québec à Montréal, Faculté des Sciences, Département de Kinanthropologie, Pavillon Sc Biologiques, SB- 4640 141 Avenue du Président-Kennedy, Montreal, Quebec, Canada H2X 1Y4. Tel.: +1 514 987 3000 ext. 5322; fax: +1 514 987 6616+1 514 987 6616; e-mail: gilles.gouspillou@gmail.com

    Search for more papers by this author
  • Isabelle Bourdel-Marchasson,

    1. Résonance Magnétique des Systèmes Biologiques, UMR 5536 CNRS - Bordeaux Segalen University, Bordeaux, France
    2. CHU de Bordeaux, Pôle de gérontologie clinique, Bordeaux, France
    Search for more papers by this author
  • Richard Rouland,

    1. Résonance Magnétique des Systèmes Biologiques, UMR 5536 CNRS - Bordeaux Segalen University, Bordeaux, France
    Search for more papers by this author
  • Guillaume Calmettes,

    1. Résonance Magnétique des Systèmes Biologiques, UMR 5536 CNRS - Bordeaux Segalen University, Bordeaux, France
    2. Department of Medicine (Cardiology), David Geffen School of Medicine, University of California, Los Angeles, CA, USA
    Search for more papers by this author
  • Marc Biran,

    1. Résonance Magnétique des Systèmes Biologiques, UMR 5536 CNRS - Bordeaux Segalen University, Bordeaux, France
    Search for more papers by this author
  • Véronique Deschodt-Arsac,

    1. INSERM U1045 – Cardio-Thoracic Research Centre – and Rhythmology and Heart Modeling Institute (LIRYC), Bordeaux University, Bordeaux, France
    Search for more papers by this author
  • Sylvain Miraux,

    1. Résonance Magnétique des Systèmes Biologiques, UMR 5536 CNRS - Bordeaux Segalen University, Bordeaux, France
    Search for more papers by this author
  • Eric Thiaudiere,

    1. Résonance Magnétique des Systèmes Biologiques, UMR 5536 CNRS - Bordeaux Segalen University, Bordeaux, France
    Search for more papers by this author
  • Philippe Pasdois,

    1. INSERM U1045 – Cardio-Thoracic Research Centre – and Rhythmology and Heart Modeling Institute (LIRYC), Bordeaux University, Bordeaux, France
    Search for more papers by this author
  • Dominique Detaille,

    1. INSERM U1045 – Cardio-Thoracic Research Centre – and Rhythmology and Heart Modeling Institute (LIRYC), Bordeaux University, Bordeaux, France
    Search for more papers by this author
  • Jean-Michel Franconi,

    1. Résonance Magnétique des Systèmes Biologiques, UMR 5536 CNRS - Bordeaux Segalen University, Bordeaux, France
    Search for more papers by this author
  • Marion Babot,

    1. Laboratoire de Physiologie Moléculaire et Cellulaire, Institut de Biochimie et Génétique Cellulaires, UMR 5095, CNRS-Université Bordeaux 2, Bordeaux Cedex, France
    Search for more papers by this author
  • Véronique Trézéguet,

    1. Laboratoire de Physiologie Moléculaire et Cellulaire, Institut de Biochimie et Génétique Cellulaires, UMR 5095, CNRS-Université Bordeaux 2, Bordeaux Cedex, France
    Search for more papers by this author
  • Laurent Arsac,

    1. Résonance Magnétique des Systèmes Biologiques, UMR 5536 CNRS - Bordeaux Segalen University, Bordeaux, France
    Search for more papers by this author
  • Philippe Diolez

    1. INSERM U1045 – Cardio-Thoracic Research Centre – and Rhythmology and Heart Modeling Institute (LIRYC), Bordeaux University, Bordeaux, France
    Search for more papers by this author

Summary

With aging, most skeletal muscles undergo a progressive loss of mass and strength, a process termed sarcopenia. Aging-related defects in mitochondrial energetics have been proposed to be causally involved in sarcopenia. However, changes in muscle mitochondrial oxidative phosphorylation with aging remain a highly controversial issue, creating a pressing need for integrative approaches to determine whether mitochondrial bioenergetics are impaired in aged skeletal muscle. To address this issue, mitochondrial bioenergetics was first investigated in vivo in the gastrocnemius muscle of adult (6 months) and aged (21 months) male Wistar rats by combining a modular control analysis approach with 31P magnetic resonance spectroscopy measurements of energetic metabolites. Using this innovative approach, we revealed that the in vivo responsiveness (‘elasticity’) of mitochondrial oxidative phosphorylation to contraction-induced increase in ATP demand is significantly reduced in aged skeletal muscle, a reduction especially pronounced under low contractile activities. In line with this in vivo aging-related defect in mitochondrial energetics, we found that the mitochondrial affinity for ADP is significantly decreased in mitochondria isolated from aged skeletal muscle. Collectively, the results of this study demonstrate that mitochondrial bioenergetics are effectively altered in vivo in aged skeletal muscle and provide a novel cellular basis for this phenomenon.

Ancillary