Extracellular superoxide dismutase ameliorates skeletal muscle abnormalities, cachexia, and exercise intolerance in mice with congestive heart failure

Circ Heart Fail. 2014 May;7(3):519-30. doi: 10.1161/CIRCHEARTFAILURE.113.000841. Epub 2014 Feb 12.

Abstract

Background: Congestive heart failure (CHF) is a leading cause of morbidity and mortality, and oxidative stress has been implicated in the pathogenesis of cachexia (muscle wasting) and the hallmark symptom, exercise intolerance. We have previously shown that a nitric oxide-dependent antioxidant defense renders oxidative skeletal muscle resistant to catabolic wasting. Here, we aimed to identify and determine the functional role of nitric oxide-inducible antioxidant enzyme(s) in protection against cardiac cachexia and exercise intolerance in CHF.

Methods and results: We demonstrated that systemic administration of endogenous nitric oxide donor S-nitrosoglutathione in mice blocked the reduction of extracellular superoxide dismutase (EcSOD) protein expression, as well as the induction of MAFbx/Atrogin-1 mRNA expression and muscle atrophy induced by glucocorticoid. We further showed that endogenous EcSOD, expressed primarily by type IId/x and IIa myofibers and enriched at endothelial cells, is induced by exercise training. Muscle-specific overexpression of EcSOD by somatic gene transfer or transgenesis (muscle creatine kinase [MCK]-EcSOD) in mice significantly attenuated muscle atrophy. Importantly, when crossbred into a mouse genetic model of CHF (α-myosin heavy chain-calsequestrin), MCK-EcSOD transgenic mice had significant attenuation of cachexia with preserved whole body muscle strength and endurance capacity in the absence of reduced HF. Enhanced EcSOD expression significantly ameliorated CHF-induced oxidative stress, MAFbx/Atrogin-1 mRNA expression, loss of mitochondria, and vascular rarefaction in skeletal muscle.

Conclusions: EcSOD plays an important antioxidant defense function in skeletal muscle against cardiac cachexia and exercise intolerance in CHF.

Keywords: capillaries; exercise; mitochondria; muscular atrophy; oxidative stress.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antioxidants / physiology
  • Cachexia / physiopathology*
  • Cachexia / prevention & control*
  • Creatine Kinase, MM Form / physiology
  • Disease Models, Animal
  • Exercise Tolerance / physiology*
  • Heart Failure / complications*
  • Heart Failure / physiopathology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Muscle Proteins / physiology
  • Muscle, Skeletal / drug effects
  • Muscle, Skeletal / pathology
  • Muscle, Skeletal / physiopathology*
  • Physical Conditioning, Animal / physiology
  • RNA, Messenger / physiology
  • S-Nitrosoglutathione / pharmacology
  • SKP Cullin F-Box Protein Ligases / physiology
  • Superoxide Dismutase / deficiency
  • Superoxide Dismutase / genetics
  • Superoxide Dismutase / physiology*

Substances

  • Antioxidants
  • Muscle Proteins
  • RNA, Messenger
  • S-Nitrosoglutathione
  • Superoxide Dismutase
  • Fbxo32 protein, mouse
  • SKP Cullin F-Box Protein Ligases
  • Creatine Kinase, MM Form