Activation of Ca(2+)-dependent protein kinase II during repeated contractions in single muscle fibres from mouse is dependent on the frequency of sarcoplasmic reticulum Ca(2+) release

Acta Physiol (Oxf). 2007 Oct;191(2):131-7. doi: 10.1111/j.1748-1716.2007.01725.x. Epub 2007 Jun 12.

Abstract

Aim: To investigate the importance and contribution of calmodulin-dependent protein kinase II (CaMKII) activity on sarcoplasmic reticulum (SR) Ca(2+)-release in response to different work intensities in single, intact muscle fibres.

Methods: CaMKII activity was blocked in single muscle fibres using either the inhibitory peptide AC3-I or the pharmacological inhibitor KN-93. The effect on tetanic force production and [Ca(2+)](i) was determined during work of different intensities. The activity of CaMKII was assessed by mathematical modelling.

Results: Using a standard protocol to induce fatigue (50x 70 Hz, 350 ms duration, every 2 s) the number of stimuli needed to induce fatigue was decreased from 47 +/- 3 contractions in control to 33 +/- 3 with AC3-I. KN-93 was a more potent inhibitor, decreasing the number of contractions needed to induce fatigue to 15 +/- 3. Tetanic [Ca(2+)](i) was 100 +/- 11%, 97 +/- 11% and 67 +/- 11% at the end of stimulation in control, AC3-I and KN-93 respectively. A similar inhibition was obtained using a high intensity protocol (20x 70 Hz, 200 ms duration, every 300 ms). However, using a long interval protocol (25x 70 Hz, 350 ms duration, every 5 s) no change was observed in either tetanic [Ca(2+)](i) or force when inhibiting CaMKII. A mathematical model used to investigate the activation pattern of CaMKII suggests that there is a threshold of active CaMKII that has to be surpassed in order for CaMKII to affect SR Ca(2+) release.

Conclusion: Our results show that CaMKII is crucial for maintaining proper SR Ca(2+) release and that this is regulated in a work intensity manner.

MeSH terms

  • Animals
  • Benzylamines / pharmacology
  • Calcium / metabolism*
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / antagonists & inhibitors
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism*
  • Enzyme Activation
  • In Vitro Techniques
  • Male
  • Mice
  • Mice, Inbred Strains
  • Models, Biological
  • Muscle Contraction / physiology*
  • Muscle Fatigue / physiology
  • Muscle Fibers, Skeletal / metabolism
  • Muscle Fibers, Skeletal / physiology*
  • Peptides / pharmacology
  • Protein Kinase Inhibitors / pharmacology
  • Sarcoplasmic Reticulum / metabolism*
  • Sulfonamides / pharmacology

Substances

  • AC3-I peptide
  • Benzylamines
  • Peptides
  • Protein Kinase Inhibitors
  • Sulfonamides
  • KN 93
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcium