Advertisement

Sports Medicine

, Volume 46, Issue 6, pp 783–792 | Cite as

Skeletal Muscle Loading Changes its Regenerative Capacity

  • Eduardo TeixeiraEmail author
  • José Alberto Duarte
Review Article

Abstract

Whenever skeletal muscle insults occur, both by functional impositions or other injury forms, skeletal muscle repair (SMR) follows. The SMR succeeds when proper skeletal muscle regeneration and limited fibrosis ensue. Muscle fiber replenishment by fibrosis negatively affects the tissue quality and functionality and, furthermore, represents the worst post-injury phenotypic adaptation. Acute muscle injury treatment commonly follows the RICE method—rest, ice, compression, and elevation. This immediate immobilization seems to be beneficial to preserving the tissue structure and avoiding further destruction; however, if these interventions are delayed, the risk of muscle atrophy and its deleterious-related effects increase, with resultant impaired SMR. Moreover, a growing body of evidence shows positive skeletal muscle loading (SML) effects during SMR since it seems to effectively increase satellite cells (SCs) in their activation, proliferation, self-renewal, and differentiation capacities. Additionally, recent data show that SML may also influence the functions of other participants in SMR, compelling SMR to achieve less fibrotic accretion and accelerated muscle mass recovery. Moreover, given the SML effects on SCs, it is plausible to consider that these can increase the myofibers’ basal myogenic potential. Thus, it seems relevant to scrutinize the possible acute and chronic SML therapeutic and prophylactic effects regarding the SMR process.

Keywords

Resistance Training Satellite Cell Resistance Exercise Vastus Lateralis Muscle Injury 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Compliance with Ethical Standards

Funding

The Research Center in Physical Activity, Health and Leisure is supported by the Portuguese Foundation for Science and Technology (FCT; UID/DTP/00617/2013). Eduardo Teixeira benefits from an FCT grant (SFRH/BD/76740/2011).

Conflict of interest

Eduardo Teixeira and José Alberto Duarte declare that they have no conflicts of interest directly relevant to the content of this review.

References

  1. 1.
    Otto A, Collins-Hooper H, Patel K. The origin, molecular regulation and therapeutic potential of myogenic stem cell populations. J Anat. 2009;215(5):477–97.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol. 1961;9:493–5.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Biressi S, Rando TA. Heterogeneity in the muscle satellite cell population. Semin Cell Dev Biol. 2010;21(8):845–54.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Yin H, Price F, Rudnicki MA. Satellite cells and the muscle stem cell niche. Physiol Rev. 2013;93(1):23–67.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Bentzinger CF, Wang YX, Dumont NA, et al. Cellular dynamics in the muscle satellite cell niche. EMBO Rep. 2013;14(12):1062–72.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Moyer AL, Wagner KR. Regeneration versus fibrosis in skeletal muscle. Curr Opin Rheumatol. 2011;23(6):568–73.CrossRefPubMedGoogle Scholar
  7. 7.
    Sciorati C, Clementi E, Manfredi AA, et al. Fat deposition and accumulation in the damaged and inflamed skeletal muscle: cellular and molecular players. Cell Mol Life Sci. 2015;72(11):2135–56.CrossRefPubMedGoogle Scholar
  8. 8.
    Charge SB, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev. 2004;84(1):209–38.CrossRefPubMedGoogle Scholar
  9. 9.
    Pillon NJ, Bilan PJ, Fink LN, et al. Cross-talk between skeletal muscle and immune cells: muscle-derived mediators and metabolic implications. Am J Physiol Endocrinol Metab. 2013;304(5):E453–65.CrossRefPubMedGoogle Scholar
  10. 10.
    Tidball JG, Villalta SA. Regulatory interactions between muscle and the immune system during muscle regeneration. Am J Physiol Regul Integr Comp Physiol. 2010;298(5):R1173–87.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Sicari BM, Rubin JP, Dearth CL, et al. An acellular biologic scaffold promotes skeletal muscle formation in mice and humans with volumetric muscle loss. Sci Transl Med. 2014;6(234):234ra58.Google Scholar
  12. 12.
    Urciuolo A, Quarta M, Morbidoni V, et al. Collagen VI regulates satellite cell self-renewal and muscle regeneration. Nat Commun. 2013;4:1964.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Kjaer M, Magnusson P, Krogsgaard M, et al. Extracellular matrix adaptation of tendon and skeletal muscle to exercise. J Anat. 2006;208(4):445–50.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Danna NR, Beutel BG, Campbell KA, et al. Therapeutic approaches to skeletal muscle repair and healing. Sports Health. 2014;6(4):348–55.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Jarvinen TA, Jarvinen TL, Kaariainen M, et al. Muscle injuries: optimising recovery. Best Pract Res Clin Rheumatol. 2007;21(2):317–31.CrossRefPubMedGoogle Scholar
  16. 16.
    Powers SK, Kavazis AN, DeRuisseau KC. Mechanisms of disuse muscle atrophy: role of oxidative stress. Am J Physiol Regul Integr Comp Physiol. 2005;288(2):R337–44.CrossRefPubMedGoogle Scholar
  17. 17.
    Richard-Bulteau H, Serrurier B, Crassous B, et al. Recovery of skeletal muscle mass after extensive injury: positive effects of increased contractile activity. Am J Physiol Cell Physiol. 2008;294(2):C467–76.CrossRefPubMedGoogle Scholar
  18. 18.
    Snijders T, Verdijk LB, Beelen M, et al. A single bout of exercise activates skeletal muscle satellite cells during subsequent overnight recovery. Exp Physiol. 2012;97(6):762–73.CrossRefPubMedGoogle Scholar
  19. 19.
    Mackey AL, Esmarck B, Kadi F, et al. Enhanced satellite cell proliferation with resistance training in elderly men and women. Scand J Med Sci Sports. 2007;17(1):34–42.PubMedGoogle Scholar
  20. 20.
    Smith HK, Merry TL. Voluntary resistance wheel exercise during post-natal growth in rats enhances skeletal muscle satellite cell and myonuclear content at adulthood. Acta Physiol (Oxf). 2012;204(3):393–402.CrossRefPubMedGoogle Scholar
  21. 21.
    Relaix F, Zammit PS. Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development. 2012;139(16):2845–56.CrossRefPubMedGoogle Scholar
  22. 22.
    Wang YX, Rudnicki MA. Satellite cells, the engines of muscle repair. Nat Rev Mol Cell Biol. 2012;13(2):127–33.Google Scholar
  23. 23.
    Suetta C, Frandsen U, Mackey AL, et al. Ageing is associated with diminished muscle re-growth and myogenic precursor cell expansion early after immobility-induced atrophy in human skeletal muscle. J Physiol. 2013;591(Pt 15):3789–804.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Lee DA, Knight MM, Campbell JJ, et al. Stem cell mechanobiology. J Cell Biochem. 2011;112(1):1–9.CrossRefPubMedGoogle Scholar
  25. 25.
    Reilly GC, Engler AJ. Intrinsic extracellular matrix properties regulate stem cell differentiation. J Biomech. 2010;43(1):55–62.CrossRefPubMedGoogle Scholar
  26. 26.
    Discher DE, Janmey P, Wang YL. Tissue cells feel and respond to the stiffness of their substrate. Science. 2005;310(5751):1139–43.CrossRefPubMedGoogle Scholar
  27. 27.
    Engler AJ, Sen S, Sweeney HL, et al. Matrix elasticity directs stem cell lineage specification. Cell. 2006;126(4):677–89.CrossRefPubMedGoogle Scholar
  28. 28.
    Pedersen BK, Febbraio MA. Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev. 2008;88(4):1379–406.CrossRefPubMedGoogle Scholar
  29. 29.
    Pedersen BK, Edward F. Adolph distinguished lecture: muscle as an endocrine organ: IL-6 and other myokines. J Appl Physiol (1985). 2009;107(4):1006–14.CrossRefGoogle Scholar
  30. 30.
    Pedersen BK, Fischer CP. Beneficial health effects of exercise—the role of IL-6 as a myokine. Trends Pharmacol Sci. 2007;28(4):152–6.CrossRefPubMedGoogle Scholar
  31. 31.
    Hvid LG. Early plasticity of human skeletal muscle in response to disuse. Acta Physiol (Oxf). 2014;210(3):460–1.CrossRefPubMedGoogle Scholar
  32. 32.
    Persson PB. Skeletal muscle satellite cells as myogenic progenitors for muscle homoeostasis, growth, regeneration and repair. Acta Physiol (Oxf). 2015;213(3):537–8.CrossRefPubMedGoogle Scholar
  33. 33.
    Parise G. Satellite cells: promoting adaptation over a lifetime. Acta Physiol (Oxf). 2014;210(3):462–4.CrossRefPubMedGoogle Scholar
  34. 34.
    Verdijk LB. Satellite cell activation as a critical step in skeletal muscle plasticity. Exp Physiol. 2014;99(11):1449–50.CrossRefPubMedGoogle Scholar
  35. 35.
    Mackey AL, Karlsen A, Couppe C, et al. Differential satellite cell density of type I and II fibres with lifelong endurance running in old men. Acta Physiol (Oxf). 2014;210(3):612–27.CrossRefPubMedGoogle Scholar
  36. 36.
    Verdijk LB, Snijders T, Drost M, et al. Satellite cells in human skeletal muscle; from birth to old age. Age (Dordr). 2014;36(2):545–7.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Petrella JK, Kim JS, Mayhew DL, et al. Potent myofiber hypertrophy during resistance training in humans is associated with satellite cell-mediated myonuclear addition: a cluster analysis. J Appl Physiol. 2008;104(6):1736–42.CrossRefPubMedGoogle Scholar
  38. 38.
    Joanisse S, Gillen JB, Bellamy LM, et al. Evidence for the contribution of muscle stem cells to nonhypertrophic skeletal muscle remodeling in humans. FASEB J. 2013;27(11):4596–605.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Rudnicki MA, Le Grand F, McKinnell I, et al. The molecular regulation of muscle stem cell function. Cold Spring Harb Symp Quant Biol. 2008;73:323–31.CrossRefPubMedGoogle Scholar
  40. 40.
    Choi S, Liu X, Li P, et al. Transcriptional profiling in mouse skeletal muscle following a single bout of voluntary running: evidence of increased cell proliferation. J Appl Physiol (1985). 2005;99(6):2406–15.CrossRefGoogle Scholar
  41. 41.
    Crameri RM, Langberg H, Magnusson P, et al. Changes in satellite cells in human skeletal muscle after a single bout of high intensity exercise. J Physiol. 2004;558(Pt 1):333–40.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Cermak NM, Snijders T, McKay BR, et al. Eccentric exercise increases satellite cell content in type II muscle fibers. Med Sci Sports Exerc. 2013;45(2):230–7.CrossRefPubMedGoogle Scholar
  43. 43.
    Bellamy LM, Joanisse S, Grubb A, et al. The acute satellite cell response and skeletal muscle hypertrophy following resistance training. PLoS One. 2014;9(10):e109739.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Hyldahl RD, Olson T, Welling T, et al. Satellite cell activity is differentially affected by contraction mode in human muscle following a work-matched bout of exercise. Front Physiol. 2014;5:485.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Verdijk LB, Koopman R, Schaart G, et al. Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly. Am J Physiol Endocrinol Metab. 2007;292(1):E151–7.CrossRefPubMedGoogle Scholar
  46. 46.
    Dreyer HC, Blanco CE, Sattler FR, et al. Satellite cell numbers in young and older men 24 hours after eccentric exercise. Muscle Nerve. 2006;33(2):242–53.CrossRefPubMedGoogle Scholar
  47. 47.
    McKay BR, Ogborn DI, Bellamy LM, et al. Myostatin is associated with age-related human muscle stem cell dysfunction. FASEB J. 2012;26(6):2509–21.CrossRefPubMedGoogle Scholar
  48. 48.
    Snijders T, Verdijk LB, Smeets JS, et al. The skeletal muscle satellite cell response to a single bout of resistance-type exercise is delayed with aging in men. Age (Dordr). 2014;36(4):9699.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Ferreira R, Neuparth MJ, Ascensao A, et al. Skeletal muscle atrophy increases cell proliferation in mice gastrocnemius during the first week of hindlimb suspension. Eur J Appl Physiol. 2006;97(3):340–6.CrossRefPubMedGoogle Scholar
  50. 50.
    Snijders T, Wall BT, Dirks ML, et al. Muscle disuse atrophy is not accompanied by changes in skeletal muscle satellite cell content. Clin Sci (Lond). 2014;126(8):557–66.CrossRefPubMedGoogle Scholar
  51. 51.
    Dirks ML, Wall BT, Snijders T, et al. Neuromuscular electrical stimulation prevents muscle disuse atrophy during leg immobilization in humans. Acta Physiol (Oxf). 2014;210(3):628–41.CrossRefPubMedGoogle Scholar
  52. 52.
    Carlson ME, Suetta C, Conboy MJ, et al. Molecular aging and rejuvenation of human muscle stem cells. EMBO Mol Med. 2009;1(8–9):381–91.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Brooks NE, Myburgh KH. Skeletal muscle wasting with disuse atrophy is multi-dimensional: the response and interaction of myonuclei, satellite cells and signaling pathways. Front Physiol. 2014;5:99.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Hochreiter-Hufford AE, Lee CS, Kinchen JM, et al. Phosphatidylserine receptor BAI1 and apoptotic cells as new promoters of myoblast fusion. Nature. 2013;497(7448):263–7.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Yu SF, Baylies MK. Cell biology: death brings new life to muscle. Nature. 2013;497(7448):196–7.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Kadi F, Thornell LE. Concomitant increases in myonuclear and satellite cell content in female trapezius muscle following strength training. Histochem Cell Biol. 2000;113(2):99–103.CrossRefPubMedGoogle Scholar
  57. 57.
    Charifi N, Kadi F, Feasson L, et al. Effects of endurance training on satellite cell frequency in skeletal muscle of old men. Muscle Nerve. 2003;28(1):87–92.CrossRefPubMedGoogle Scholar
  58. 58.
    Kadi F, Schjerling P, Andersen LL, et al. The effects of heavy resistance training and detraining on satellite cells in human skeletal muscles. J Physiol. 2004;558(Pt 3):1005–12.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Verdijk LB, Gleeson BG, Jonkers RA, et al. Skeletal muscle hypertrophy following resistance training is accompanied by a fiber type-specific increase in satellite cell content in elderly men. J Gerontol A Biol Sci Med Sci. 2009;64(3):332–9.CrossRefPubMedGoogle Scholar
  60. 60.
    Mackey AL, Andersen LL, Frandsen U, et al. Strength training increases the size of the satellite cell pool in type I and II fibres of chronically painful trapezius muscle in females. J Physiol. 2011;589(Pt 22):5503–15.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Mackey AL, Holm L, Reitelseder S, et al. Myogenic response of human skeletal muscle to 12 weeks of resistance training at light loading intensity. Scand J Med Sci Sports. 2011;21(6):773–82.CrossRefPubMedGoogle Scholar
  62. 62.
    Fry CS, Noehren B, Mula J, et al. Fibre type-specific satellite cell response to aerobic training in sedentary adults. J Physiol. 2014;592(Pt 12):2625–35.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    O’Connor RS, Pavlath GK. Point:Counterpoint: satellite cell addition is/is not obligatory for skeletal muscle hypertrophy. J Appl Physiol (1985). 2007;103(3):1099–100.CrossRefGoogle Scholar
  64. 64.
    Jackson JR, Mula J, Kirby TJ, et al. Satellite cell depletion does not inhibit adult skeletal muscle regrowth following unloading-induced atrophy. Am J Physiol Cell Physiol. 2012;303(8):C854–61.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    McCarthy JJ, Mula J, Miyazaki M, et al. Effective fiber hypertrophy in satellite cell-depleted skeletal muscle. Development. 2011;138(17):3657–66.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Van der Meer SF, Jaspers RT, Degens H. Is the myonuclear domain size fixed? J Musculoskelet Neuronal Interact. 2011;11(4):286–97.PubMedGoogle Scholar
  67. 67.
    Verney J, Kadi F, Charifi N, et al. Effects of combined lower body endurance and upper body resistance training on the satellite cell pool in elderly subjects. Muscle Nerve. 2008;38(3):1147–54.CrossRefPubMedGoogle Scholar
  68. 68.
    Leenders M, Verdijk LB, van der Hoeven L, et al. Elderly men and women benefit equally from prolonged resistance-type exercise training. J Gerontol A Biol Sci Med Sci. 2013;68(7):769–79.CrossRefPubMedGoogle Scholar
  69. 69.
    Snijders T, Verdijk LB, Hansen D, et al. Continuous endurance-type exercise training does not modulate satellite cell content in obese type 2 diabetes patients. Muscle Nerve. 2011;43(3):393–401.CrossRefPubMedGoogle Scholar
  70. 70.
    Watt FM, Hogan BL. Out of Eden: stem cells and their niches. Science. 2000;287(5457):1427–30.CrossRefPubMedGoogle Scholar
  71. 71.
    Moore KA, Lemischka IR. Stem cells and their niches. Science. 2006;311(5769):1880–5.CrossRefPubMedGoogle Scholar
  72. 72.
    Pannerec A, Marazzi G, Sassoon D. Stem cells in the hood: the skeletal muscle niche. Trends Mol Med. 2012;18(10):599–606.CrossRefPubMedGoogle Scholar
  73. 73.
    Cornelison DD. Context matters: in vivo and in vitro influences on muscle satellite cell activity. J Cell Biochem. 2008;105(3):663–9.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Kuang S, Gillespie MA, Rudnicki MA. Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell. 2008;2(1):22–31.CrossRefPubMedGoogle Scholar
  75. 75.
    Pedersen BK. Muscle as a secretory organ. Compr Physiol. 2013;3(3):1337–62.PubMedGoogle Scholar
  76. 76.
    Bonsignore MR, Morici G, Santoro A, et al. Circulating hematopoietic progenitor cells in runners. J Appl Physiol (1985). 2002;93(5):1691–7.CrossRefGoogle Scholar
  77. 77.
    Ribeiro F, Ribeiro IP, Alves AJ, et al. Effects of exercise training on endothelial progenitor cells in cardiovascular disease: a systematic review. Am J Phys Med Rehabil. 2013;92(11):1020–30.CrossRefPubMedGoogle Scholar
  78. 78.
    Christov C, Chretien F, Abou-Khalil R, et al. Muscle satellite cells and endothelial cells: close neighbors and privileged partners. Mol Biol Cell. 2007;18(4):1397–409.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Yan Z, Okutsu M, Akhtar YN, et al. Regulation of exercise-induced fiber type transformation, mitochondrial biogenesis, and angiogenesis in skeletal muscle. J Appl Physiol (1985). 2011;110(1):264–74.CrossRefPubMedCentralGoogle Scholar
  80. 80.
    Arsic N, Zacchigna S, Zentilin L, et al. Vascular endothelial growth factor stimulates skeletal muscle regeneration in vivo. Mol Ther. 2004;10(5):844–54.CrossRefPubMedGoogle Scholar
  81. 81.
    Zanou N, Gailly P. Skeletal muscle hypertrophy and regeneration: interplay between the myogenic regulatory factors (MRFs) and insulin-like growth factors (IGFs) pathways. Cell Mol Life Sci. 2013;70(21):4117–30.CrossRefPubMedGoogle Scholar
  82. 82.
    Musaro A, Giacinti C, Borsellino G, et al. Stem cell-mediated muscle regeneration is enhanced by local isoform of insulin-like growth factor 1. Proc Natl Acad Sci USA. 2004;101(5):1206–10.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Grounds MD. The need to more precisely define aspects of skeletal muscle regeneration. Int J Biochem Cell Biol. 2014;56:56–65.CrossRefPubMedGoogle Scholar
  84. 84.
    Hatade T, Takeuchi K, Fujita N, et al. Effect of heat stress soon after muscle injury on the expression of MyoD and myogenin during regeneration process. J Musculoskelet Neuronal Interact. 2014;14(3):325–33.PubMedGoogle Scholar
  85. 85.
    Mason DL, Dickens VA, Vail A. Rehabilitation for hamstring injuries. Cochrane Database Syst Rev. 2012;(12):Art.No:CD004575. doi: 10.1002/14651858.CD004575.pub3.
  86. 86.
    Askling CM, Tengvar M, Tarassova O, et al. Acute hamstring injuries in Swedish elite sprinters and jumpers: a prospective randomised controlled clinical trial comparing two rehabilitation protocols. Br J Sports Med. 2014;48(7):532–9.CrossRefPubMedGoogle Scholar
  87. 87.
    Askling CM, Tengvar M, Thorstensson A. Acute hamstring injuries in Swedish elite football: a prospective randomised controlled clinical trial comparing two rehabilitation protocols. Br J Sports Med. 2013;47(15):953–9.CrossRefPubMedGoogle Scholar
  88. 88.
    Ambrosio F, Ferrari RJ, Distefano G, et al. The synergistic effect of treadmill running on stem-cell transplantation to heal injured skeletal muscle. Tissue Eng Part A. 2010;16(3):839–49.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Palermo AT, LaBarge MA, Doyonnas R, et al. Bone marrow contribution to skeletal muscle: a physiological response to stress. Dev Biol. 2005;279(2):336–44.CrossRefPubMedGoogle Scholar
  90. 90.
    Hwang JH, Ra YJ, Lee KM, et al. Therapeutic effect of passive mobilization exercise on improvement of muscle regeneration and prevention of fibrosis after laceration injury of rat. Arch Phys Med Rehabil. 2006;87(1):20–6.CrossRefPubMedGoogle Scholar
  91. 91.
    Rullman E, Norrbom J, Stromberg A, et al. Endurance exercise activates matrix metalloproteinases in human skeletal muscle. J Appl Physiol (1985). 2009;106(3):804–12.CrossRefGoogle Scholar
  92. 92.
    Silveira EM, Rodrigues MF, Krause MS, et al. Acute exercise stimulates macrophage function: possible role of NF-kappaB pathways. Cell Biochem Funct. 2007;25(1):63–73.CrossRefPubMedGoogle Scholar
  93. 93.
    Woods J, Lu Q, Ceddia MA, et al. Special feature for the Olympics: effects of exercise on the immune system: exercise-induced modulation of macrophage function. Immunol Cell Biol. 2000;78(5):545–53.CrossRefPubMedGoogle Scholar
  94. 94.
    Walsh NP, Gleeson M, Shephard RJ, et al. Position statement. Part one: immune function and exercise. Exerc Immunol Rev. 2011;17:6–63.PubMedGoogle Scholar
  95. 95.
    Guo BS, Cheung KK, Yeung SS, et al. Electrical stimulation influences satellite cell proliferation and apoptosis in unloading-induced muscle atrophy in mice. PLoS One. 2012;7(1):e30348.CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Zhang BT, Yeung SS, Liu Y, et al. The effects of low frequency electrical stimulation on satellite cell activity in rat skeletal muscle during hindlimb suspension. BMC Cell Biol. 2010;11:87.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Centro de Investigação em Atividade Física e Saúde, Faculdade de Desporto da Universidade do Porto (CIAFEL-FADEUP)PortoPortugal

Personalised recommendations