Research article
Extraocular, limb and diaphragm muscle group-specific antioxidant enzyme activity patterns in control and mdx mice

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Abstract

The mechanisms primarily responsible for the degenerative processes occurring in dystrophic skeletal muscle remain unresolved. The identification of the mechanisms that lead to the complete sparing of extraocular muscle in dystrophinopathies is of particular interest. A number of studies have provided evidence to suggest that the muscle pathology that characterizes muscular dystrophy may be, in part, free radical mediated. In the present study, we examined the antioxidant enzyme status of extraocular, diaphragm and gastrocnemius muscles in control strain and mdx mice. Our results revealed that in the control strain, both extraocular and diaphragm muscles had higher copper/zinc superoxide dismutase, manganese superoxide dismutase and selenium dependent glutathione peroxidase activities as compared to the gastrocnemius. Furthermore, the diaphragm had higher glutathione reductase activity as compared to the gastrocnemius. These findings indicate that the highly aerobic extraocular and diaphragm muscles have higher antioxidant enzyme capacity than the gastrocnemius, a muscle more dependent on anaerobic energy metabolism. Changes in the antioxidant enzyme status of the mdx mouse correlated, in part, with the degree of histopathological involvement of the three muscle groups assessed.

References (65)

  • H. Hoppeler et al.

    Design of the mammalian respiratory system. VI. Distribution of mitochondria and capillaries in various muscles

    Resp. Physiol.

    (1981)
  • N.C. Kar et al.

    Catalase, superoxide dismutase, glutathione reductase and thiobarbituric reactive products in normal and dystrophic human muscle

    Clin. Chim. Acta

    (1979)
  • B. Ketterer et al.

    Glutathione transferases: a possible role in the detoxication and repair of DNA and lipid hydroperoxides

    Mut. Res.

    (1989)
  • J. Krall et al.

    Superoxide mediates the toxicity of paraquat for cultured mammalian cells

    J. Biol. Chem.

    (1988)
  • R.A. Lawrence et al.

    Hepatic cytosolic non-selenium dependent glutathione peroxidase activity

    J. Nutr.

    (1978)
  • C. Little et al.

    An intracellular glutathione peroxidase with a lipid peroxide substrate

    Biochem. Biophys. Res. Commun.

    (1968)
  • J.M. McCord et al.

    Superoxide dismutase: an enzymatic function for erythrocuprein (hemocuprein)

    J. Biol. Chem.

    (1969)
  • F. Mechler et al.

    Lipid peroxidation and superoxide dismutase activity in muscle and erythrocytes in Duchenne muscular dystrophy

    J. Neurol. Sci.

    (1984)
  • C. Michiels et al.

    Importance of Se-glutathione peroxidase, catalase and Cu/ZnSOD for cell survival against oxidative stress

    Free Radic. Biol. Med.

    (1994)
  • Y. Mizuno

    Glucose-6-phosphate dehydrogenase, 6-phosphogluconate dehydrogenase and glyceraldehyde-3-phosphate dehydrogenase activities in early stages of development in dystrophic chickens

    J. Neurol. Sci.

    (1985)
  • M.E. Murphy et al.

    Activities of antioxidant enzymes in muscle, liver and lung of chickens with inherited muscular dystrophy

    Biochem. Biophys. Res. Commun.

    (1986)
  • S.T. Omaye et al.

    Glutathione peroxidase, glutathione reductase and thiobarbituric reactive products in muscles of chickens and mice with genetic muscular dystrophy

    Life Sci.

    (1974)
  • C. Pastoret et al.

    Mdx mice show progressive weakness and muscle deterioration with age

    J. Neurol. Sci.

    (1995)
  • J.R. Prohaska

    The glutathione peroxidase activity of glutathione-S-transferases

    Biochim. Biophys. Acta

    (1980)
  • J.R. Prohaska et al.

    Glutathione peroxidase activity of glutathione-S-transferases purified from rat liver

    Biochem. Biophys. Res. Commun.

    (1977)
  • C. Shudo et al.

    Effects of efonidipine hydrochloride (NZ-105), a new calcium antagonist, against acute renal failure in rats

    Gen. Pharmacol.

    (1994)
  • D.R. Spitz et al.

    An assay for superoxide dismutase activity in mammalian tissue homogenates

    Anal. Biochem.

    (1989)
  • R.A. Weisiger et al.

    Superoxide dismutase: Organelle specificity

    J. Biol. Chem.

    (1973)
  • R.A. Weisiger et al.

    Mitochondrial superoxide dismutase: Site of synthesis and intramitochondrial localization

    J. Biol. Chem.

    (1973)
  • M. Woo et al.

    Muscle fiber growth and necrosis in dystrophic muscles: a comparative study between dy and mdx mice

    J. Neurol. Sci.

    (1987)
  • K. Asayama et al.

    Lipid peroxide and antioxidant enzymes in muscle and non-muscle of dystrophic mouse

    Muscle Nerve

    (1989)
  • A.J. Bakker et al.

    Calcium levels in myotubes grown from the skeletal muscle of dystrophic (mdx) and normal mice

    J. Physiol. (Lond.)

    (1993)
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