Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2017, Article ID 5695217, 8 pages
https://doi.org/10.1155/2017/5695217
Research Article

Electrical Stimulation of Denervated Rat Skeletal Muscle Retards Capillary and Muscle Loss in Early Stages of Disuse Atrophy

1Institute for Human Movement and Medical Sciences, Niigata University of Health and Welfare, Niigata, Japan
2National Institute of Fitness and Sports in Kanoya, Kanoya, Japan
3Niigata Rehabilitation Hospital, Niigata, Japan

Correspondence should be addressed to Hiroyuki Tamaki; pj.ca.whun@ikamat-ikuyorih

Received 8 January 2017; Accepted 29 March 2017; Published 13 April 2017

Academic Editor: Leonardo F. Ferreira

Copyright © 2017 Kouki Nakagawa 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. S. C. Bodine-Fowler, S. Allsing, and M. J. Botte, “Time course of muscle atrophy and recovery following a phenol-induced nerve block,” Muscle and Nerve, vol. 19, no. 4, pp. 497–504, 1996. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Ishido, K. Kami, and M. Masuhara, “In vivo expression patterns of MyoD, p21, and Rb proteins in myonuclei and satellite cells of denervated rat skeletal muscle,” American Journal of Physiology—Cell Physiology, vol. 287, no. 2, pp. C484–C493, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. R. R. Roy, H. Zhong, B. Siengthai, and V. Reggie Edgerton, “Activity-dependent influences are greater for fibers in rat medial gastrocnemius than tibialis anterior muscle,” Muscle and Nerve, vol. 32, no. 4, pp. 473–482, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Fujino, H. Kondo, F. Nagatomo, and A. Ishihara, “Capillary growth and regression in skeletal muscle,” The Journal of Physical Fitness and Sports Medicine, vol. 3, no. 5, pp. 483–491, 2014. View at Publisher · View at Google Scholar
  5. K. Tyml, O. Mathieu-Costello, L. Cheng, and E. G. Noble, “Differential microvascular response to disuse in rat hindlimb skeletal muscles,” Journal of Applied Physiology, vol. 87, no. 4, pp. 1496–1505, 1999. View at Google Scholar · View at Scopus
  6. A. Wagatsuma, H. Tamaki, and F. Ogita, “Capillary supply and gene expression of angiogenesis-related factors in murine skeletal muscle following denervation,” Experimental Physiology, vol. 90, no. 3, pp. 403–409, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. U. Carraro, K. Rossini, W. Mayr, and H. Kern, “Muscle fiber regeneration in human permanent lower motoneuron denervation: relevance to safety and effectiveness of FES-training, which induces muscle recovery in SCI subjects,” Artificial Organs, vol. 29, no. 3, pp. 187–191, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. H. Kern, S. Salmons, W. Mayr, K. Rossini, and U. Carraro, “Recovery of long-term denervated human muscles induced by electrical stimulation,” Muscle and Nerve, vol. 31, no. 1, pp. 98–101, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Mödlin, C. Forstner, C. Hofer et al., “Electrical stimulation of denervated muscles: first results of a clinical study,” Artificial Organs, vol. 29, no. 3, pp. 203–206, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. J. E. Stevens-Lapsley, J. E. Balter, P. Wolfe, D. G. Eckhoff, and W. M. Kohrt, “Early neuromuscular electrical stimulation to improve quadriceps muscle strength after total knee arthroplasty: a randomized controlled trial,” Physical Therapy, vol. 92, no. 2, pp. 210–226, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. D. Gigo-Benato, T. L. Russo, S. Geuna, N. R. S. R. Domingues, T. F. Salvini, and N. A. Parizotto, “Electrical stimulation impairs early functional recovery and accentuates skeletal muscle atrophy after sciatic nerve crush injury in rats,” Muscle and Nerve, vol. 41, no. 5, pp. 685–693, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. C. M. Pinheiro-Dardis and T. L. Russo, “Electrical stimulation based on chronaxie increases fibrosis and modulates TWEAK/Fn14, TGF-β/myostatin, and MMP pathways in denervated muscles,” American Journal of Physical Medicine & Rehabilitation, vol. 96, no. 4, pp. 260–267, 2017. View at Publisher · View at Google Scholar
  13. K. Tomori, Y. Ohta, T. Nishizawa, H. Tamaki, and H. Takekura, “Low-intensity electrical stimulation ameliorates disruption of transverse tubules and neuromuscular junctional architecture in denervated rat skeletal muscle fibers,” Journal of Muscle Research and Cell Motility, vol. 31, no. 3, pp. 195–205, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. A.-C. D. Salter, F. J. R. Richmond, and G. E. Loeb, “Effects of muscle immobilization at different lengths on tetrodotoxin-induced disuse atrophy,” IEEE Transactions on Neural Systems and Rehabilitation Engineering, vol. 11, no. 3, pp. 209–217, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. N. Fujita, S. Murakami, T. Arakawa, A. Miki, and H. Fujino, “The combined effect of electrical stimulation and resistance isometric contraction on muscle atrophy in rat tibialis anterior muscle,” Bosnian Journal of Basic Medical Sciences, vol. 11, no. 2, pp. 74–79, 2011. View at Google Scholar · View at Scopus
  16. H. Tamaki, K. Tomori, K. Yotani et al., “Electrical stimulation of denervated rat skeletal muscle retards trabecular bone loss in early stages of disuse musculoskeletal atrophy,” Journal of Musculoskeletal Neuronal Interactions, vol. 14, no. 2, pp. 220–228, 2014. View at Google Scholar · View at Scopus
  17. X. Chen and Y. Li, “Role of matrix metalloproteinases in skeletal muscle: migration, differentiation, regeneration and fibrosis,” Cell Adhesion & Migration, vol. 3, no. 4, pp. 337–341, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. S. A. Olenich, N. Gutierrez-Reed, G. N. Audet, and M. I. Olfert, “Temporal response of positive and negative regulators in response to acute and chronic exercise training in mice,” Journal of Physiology, vol. 591, no. 20, pp. 5157–5169, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. Q. X. A. Sang, “Complex role of matrix metalloproteinases in angiogenesis,” Cell Research, vol. 8, no. 3, pp. 171–177, 1998. View at Publisher · View at Google Scholar · View at Scopus
  20. H. W. Schnaper, D. S. Grant, W. G. Stetler‐Stevenson et al., “Type IV collagenase(s) and TIMPs modulate endothelial cell morphogenesis in vitro,” Journal of Cellular Physiology, vol. 156, no. 2, pp. 235–246, 1993. View at Publisher · View at Google Scholar · View at Scopus
  21. D. Miyazaki, A. Nakamura, K. Fukushima, K. Yoshida, S. Takeda, and S.-I. Ikeda, “Matrix metalloproteinase-2 ablation in dystrophin-deficient mdx muscles reduces angiogenesis resulting in impaired growth of regenerated muscle fibers,” Human Molecular Genetics, vol. 20, no. 9, pp. 1787–1799, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. G. Lluri and D. M. Jaworski, “Regulation of TIMP-2, MT1-MMP, and MMP-2 expressioN during C2C12 differentiation,” Muscle and Nerve, vol. 32, no. 4, pp. 492–499, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Zimowska, E. Brzoska, M. Swierczynska, W. Streminska, and J. Moraczewski, “Distinct patterns of MMP-9 and MMP-2 activity in slow and fast twitch skeletal muscle regeneration in vivo,” International Journal of Developmental Biology, vol. 52, no. 2-3, pp. 307–314, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Z. Reznick, O. Menashe, M. Bar-Shai, R. Coleman, and E. Carmeli, “Expression of matrix metalloproteinases, inhibitor, and acid phosphatase in muscles of immobilized hindlimbs of rats,” Muscle and Nerve, vol. 27, no. 1, pp. 51–59, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. T. L. Russo, S. M. Peviani, J. L. Q. Durigan, and T. Fátima Salvini, “Electrical stimulation increases matrix metalloproteinase-2 gene expression but does not change its activity in denervated rat muscle,” Muscle and Nerve, vol. 37, no. 5, pp. 593–600, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. S. M. Peviani, T. L. Russo, J. L. Q. Durigan et al., “Stretching and electrical stimulation regulate the metalloproteinase-2 in rat denervated skeletal muscle,” Neurological Research, vol. 32, no. 8, pp. 891–896, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. E. Carmeli, M. Moas, S. Lennon, and S. K. Powers, “High intensity exercise increases expression of matrix metalloproteinases in fast skeletal muscle fibres,” Experimental Physiology, vol. 90, no. 4, pp. 613–619, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. T. L. Haas, M. Milkiewicz, S. J. Davis et al., “Matrix metalloproteinase activity is required for activity-induced angiogenesis in rat skeletal muscle,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 279, no. 4, pp. H1540–H1547, 2000. View at Google Scholar · View at Scopus
  29. J. Charan and N. D. Kantharia, “How to calculate sample size in animal studies?” Journal of Pharmacology and Pharmacotherapeutics, vol. 4, no. 4, pp. 303–306, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. G. Kerckhofs, M. Durand, R. Vangoitsenhoven et al., “Changes in bone macro- and microstructure in diabetic obese mice revealed by high resolution microfocus X-ray computed tomography,” Scientific Reports, vol. 6, article 35517, 2016. View at Publisher · View at Google Scholar
  31. H. Tamaki, K. Yotani, F. Ogita et al., “Electrical stimulation of denervated rat skeletal muscle ameliorates bone fragility and muscle loss in early-stage disuse musculoskeletal atrophy,” Calcified Tissue International, vol. 100, no. 4, pp. 420–430, 2017. View at Google Scholar
  32. H. Sakakima, S. Kawamata, S. Kai, J. Ozawa, and N. Matsuura, “Effects of short-term denervation and subsequent reinnervation on motor endplates and the soleus muscle in the rat,” Archives of Histology and Cytology, vol. 63, no. 5, pp. 495–506, 2000. View at Publisher · View at Google Scholar · View at Scopus
  33. H. Sakakima, Y. Yoshida, N. Morimoto, and K. Sakae, “The effect of denervation and subsequent reinnervation on the morphology of rat soleus muscles,” Journal of Physical Therapy Science, vol. 14, no. 1, pp. 21–26, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Takekura, H. Tamaki, T. Nishizawa, and N. Kasuga, “Plasticity of the transverse tubules following denervation and subsequent reinnervation in rat slow and fast muscle fibres,” Journal of Muscle Research and Cell Motility, vol. 24, no. 7, pp. 439–451, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. H. Tamaki, K. Yotani, F. Ogita et al., “Changes over time in structural plasticity of trabecular bone in rat tibiae immobilized by reversible sciatic denervation,” Journal of Musculoskeletal Neuronal Interactions, vol. 13, no. 3, pp. 251–258, 2013. View at Google Scholar · View at Scopus
  36. H. Tamaki, K. Yotani, F. Ogita et al., “Effect of electrical stimulation-induced muscle force and streptomycin treatment on muscle and trabecular bone mass in early-stage disuse musculoskeletal atrophy,” Journal of Musculoskeletal Neuronal Interactions, vol. 15, no. 3, pp. 270–278, 2015. View at Google Scholar · View at Scopus
  37. K. Tomori, R. Kobayashi, T. Koseki, and Y. Ohta, “Effect of neuromuscular electrical stimulation of denervated muscle on the mRNA expression of IGFs in rat skeletal muscle and sciatic nerve,” Journal of Physical Therapy Science, vol. 21, no. 3, pp. 269–273, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. F. N. Daussin, J. Zoll, S. P. Dufour et al., “Effect of interval versus continuous training on cardiorespiratory and mitochondrial functions: Relationship to aerobic performance improvements in sedentary subjects,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 295, no. 1, pp. R264–R272, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. R. E. Andrews, K. M. Shah, J. M. Wilkinson, and A. Gartland, “Effects of cobalt and chromium ions at clinically equivalent concentrations after metal-on-metal hip replacement on human osteoblasts and osteoclasts: implications for skeletal health,” Bone, vol. 49, no. 4, pp. 717–723, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. B.-T. Zhang, S. S. Yeung, Y. Liu et al., “The effects of low frequency electrical stimulation on satellite cell activity in rat skeletal muscle during hindlimb suspension,” BMC Cell Biology, vol. 11, article 87, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. B.-S. Guo, K.-K. Cheung, S. S. Yeung, B.-T. Zhang, and E. W. Yeung, “Electrical stimulation influences satellite cell proliferation and apoptosis in unloading-induced muscle atrophy in mice,” PLoS ONE, vol. 7, no. 1, Article ID e30348, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Egginton and O. Hudlicka, “Selective long-term electrical stimulation of fast glycolytic fibres increases capillary supply but not oxidative enzyme activity in rat skeletal muscles,” Experimental Physiology, vol. 85, no. 5, pp. 567–573, 2000. View at Publisher · View at Google Scholar · View at Scopus
  43. O. Hudlicka and S. Price, “The role of blood flow and/or muscle hypoxia in capillary growth in chronically stimulated fast muscles,” Pflügers Archiv, vol. 417, no. 1, pp. 67–72, 1990. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Shen, J. Gao, J. Li, and J. Su, “Effect of stimulation frequency on angiogenesis and gene expression in ischemic skeletal muscle of rabbit,” Canadian Journal of Physiology and Pharmacology, vol. 87, no. 5, pp. 396–401, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. M. D. Brown, M. A. Cotter, O. Hudlická, and G. Vrbová, “The effects of different patterns of muscle activity on capillary density, mechanical properties and structure of slow and fast rabbit muscles,” Pflügers Archiv, vol. 361, no. 3, pp. 241–250, 1976. View at Publisher · View at Google Scholar · View at Scopus
  46. F. M. Hansen-Smith, O. Hudlicka, and S. Egginton, “In vivo angiogenesis in adult rat skeletal muscle: early changes in capillary network architecture and ultrastructure,” Cell and Tissue Research, vol. 286, no. 1, pp. 123–136, 1996. View at Publisher · View at Google Scholar · View at Scopus
  47. O. Hudlicka, L. Dodd, E. M. Renkin, and S. D. Gray, “Early changes in fiber profile and capillary density in long-term stimulated muscles,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 12, no. 4, pp. H528–H535, 1982. View at Google Scholar · View at Scopus
  48. O. Mrázková and L. Puzanová, “The capillary bed in denervated muscle,” Folia Morphologica, vol. 19, no. 1, pp. 71–81, 1971. View at Google Scholar · View at Scopus
  49. E. I. Dedkov, T. Y. Kostrominova, A. B. Borisov, and B. M. Carlson, “Resistance vessel remodeling and reparative angiogenesis in the microcirculatory bed of long-term denervated skeletal muscles,” Microvascular Research, vol. 63, no. 1, pp. 96–114, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. D. Desplanches, M. H. Mayet, B. Sempore, and R. Flandrois, “Structural and functional responses to prolonged hindlimb suspension in rat muscle,” Journal of Applied Physiology, vol. 63, no. 2, pp. 558–563, 1987. View at Google Scholar · View at Scopus
  51. F. Kuwahara, H. Kai, K. Tokuda et al., “Hypoxia-inducible factor-1α/vascular endothelial growth factor pathway for adventitial vasa vasorum formation in hypertensive rat aorta,” Hypertension, vol. 39, no. 1, pp. 46–50, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. I. Zachary, “Signaling mechanisms mediating vascular protective actions of vascular endothelial growth factor,” American Journal of Physiology—Cell Physiology, vol. 280, no. 6, pp. C1375–C1386, 2001. View at Google Scholar · View at Scopus
  53. M. Scheler, M. Irmler, S. Lehr et al., “Cytokine response of primary human myotubes in an in vitro exercise model,” American Journal of Physiology—Cell Physiology, vol. 305, no. 8, pp. C877–C886, 2013. View at Publisher · View at Google Scholar · View at Scopus
  54. S. Egginton and O. Hudlická, “Early changes in performance, blood flow and capillary fine structure in rat fast muscles induced by electrical stimulation,” Journal of Physiology, vol. 515, no. 1, pp. 265–275, 1999. View at Publisher · View at Google Scholar · View at Scopus
  55. O. Mathieu-Costello, P. J. Agey, L. Wu, J. Hang, and T. H. Adair, “Capillary-to-fiber surface ratio in rat fast-twitch hindlimb muscles after chronic electrical stimulation,” Journal of Applied Physiology, vol. 80, no. 3, pp. 904–909, 1996. View at Google Scholar · View at Scopus
  56. N. G. dela Paz, T. E. Walshe, L. L. Leach, M. Saint-Geniez, and P. A. D'Amore, “Role of shear-stress-induced VEGF expression in endothelial cell survival,” Journal of Cell Science, vol. 125, no. 4, pp. 831–843, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. T. P. Quinn, M. Schlueter, S. J. Soifer, and J. A. Gutierrez, “Cyclic mechanical stretch induces VEGF and FGF-2 expression in pulmonary vascular smooth muscle cells,” American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 282, no. 5, pp. L897–L903, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Nagasaka, M. Kohzuki, T. Fujii et al., “Effect of low-voltage electrical stimulation on angiogenic growth factors in ischaemic rat skeletal muscle,” Clinical and Experimental Pharmacology and Physiology, vol. 33, no. 7, pp. 623–627, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. J. Folkman, “Angiogenesis in cancer, vascular, rheumatoid and other disease,” Nature Medicine, vol. 1, no. 1, pp. 27–30, 1995. View at Publisher · View at Google Scholar · View at Scopus
  60. T.-S. Yu, Z. Li, R. Zhao, Y. Zhang, Z.-H. Zhang, and D.-W. Guan, “Time-dependent expression of MMP-2 and TIMP-2 after rats skeletal muscle contusion and their application to determine wound age,” Journal of Forensic Sciences, vol. 61, no. 2, pp. 527–533, 2016. View at Publisher · View at Google Scholar · View at Scopus
  61. E. Carmeli, M. Moas, A. Z. Reznick, and R. Coleman, “Matrix metalloproteinases and skeletal muscle: a brief review,” Muscle and Nerve, vol. 29, no. 2, pp. 191–197, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. X. W. Cheng, M. Kuzuya, K. Nakamura et al., “Mechanisms underlying the impairment of ischemia-induced neovascularization in matrix metalloproteinase 2-deficient mice,” Circulation Research, vol. 100, no. 6, pp. 904–913, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. H. Tamaki, K. Yotani, F. Ogita et al., “Changes over time in structural plasticity of trabecular bone in rat tibiae immobilized by reversible sciatic denervation,” Journal of Musculoskeletal & Neuronal Interactions, vol. 13, no. 3, pp. 289–296, 2013. View at Google Scholar · View at Scopus
  64. T. Tanaka, Y. Kariya, and Y. Hoshino, “Histochemical study on the changes in muscle fibers in relation to the effects of aging on recovery from muscular atrophy caused by disuse in rats,” Journal of Orthopaedic Science, vol. 9, no. 1, pp. 76–85, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. J. Tuukkanen, Z. Peng, and H. K. Vaananen, “The effect of training on the recovery from immobilization-induced bone loss in rats,” Acta Physiologica Scandinavica, vol. 145, no. 4, pp. 407–411, 1992. View at Publisher · View at Google Scholar · View at Scopus
  66. M. P. Lewis, H. L. Tippett, A. C. M. Sinanan, M. J. Morgan, and N. P. Hunt, “Gelatinase-B (matrix metalloproteinase-9; MMP-9) secretion is involved in the migratory phase of human and murine muscle cell cultures,” Journal of Muscle Research and Cell Motility, vol. 21, no. 3, pp. 223–233, 2000. View at Publisher · View at Google Scholar · View at Scopus