Carbon monoxide improves cardiac function and mitochondrial population quality in a mouse model of metabolic syndrome

PLoS One. 2012;7(8):e41836. doi: 10.1371/journal.pone.0041836. Epub 2012 Aug 1.

Abstract

Aims: Metabolic syndrome induces cardiac dysfunction associated with mitochondria abnormalities. As low levels of carbon monoxide (CO) may improve myocardial and mitochondrial activities, we tested whether a CO-releasing molecule (CORM-3) reverses metabolic syndrome-induced cardiac alteration through changes in mitochondrial biogenesis, dynamics and autophagy.

Methods and results: Mice were fed with normal diet (ND) or high-fat diet (HFD) for twelve weeks. Then, mice received two intraperitoneal injections of CORM-3 (10 mg x kg(-1)), with the second one given 16 hours after the first. Contractile function in isolated hearts and mitochondrial parameters were evaluated 24 hours after the last injection. Mitochondrial population was explored by electron microscopy. Changes in mitochondrial dynamics, biogenesis and autophagy were assessed by western-blot and RT-qPCR. Left ventricular developed pressure was reduced in HFD hearts. Mitochondria from HFD hearts presented reduced membrane potential and diminished ADP-coupled respiration. CORM-3 restored both cardiac and mitochondrial functions. Size and number of mitochondria increased in the HFD hearts but not in the CORM-3-treated HFD group. CORM-3 modulated HFD-activated mitochondrial fusion and biogenesis signalling. While autophagy was not activated in the HFD group, CORM-3 increased the autophagy marker LC3-II. Finally, ex vivo experiments demonstrated that autophagy inhibition by 3-methyladenine abolished the cardioprotective effects of CORM-3.

Conclusion: CORM-3 may modulate pathways controlling mitochondrial quality, thus leading to improvements of mitochondrial efficiency and HFD-induced cardiac dysfunction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antimetabolites / pharmacology*
  • Autophagy / drug effects
  • Carbon Monoxide / pharmacology*
  • Dietary Fats / adverse effects
  • Female
  • Heart Diseases* / drug therapy
  • Heart Diseases* / etiology
  • Heart Diseases* / metabolism
  • Heart Diseases* / physiopathology
  • Humans
  • Metabolic Syndrome* / chemically induced
  • Metabolic Syndrome* / drug therapy
  • Metabolic Syndrome* / metabolism
  • Metabolic Syndrome* / physiopathology
  • Mice
  • Mitochondria, Heart / metabolism*
  • Myocardial Contraction / drug effects*
  • Organometallic Compounds / pharmacology*
  • Signal Transduction / drug effects

Substances

  • Antimetabolites
  • Dietary Fats
  • Organometallic Compounds
  • tricarbonylchloro(glycinato)ruthenium(II)
  • Carbon Monoxide

Grants and funding

This work was supported by EA4484– Université Lille 2– Ministère de l’Enseignement Supérieur et de la Recherche; CPER “cardiodiabète 2008” - FEDER Région Nord Pas-de-Calais 08480265; Fondation de France 2009002501 and Fondation Coeur et Artères FCA09T6. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.