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BioMed Research International
Volume 2014 (2014), Article ID 943806, 20 pages
http://dx.doi.org/10.1155/2014/943806
Research Article

Muscle-Type Specific Autophosphorylation of CaMKII Isoforms after Paced Contractions

1School of HealthCare Science, Institute for Biomedical Research into Human Movement and Health, Manchester Metropolitan University, Manchester M1 5GD, UK
2Laboratory for Myology, Faculty of Human Movement Sciences, MOVE Research Institute Amsterdam, VU University Amsterdam, 1081 BT Amsterdam, The Netherlands
3Department of Biomedical Engineering, Eindhoven University of Technology, 5612 AZ Eindhoven, The Netherlands
4Laboratory for Muscle Plasticity, Department of Orthopedics, University of Zurich, Balgrist University Hospital, Forchstrasse 340, 8008 Zurich, Switzerland

Received 6 May 2014; Accepted 27 May 2014; Published 26 June 2014

Academic Editor: Calvin Yu-Chian Chen

Copyright © 2014 Wouter Eilers et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Hennig and T. Lomo, “Firing patterns of motor units in normal rats,” Nature, vol. 314, no. 6007, pp. 164–166, 1985. View at Google Scholar · View at Scopus
  2. M. E. Anderson, “Connections count: excitation-contraction meets excitation-transcription coupling,” Circulation Research, vol. 86, no. 7, pp. 717–719, 2000. View at Google Scholar · View at Scopus
  3. S. Schiaffino and A. L. Serrano, “Calcineurin signaling and neural control of skeletal muscle fiber type and size,” Trends in Pharmacological Sciences, vol. 23, no. 12, pp. 569–575, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. M. W. Berchtold, H. Brinkmeier, and M. Müntener, “Calcium ion in skeletal muscle: its crucial role for muscle function, plasticity, and disease,” Physiological Reviews, vol. 80, no. 3, pp. 1215–1265, 2000. View at Google Scholar · View at Scopus
  5. M. Brini, T. Cali, D. Ottolini, and E. Carafoli, “Intracellular calcium homeostasis and signaling,” in Metallomics and the Cell, vol. 12 of Metal Ions in Life Sciences, pp. 119–168, 2013. View at Publisher · View at Google Scholar
  6. S. Schiaffino and C. Reggiani, “Fiber types in mammalian skeletal muscles,” Physiological Reviews, vol. 91, no. 4, pp. 1447–1531, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. E. R. Chin, “Role of Ca2+/calmodulin-dependent kinases in skeletal muscle plasticity,” Journal of Applied Physiology, vol. 99, no. 2, pp. 414–423, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. D. Kernell, O. Eerbeek, B. A. Verhey, and Y. Donselaar, “Effects of physiological amounts of high- and low-rate chronic stimulation on fast-twitch muscle of the cat hindlimb. I. Speed- and force-related properties,” Journal of Neurophysiology, vol. 58, no. 3, pp. 598–613, 1987. View at Google Scholar · View at Scopus
  9. A. de Haan, C. J. de Ruiter, A. Lind, and A. J. Sargeant, “Age-related changes in force and efficiency in rat skeletal muscle,” Acta Physiologica Scandinavica, vol. 147, no. 4, pp. 347–355, 1993. View at Google Scholar · View at Scopus
  10. K. Gundersen, E. Leberer, T. Lomo, D. Pette, and R. S. Staron, “Fibre types, calcium-sequestering proteins and metabolic enzymes in denervated and chronically stimulated muscles of the rat,” Journal of Physiology, vol. 398, pp. 177–189, 1988. View at Google Scholar · View at Scopus
  11. B. R. Eisenberg, D. J. Dix, Z. W. Lin, and M. P. Wenderoth, “Relationship of membrane systems in muscle to isomyosin content,” Canadian Journal of Physiology and Pharmacology, vol. 65, no. 4, pp. 598–605, 1987. View at Google Scholar · View at Scopus
  12. A. J. Rose, T. J. Alsted, J. B. Kobberø, and E. A. Richter, “Regulation and function of Ca2+-calmodulin-dependent protein kinase II of fast-twitch rat skeletal muscle,” Journal of Physiology, vol. 580, no. 3, pp. 993–1005, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. K.-U. Bayer, K. Harbers, and H. Schulman, “αKAP is an anchoring protein for a novel CaM kinase II isoform in skeletal muscle,” EMBO Journal, vol. 17, no. 19, pp. 5598–5605, 1998. View at Publisher · View at Google Scholar · View at Scopus
  14. P. Tavi and H. Westerblad, “The role of in vivo Ca2+ signals acting on Ca2+-calmodulin-dependent proteins for skeletal muscle plasticity,” Journal of Physiology, vol. 589, no. 21, pp. 5021–5031, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Hudmon and H. Schulman, “Structure-function of the multifunctional Ca2+/calmodulin-dependent protein kinase II,” Biochemical Journal, vol. 364, no. 3, pp. 593–611, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. J. J. Saucerman and D. M. Bers, “Calmodulin mediates differential sensitivity of CaMKII and calcineurin to local Ca2+ in cardiac myocytes,” Biophysical Journal, vol. 95, no. 10, pp. 4597–4612, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. J. M. Bradshaw, Y. Kubota, T. Meyer, and H. Schulman, “An ultrasensitive Ca2+/calmodulin-dependent protein kinase II-protein phosphatase 1 switch facilitates specificity in postsynaptic calcium signaling,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 18, pp. 10512–10517, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Flück, M. N. Waxham, M. T. Hamilton, and F. W. Booth, “Skeletal muscle Ca2+-independent kinase activity increases during either hypertrophy or running,” Journal of Applied Physiology, vol. 88, no. 1, pp. 352–358, 2000. View at Google Scholar · View at Scopus
  19. G. Dupont and A. Goldbeter, “CaM kinase II as frequency decoder of Ca2+ oscillations,” BioEssays, vol. 20, no. 8, pp. 607–610, 1998. View at Google Scholar
  20. T. R. Gaertner, S. J. Kolodziej, D. Wang et al., “Comparative analyses of the three-dimensional structures and enzymatic properties of α, β, γ, and δ isoforms of Ca2+-calmodulin-dependent protein kinase II,” Journal of Biological Chemistry, vol. 279, no. 13, pp. 12484–12494, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. L. S. Maier, “Ca2+/calmodulin-dependent protein kinase II (CaMKII) in the heart,” Advances in Experimental Medicine and Biology, vol. 740, pp. 685–702, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. L. S. Maier, “CaMKIIδ overexpression in hypertrophy and heart failure: cellular consequences for excitation-contraction coupling,” Brazilian Journal of Medical and Biological Research, vol. 38, no. 9, pp. 1293–1302, 2005. View at Google Scholar · View at Scopus
  23. C. Li, X. Cai, H. Sun et al., “The δA isoform of calmodulin kinase II mediates pathological cardiac hypertrophy by interfering with the HDAC4-MEF2 signaling pathway,” Biochemical and Biophysical Research Communications, vol. 409, no. 1, pp. 125–130, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. P. De Koninck and H. Schulman, “Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations,” Science, vol. 279, no. 5348, pp. 227–230, 1998. View at Publisher · View at Google Scholar · View at Scopus
  25. H. Fujii, M. Inoue, H. Okuno et al., “Nonlinear decoding and asymmetric representation of neuronal input information by CaMKIIα and calcineurin,” Cell Reports, vol. 3, no. 4, pp. 978–987, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. L. Li, M. I. Stefan, and N. Le Novère, “Calcium input frequency, duration and amplitude differentially modulate the relative activation of calcineurin and CaMKII,” PLoS ONE, vol. 7, no. 9, Article ID e43810, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Carroll, P. Nicotera, and D. Pette, “Calcium transients in single fibers of low-frequency stimulated fast- twitch muscle of rat,” American Journal of Physiology: Cell Physiology, vol. 277, no. 6, pp. C1122–C1129, 1999. View at Google Scholar · View at Scopus
  28. C. J. De Ruiter, A. De Haan, and A. J. Sargeant, “Physiological characteristics of two extreme muscle compartments in gastrocnemius medialis of the anaesthetized rat,” Acta Physiologica Scandinavica, vol. 153, no. 4, pp. 313–324, 1995. View at Google Scholar · View at Scopus
  29. W. Groenendaal, J. A. L. Jeneson, P. J. Verhoog et al., “Computational modelling identifies the impact of subtle anatomical variations between amphibian and mammalian skeletal muscle on spatiotemporal calcium dynamics,” IET Systems Biology, vol. 2, no. 6, pp. 411–422, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. Z. Zi, K.-H. Cho, M.-H. Sung, X. Xia, J. Zheng, and Z. Sun, “In silico identification of the key components and steps in IFN-γ induced JAK-STAT signaling pathway,” FEBS Letters, vol. 579, no. 5, pp. 1101–1108, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Vanlier, C. A. Tiemann, P. A. J. Hilbers, and N. A. W. van Riel, “Parameter uncertainty in biochemical models described by ordinary differential equations,” Mathematical Biosciences, vol. 246, no. 2, pp. 305–314, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. R. Bottinelli, “Functional heterogeneity of mammalian single muscle fibres: do myosin isoforms tell the whole story?” Pflugers Archiv European Journal of Physiology, vol. 443, no. 1, pp. 6–17, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. N. Narayanan and A. Xu, “Phosphorylation and regulation of the Ca2+-pumping ATPase in cardiac sarcoplasmic reticulum by calcium/calmodulin-dependent protein kinase,” Basic Research in Cardiology, vol. 92, supplement 1, pp. 25–35, 1997. View at Google Scholar · View at Scopus
  34. X. Mu, L. D. Brown, Y. Liu, and M. F. Schneider, “Roles of the calcineurin and CaMK signaling pathways in fast-to-slow fiber type transformation of cultured adult mouse skeletal muscle fibers,” Physiological Genomics, vol. 30, no. 3, pp. 300–312, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Philippi and A. H. Sillau, “Oxidative capacity distribution in skeletal muscle fibers of the rat,” Journal of Experimental Biology, vol. 189, pp. 1–11, 1994. View at Google Scholar · View at Scopus
  36. S. M. Baylor and S. Hollingworth, “Model of sarcomeric Ca2+ movements, including ATP Ca2+ binding and diffusion, during activation of frog skeletal muscle,” Journal of General Physiology, vol. 112, no. 3, pp. 297–316, 1998. View at Publisher · View at Google Scholar · View at Scopus
  37. T. J. Hund and Y. Rudy, “Rate dependence and regulation of action potential and calcium transient in a canine cardiac ventricular cell model,” Circulation, vol. 110, no. 20, pp. 3168–3174, 2004. View at Publisher · View at Google Scholar · View at Scopus