Contraction-mediated glycogenolysis in mouse skeletal muscle lacking creatine kinase: the role of phosphorylase b activation

J Physiol. 2003 Dec 1;553(Pt 2):523-31. doi: 10.1113/jphysiol.2003.051078. Epub 2003 Sep 8.

Abstract

Skeletal muscle that is deficient in creatine kinase (CK-/-) exhibits accelerated glycogenolysis during contraction. Understanding this phenomenon could provide insight into the control of glycogenolysis during contraction. Therefore, glycogen breakdown was investigated in isolated extensor digitorum longus CK-/- muscle. Muscles were stimulated to produce repeated tetani for 20 s in the presence of sodium cyanide to block mitochondrial respiration. Accumulation of lactate after stimulation was similar in wild-type (WT) and CK-/- muscles, whereas accumulation of glucose-6-phosphate was twofold higher in CK-/- muscles, indicating greater glycogenolysis in CK-/- muscles. Total phosphorylase activity was decreased by almost 30 % in CK-/- muscle (P < 0.001). Phosphorylase fractional activity (-/+ 3.3 mM AMP) was similar in both groups in the basal state (about 10 %), but increased to a smaller extent in CK-/- muscles after stimulation (39 +/- 4 % vs. 52 +/- 4 % in WT, P < 0.05). Inorganic phosphate, the substrate for phosphorylase, increased marginally in CK-/- muscles after stimulation (basal = 25.3 +/- 2.2 micromol (g dry muscle)-1; stimulated = 33.9 +/- 2.3 micromol (g dry muscle)-1), but substantially in WT muscles (basal = 11.4 +/- 0.7 micromol (g dry muscle)-1; stimulated = 54.2 +/- 4.5 micromol (g dry muscle)-1). Kinetic studies of phosphorylase b (dephosphorylated enzyme) from muscle extracts in vitro demonstrated higher relative activities in CK-/- muscles (60-135 %) in response to low AMP concentrations (up to 50 microM) in both the basal state and after stimulation (P < 0.05), whereas no differences in activity between CK-/- and WT muscles were observed at high AMP concentrations (> 100 microM). These data indicate that allosteric activation of phosphorylase b accounts for the accelerated glycogenolysis in CK-/- muscle during contraction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Diphosphate / metabolism
  • Adenosine Monophosphate / metabolism
  • Adenosine Monophosphate / pharmacology
  • Adenosine Triphosphate / metabolism
  • Animals
  • Creatine / metabolism
  • Creatine Kinase / genetics*
  • Electric Stimulation
  • Enzyme Activation / drug effects
  • Glucose-6-Phosphate / metabolism
  • Glycogen / metabolism*
  • Glycogen Phosphorylase / metabolism
  • Glycogen Synthase / metabolism
  • In Vitro Techniques
  • Inosine / metabolism
  • Inosine Monophosphate / metabolism
  • Lactic Acid / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Muscle Contraction / physiology*
  • Muscle Fatigue / physiology
  • Muscle, Skeletal / metabolism*
  • Phosphocreatine / metabolism
  • Phosphorylase a / metabolism
  • Phosphorylase b / metabolism*
  • Sodium Cyanide / pharmacology

Substances

  • Phosphocreatine
  • Inosine Monophosphate
  • Lactic Acid
  • Adenosine Monophosphate
  • Glucose-6-Phosphate
  • Inosine
  • Adenosine Diphosphate
  • Adenosine Triphosphate
  • Glycogen
  • Glycogen Phosphorylase
  • Phosphorylase a
  • Phosphorylase b
  • Glycogen Synthase
  • Creatine Kinase
  • Creatine
  • Sodium Cyanide