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Measures of Growth Processes and Myogenesis in Glycolytic and Oxidative Muscle Fibers in Rats after Indirect Electrical Stimulation

We report here a comparative study of activity in signal pathways and gene expression in the red (RGM) and white (WGM) parts of the gastrocnemius muscle in rats after series of short (1 sec) tetanic contractions evoked by stimulation of the motor nerve at a frequency of 100 Hz and an amplitude sufficient to activate all the motor units of the muscle. At 2 h after stimulation, WGM showed more marked increases in the level of ERK1/2 phosphorylation than RGM, though increases in AMPK phosphorylation were no different. Furthermore, the increases in MyoD and myogenin mRNA in WGM were significantly greater than those in RGM, while the effects of stimulation on expression of the IGF-1, MaFbx, and MuRF genes were weak and similar in WGM and RGM. There was also an increase in the content of myostatin mRNA in RGM. Thus, glycolytic muscle fibers in WGM display more marked regulatory hypertrophic-type shifts than the oxidative muscle fibers making up RGM.

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References

  1. 1.

    A. A. Borzykh, D. K. Gainullina, I. V. Kuz’min, et al., “Comparative analysis of gene expression in locomotor muscles and diaphragm in rats,” Ros. Fiziol. Zh., 98, No. 12, 1587–1594 (2012).

    CAS  Google Scholar 

  2. 2.

    D. G. Allen, G. D. Lamb, and H. Westerblad, “Skeletal muscle fatigue: cellular mechanisms,” Physiol. Rev., 88, No. 1, 287–332 (2008).

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    P. H. Atherton, J. M. Higginson, J. Singh, and H. Wackerhage, “Concentrations of signal transduction proteins exercise and insulin responses in rat extensor digitorum longus and soleus muscles,” Mol. Cell Biochem., 261, No. 1–2, 111–116 (2004).

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    M. Badier, C. Guillot, C. Danger, et al., “M-wave changes after highand low-frequency electrically induced fatigue in different muscles,” Muscle Nerve, 22, No. 4, 488–496 (1999).

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    J. D. Bartlett, J. C. Hwa, T. S. Jeong, et al., “Matched work high-intensity interval and continuous running induce similar increases in PGC-Ialpha mRNA, AMPK, p38, and p53 phosphorylation in human skeletal muscle,” J. Appl. Physiol., 112, 1135–1143 (2012).

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    S. M. Baylor and S. Hollingworth, “Intracellular calcium movements during excitation-contraction coupling in mammalian slowtwitch and fast-twitch muscle fibers,” J. Gen. Physiol., 139, No. 4, 261–272 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. 7.

    D. Bloemberg and J. Quadrilatero, “Rapid determination of myosin heavy chain expression in rat, mouse, and human skeletal muscle using multicolor immunofluorescence analysis,” PLoS One, 7, No. 4, e35273–e35284 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

    C. J. Carlson, F. W. Booth, and S. E. Gordon, “Skeletal muscle myostatin mRNA expression is fiber-type specific and increases during hindlimb unloading,” Am. J. Physiol., 277, No. 2, R601–R606 (1999).

    CAS  PubMed  Google Scholar 

  9. 9.

    N. M. Cermak, T. Snijders, B. R. McKay, et al., “Eccentric exercise increases satellite cell content in type II muscle fibers,” J. Med. Sci. Sports Exerc., 45, No. 2, 230–237 (2013).

    Article  Google Scholar 

  10. 10.

    M. D. Delp and C. Duan, “Composition and size of type I, IIA, IID/X, and IIB fibers and citrate synthase activity of rat muscle,” J. Appl. Physiol., 80, No. 1, 261–270 (1996).

    CAS  PubMed  Google Scholar 

  11. 11.

    V. C. Foletta, L. J. White, A. E. Larsen, et al., “The role and regulation of MAFbx/atrogin-1 and MuRF1 in skeletal muscle atrophy,” Pflügers Arch., 461, No. 3, 325–335 (2011).

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    E. L. Glynn, C. S. Fry, M. J. Drummond, et al., “Muscle protein breakdown has a minor role in the protein anabolic response to essential amino acid and carbohydrate intake following resistance exercise,” Am. J. Physiol. Regul. Integr. Comp. Physiol., 299, No. 2, R533–R540 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. 13.

    M. D. Gomes, S. H. Lecker, R. T. Jagoe, et al., “Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy,” Proc. Natl. Acad. Sci. USA, 98, No. 25, 14,440–14,445 (2001).

    CAS  Article  Google Scholar 

  14. 14.

    K. Gundersen, “Excitation-transcription coupling in skeletal muscle: the molecular pathways of exercise,” Biol. Rev. Camb. Philos. Soc., 86, No. 3, 564–600 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  15. 15.

    K. M. Heinemeier, J. L. Olesen, F. Haddad, et al., “Effect of unloading followed by reloading on expression of collagen and related growth factors in rat tendon and muscle,” J. Appl. Physiol., 106, No. 1, 178–186 (2009).

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    S. M. Hughes, J. M. Taylor, S. J. Tapscott, et al., “Selective accumulation of MyoD and myogenin mRNAs in fast and slow adult skeletal muscle is controlled by innervation and hormones,” Development, 118, No. 4, 1137–1147 (1993).

    CAS  PubMed  Google Scholar 

  17. 17.

    E. Hultman and P. L. Greenhaff, “Skeletal muscle energy metabolism and fatigue during intense exercise in man,” Sci. Prog., 75, No. 298, 361–370 (1991).

    CAS  PubMed  Google Scholar 

  18. 18.

    M. Ishido, K. Kami, and M. Masuhara, “Localization of MyoD, myogenin and cell cycle regulatory factors in hypertrophying rat skeletal muscles,” Acta Physiol. Scand., 180, No. 3, 281–289 (2004).

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    M. Karalaki, S. Fili, A. Philippou, and M. Koutsilieris, “Muscle regeneration: cellular and molecular events,” In Vivo, 23, No. 5, 779–796 (2009).

    CAS  PubMed  Google Scholar 

  20. 20.

    I. Kim, D. Yang, X. Tang, and J. L. Carroll, “Reference gene validation for qPCR in rat carotid body during postnatal development,” BMC Res. Notes, 4, 440–448 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. 21.

    B. J. Krawiec, G. J. Nystrom, R. A. Frost, et al., “AMP-activated protein kinase agonists increase mRNA content of the muscle-specific ubiquitin ligases MAFbx and MuRF1 in C2C12 cells,” Am. J. Physiol. Endocrinol. Metab., 292, No. 6, E1555–E1567 (2007).

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    R. S. Lee-Young, B. J. Canny, D. E. Myers, and G. K. McDonnell, “AMPK activation is fiber type specific in human skeletal muscle: effects of exercise and short-term exercise training,” J. Appl. Physiol., 107, No. 1, 283–289 (2009).

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    B. R. MacIntosh, S. P. Esau, R. J. Holash, and J. R. Fletcher, “Procedures for rat in situ skeletal muscle contractile properties,” J. Vis. Exp., 56, e3167 (2011).

    Google Scholar 

  24. 24.

    A. Matsakas, C. Bozzo, N. Cacciani, et al., “Effect of swimming on myostatin expression in white and red gastrocnemius muscle and in cardiac muscle of rats,” Exp. Physiol., 6, 983–994 (2006).

    Article  Google Scholar 

  25. 25.

    T. Moritani, M. Muro, and A. Kijima, “Electromechanical changes during electrically induced and maximal voluntary contractions: electrophysiologic responses of different muscle fiber types during stimulated contractions,” Exp. Neurol., 88, No. 3, 471–483 (1985).

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    G. A. Nader and K. A. Esser, “Intracellular signaling specificity in skeletal muscle in response to different modes of exercise,” J. Appl. Physiol. (1985), 90, No. 5, 1936–1942 (2001).

    CAS  PubMed  Google Scholar 

  27. 27.

    A. S. Pimenta, R. H. Lambertucci, R. Gorjão, et al., “Effect of a single session of electrical stimulation on activity and expression of citrate synthase and antioxidant enzymes in rat soleus muscle,” Eur. J. Appl. Physiol. 102, No. 1, 119–126 (2007).

    Article  Google Scholar 

  28. 28.

    D. Popov, R. Zinovkin, E. Karger, et al., “Effects of continuous and intermittent aerobic exercise upon mRNA expression of metabolic genes in human skeletal muscle,” J. Sports Med. Phys. Fitness, 54, No. 3, 362–369 (2014).

    CAS  PubMed  Google Scholar 

  29. 29.

    A. C. Ronda, A. Vasconsuelo, and R. Boland, “Extracellular-regulated kinase and p38 mitogen-activated protein kinases are involved in the antiapoptotic action of 17beta-estradiol in skeletal muscle cells,” J. Endocrinol., 206, No. 2, 235–246 (2010).

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    D. G. Sale, “Influence of exercise and training on motor unit activation,” Exerc. Sport Sci. Rev., 15, 95–151 (1987).

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    H. Shi, J. M. Scheffler, J. M. Pleitner, et al., “Modulation of skeletal muscle fiber type by mitogen-activated protein kinase signaling,” FASEB J., 22, No. 8, 2990–3000 (2008).

    CAS  Article  PubMed  Google Scholar 

  32. 32.

    A. Tsutaki, R. Ogasawara, K. Kobayashi, et al., “Effect of intermittent low-frequency electrical stimulation on the rat gastrocnemius muscle,” Biomed. Res. Int., 2013, 480620 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    T. Van Wessel, A. de Haan, W. J. van der Laarse, and R. T. Jaspers, “The muscle fiber type-fiber size paradox: hypertrophy or oxidative metabolism?” Eur. J. Appl. Physiol., 110, No. 4, 665–694 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    C. Wretman, U. Widegren, A. Lionikas, et al., “Differential activation of mitogen-activated protein kinase signalling pathways by isometric contractions in isolated slow- and fast-twitch rat skeletal muscle,” Acta Physiol. Scand., 70, No. 1, 45–49 (2000).

    Article  Google Scholar 

  35. 35.

    X. Yang, A. Wei, Y. Liu, et al., “IGF-1 protects retinal ganglion cells from hypoxia-induced apoptosis by activating the Erk-1/2 and Akt pathways,” Mol. Vis., 19, 1901–1912 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. 36.

    N. Zanou and P. Gailly, “Skeletal muscle hypertrophy and regeneration: interplay between the myogenic regulatory factors (MRFs) and insulin-like growth factors (IGFs) pathways,” Cell Mol. Life Sci., 70, No. 21, 4117–4130 (2013).

    CAS  Article  PubMed  Google Scholar 

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Correspondence to A. A. Borzykh.

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Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 101, No. 11, pp. 1289–1298, November, 2015.

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Borzykh, A.A., Kuz’min, I.V., Lysenko, E.A. et al. Measures of Growth Processes and Myogenesis in Glycolytic and Oxidative Muscle Fibers in Rats after Indirect Electrical Stimulation. Neurosci Behav Physi 47, 352–358 (2017). https://doi.org/10.1007/s11055-017-0404-4

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Keywords

  • rat
  • gastrocnemius muscle
  • glycolytic and oxidative muscle fibers
  • ERK1/2
  • MyoD
  • myogenin
  • myostatin