Current evidence that exercise can increase the number of adult stem cells

  • F. MacalusoEmail author
  • K. H. Myburgh
EMC2012 Special Issue - Original Paper


The number of adult stem cells (ASCs) is very small, limiting the regenerative potential of tissues. One of the most studied ASCs in humans is the satellite cell (SC), which proliferates and increases pool size under exercise stress and muscle damage. This review examines the growth factor response to specific types of exercise to show the potential of exercise to stimulate not only SC self-renewal, but also other ASCs. We postulate that the same factors that stimulate a high proliferation of SCs in skeletal muscle after physical exercise should also stimulate the proliferation of ASCs in the tissue in which they reside, such as heart, bone, liver and etc. Regular exercise should be promoted, not only for disease prevention, but to maintain a high ASCs reserve and progenitor cell potential for rapid activation in response to future stressors and damage.


Niche Self-renewal Tissue repair Satellite cell Endurance training Resistance training 


  1. Adams GR, McCue SA (1998) Localized infusion of IGF-I results in skeletal muscle hypertrophy in rats. J Appl Physiol 84(5):1716–1722PubMedGoogle Scholar
  2. Allen RE, Boxhorn LK (1989) Regulation of skeletal muscle satellite cell proliferation and differentiation by transforming growth factor-beta, insulin-like growth factor I, and fibroblast growth factor. J Cell Physiol 138(2):311–315. doi: 10.1002/jcp1041380213 PubMedCrossRefGoogle Scholar
  3. Allen RE, Sheehan SM, Taylor RG, Kendall TL, Rice GM (1995) Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro. J Cell Physiol 165(2):307–312. doi: 10.1002/jcp1041650211 PubMedCrossRefGoogle Scholar
  4. Allen RE, Temm-Grove CJ, Sheehan SM, Rice G (1997) Skeletal muscle satellite cell cultures. Methods Cell Biol 52:155–176PubMedCrossRefGoogle Scholar
  5. Atari M, Barajas M, Hernandez-Alfaro F, Gil C, Fabregat M, Padro EF, Giner L, Casals N (2011) Isolation of pluripotent stem cells from human third molar dental pulp. Histol Histopathol 26(8):1057–1070PubMedGoogle Scholar
  6. Bamman MM, Shipp JR, Jiang J, Gower BA, Hunter GR, Goodman A, McLafferty CL Jr, Urban RJ (2001) Mechanical load increases muscle IGF-I and androgen receptor mRNA concentrations in humans. Am J Physiol Endocrinol Metab 280(3):E383–E390PubMedGoogle Scholar
  7. Barton ER (2006) Viral expression of insulin-like growth factor-I isoforms promotes different responses in skeletal muscle. J Appl Physiol 100(6):1778–1784PubMedCrossRefGoogle Scholar
  8. Barton ER, DeMeo J, Lei H (2010) The insulin-like growth factor (IGF)-I E-peptides are required for isoform-specific gene expression and muscle hypertrophy after local IGF-I production. J Appl Physiol 108(5):1069–1076PubMedCrossRefGoogle Scholar
  9. Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S, Kasahara H, Rota M, Musso E, Urbanek K, Leri A, Kajstura J, Nadal-Ginard B, Anversa P (2003) Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114(6):763–776PubMedCrossRefGoogle Scholar
  10. Boldrin L, Muntoni F, Morgan JE (2010) Are human and mouse satellite cells really the same? J Histochem Cytochem 58(11):941–955. doi: 10.1369/jhc.2010.956201 PubMedCrossRefGoogle Scholar
  11. Bonsignore MR, Morici G, Santoro A, Pagano M, Cascio L, Bonanno A, Abate P, Mirabella F, Profita M, Insalaco G, Gioia M, Vignola AM, Majolino I, Testa U, Hogg JC (2002) Circulating hematopoietic progenitor cells in runners. J Appl Physiol 93(5):1691–1697. doi: 10.1152/japplphysiol.00376.2002 PubMedGoogle Scholar
  12. Broholm C, Pedersen BK (2010) Leukaemia inhibitory factor—an exercise-induced myokine. Exerc Immunol Rev 16:77–85PubMedGoogle Scholar
  13. Broholm C, Mortensen OH, Nielsen S, Akerstrom T, Zankari A, Dahl B, Pedersen BK (2008) Exercise induces expression of leukaemia inhibitory factor in human skeletal muscle. J Physiol 586(8):2195–2201. doi: 10.1113/jphysiol.2007.149781 PubMedCrossRefGoogle Scholar
  14. Broholm C, Laye MJ, Brandt C, Vadalasetty R, Pilegaard H, Pedersen BK, Scheele C (2011) LIF is a contraction-induced myokine stimulating human myocyte proliferation. J Appl Physiol 111(1):251–259. doi: 10.1152/japplphysiol.01399.2010 PubMedCrossRefGoogle Scholar
  15. Brooks NE, Cadena SM, Vannier E, Cloutier G, Carambula S, Myburgh KH, Roubenoff R, Castaneda-Sceppa C (2010) Effects of resistance exercise combined with essential amino acid supplementation and energy deficit on markers of skeletal muscle atrophy and regeneration during bed rest and active recovery. Muscle Nerve 42(6):927–935. doi: 10.1002/mus.21780 PubMedCrossRefGoogle Scholar
  16. Cannon JG, St Pierre BA (1998) Cytokines in exertion-induced skeletal muscle injury. Mol Cell Biochem 179(1–2):159–167PubMedCrossRefGoogle Scholar
  17. Carlson ME, Conboy IM (2007) Loss of stem cell regenerative capacity within aged niches. Aging Cell 6(3):371–382. doi: 10.1111/j.1474-9726.2007.00286.x PubMedCrossRefGoogle Scholar
  18. Carlson ME, Conboy MJ, Hsu M, Barchas L, Jeong J, Agrawal A, Mikels AJ, Agrawal S, Schaffer DV, Conboy IM (2009) Relative roles of TGF-beta1 and Wnt in the systemic regulation and aging of satellite cell responses. Aging Cell 8(6):676–689. doi: 10.1111/j.1474-9726.2009.00517.x PubMedCrossRefGoogle Scholar
  19. Chakravarthy MV, Abraha TW, Schwartz RJ, Fiorotto ML, Booth FW (2000) Insulin-like growth factor-I extends in vitro replicative life span of skeletal muscle satellite cells by enhancing G1/S cell cycle progression via the activation of phosphatidylinositol 3’-kinase/Akt signaling pathway. J Biol Chem 275(46):35942–35952. doi: 10.1074/jbc.M005832200 PubMedCrossRefGoogle Scholar
  20. Charifi N, Kadi F, Feasson L, Denis C (2003) Effects of endurance training on satellite cell frequency in skeletal muscle of old men. Muscle Nerve 28(1):87–92. doi: 10.1002/mus.10394 PubMedCrossRefGoogle Scholar
  21. Charge SB, Rudnicki MA (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev 84(1): 209–238. doi: 10.1152/physrev.00019.200384/1/209 Google Scholar
  22. Cheng M, Nguyen MH, Fantuzzi G, Koh TJ (2008) Endogenous interferon-gamma is required for efficient skeletal muscle regeneration. Am J Physiol Cell Physiol 294(5):C1183–C1191. doi: 10.1152/ajpcell.00568.2007 PubMedCrossRefGoogle Scholar
  23. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA (2005) Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433(7027):760–764. doi: 10.1038/nature03260 PubMedCrossRefGoogle Scholar
  24. Cossu G, Tajbakhsh S (2007) Oriented cell divisions and muscle satellite cell heterogeneity. Cell 129(5):859–861. doi: 10.1016/j.cell.2007.05.029 PubMedCrossRefGoogle Scholar
  25. Cotman CW, Berchtold NC, Christie LA (2007) Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 30(9):464–472PubMedCrossRefGoogle Scholar
  26. Covey MV, Levison SW (2007) Leukemia inhibitory factor participates in the expansion of neural stem/progenitors after perinatal hypoxia/ischemia. Neuroscience 148(2):501–509. doi: 10.1016/j.neuroscience.2007.06.015 PubMedCrossRefGoogle Scholar
  27. Crameri RM, Langberg H, Magnusson P, Jensen CH, Schroder HD, Olesen JL, Suetta C, Teisner B, Kjaer M (2004) Changes in satellite cells in human skeletal muscle after a single bout of high intensity exercise. J Physiol 558(Pt 1):333–340. doi: 10.1113/jphysiol.2004.061846 PubMedCrossRefGoogle Scholar
  28. Crameri RM, Aagaard P, Qvortrup K, Langberg H, Olesen J, Kjaer M (2007) Myofibre damage in human skeletal muscle: effects of electrical stimulation versus voluntary contraction. J Physiol 583(Pt 1):365–380. doi: 10.1113/jphysiol.2007.128827 PubMedCrossRefGoogle Scholar
  29. Czarkowska-Paczek B, Bartlomiejczyk I, Przybylski J (2006) The serum levels of growth factors: PDGF, TGF-beta and VEGF are increased after strenuous physical exercise. J Physiol Pharmacol 57(2):189–197PubMedGoogle Scholar
  30. Darr KC, Schultz E (1987) Exercise-induced satellite cell activation in growing and mature skeletal muscle. J Appl Physiol 63(5):1816–1821PubMedGoogle Scholar
  31. Di Felice V, De Luca A, Colorito ML, Montalbano A, Ardizzone NM, Macaluso F, Gammazza AM, Cappello F, Zummo G (2009) Cardiac stem cell research: an elephant in the room? Anat Rec (Hoboken) 292(3):449–454. doi: 10.1002/ar.20858 CrossRefGoogle Scholar
  32. Doherty TJ (2003) Invited review: aging and sarcopenia. J Appl Physiol 95(4):1717–1727. doi: 10.1152/japplphysiol.00347.2003 PubMedGoogle Scholar
  33. Donnikov AE, Shkurnikov MY, Akimov EB, Grebenyuk ES, Khaustova SA, Shahmatova EM, Tonevitsky AG (2009) Effect of a six-hour marathon ultra-race on the levels of IL-6, LIF, and SCF. Bull Exp Biol Med 148(5):819–821PubMedCrossRefGoogle Scholar
  34. Dunker N, Krieglstein K (2000) Targeted mutations of transforming growth factor-beta genes reveal important roles in mouse development and adult homeostasis. Eur J Biochem 267(24):6982–6988PubMedCrossRefGoogle Scholar
  35. Ellison GM, Waring CD, Vicinanza C, Torella D (2011) Physiological cardiac remodelling in response to endurance exercise training: cellular and molecular mechanisms. Heart. doi: 10.1136/heartjnl-2011-300639 PubMedGoogle Scholar
  36. Fabel K, Fabel K, Tam B, Kaufer D, Baiker A, Simmons N, Kuo CJ, Palmer TD (2003) VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci 18(10):2803–2812PubMedCrossRefGoogle Scholar
  37. Friedrichs M, Wirsdorfer F, Flohe SB, Schneider S, Wuelling M, Vortkamp A (2011) Bmp-signaling balances proliferation and differentiation of muscle satellite cell descendants. BMC Cell Biol 12(1):26. doi: 10.1186/1471-2121-12-26 PubMedCrossRefGoogle Scholar
  38. Gal-Levi R, Leshem Y, Aoki S, Nakamura T, Halevy O (1998) Hepatocyte growth factor plays a dual role in regulating skeletal muscle satellite cell proliferation and differentiation. Biochim Biophys Acta 1402(1):39–51PubMedCrossRefGoogle Scholar
  39. Gnocchi VF, White RB, Ono Y, Ellis JA, Zammit PS (2009) Further characterisation of the molecular signature of quiescent and activated mouse muscle satellite cells. PLoS ONE 4(4):e5205. doi: 10.1371/journal.pone.0005205 PubMedCrossRefGoogle Scholar
  40. Greco V, Guo S (2010) Compartmentalized organization: a common and required feature of stem cell niches? Development 137(10):1586–1594. doi: 10.1242/dev.041103 PubMedCrossRefGoogle Scholar
  41. Grounds MD (1998) Age-associated changes in the response of skeletal muscle cells to exercise and regeneration. Ann N Y Acad Sci 854:78–91PubMedCrossRefGoogle Scholar
  42. Gundersen K (2011) Excitation-transcription coupling in skeletal muscle: the molecular pathways of exercise. Biol Rev Camb Philos Soc 86(3):564–600. doi: 10.1111/j.1469-185X.2010.00161.x PubMedCrossRefGoogle Scholar
  43. Hasani-Ranjbar S, Soleymani Far E, Heshmat R, Rajabi H, Kosari H (2011) Time course responses of serum GH, insulin, IGF-1, IGFBP1, and IGFBP3 concentrations after heavy resistance exercise in trained and untrained men. Endocrine. doi: 10.1007/s12020-011-9537-3 PubMedGoogle Scholar
  44. Hawke TJ, Garry DJ (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91(2):534–551PubMedGoogle Scholar
  45. Hoch RV, Soriano P (2003) Roles of PDGF in animal development. Development 130(20):4769–4784. doi: 10.1242/dev.00721 PubMedCrossRefGoogle Scholar
  46. Jaumot M, Estanol JM, Casanovas O, Grana X, Agell N, Bachs O (1997) The cell cycle inhibitor p21CIP is phosphorylated by cyclin A-CDK2 complexes. Biochem Biophys Res Commun 241(2):434–438. doi: 10.1006/bbrc.1997.7787 PubMedCrossRefGoogle Scholar
  47. Jones NC, Tyner KJ, Nibarger L, Stanley HM, Cornelison DD, Fedorov YV, Olwin BB (2005) The p38alpha/beta MAPK functions as a molecular switch to activate the quiescent satellite cell. J Cell Biol 169(1):105–116. doi: 10.1083/jcb.200408066 PubMedCrossRefGoogle Scholar
  48. Kadi F, Schjerling P, Andersen LL, Charifi N, Madsen JL, Christensen LR, Andersen JL (2004) The effects of heavy resistance training and detraining on satellite cells in human skeletal muscles. J Physiol 558(Pt 3):1005–1012. doi: 10.1113/jphysiol.2004.065904 PubMedCrossRefGoogle Scholar
  49. Knaepen K, Goekint M, Heyman EM, Meeusen R (2010) Neuroplasticity-exercise-induced response of peripheral brain-derived neurotrophic factor: a systematic review of experimental studies in human subjects. Sports Med 40(9):765–801. doi: 10.2165/11534530-000000000-00000 PubMedCrossRefGoogle Scholar
  50. Kraemer WJ, Marchitelli L, Gordon SE, Harman E, Dziados JE, Mello R, Frykman P, McCurry D, Fleck SJ (1990) Hormonal and growth factor responses to heavy resistance exercise protocols. J Appl Physiol 69(4):1442–1450PubMedGoogle Scholar
  51. Kuang S, Gillespie MA, Rudnicki MA (2008) Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell 2(1):22–31. doi: 10.1016/j.stem.2007.12.012 PubMedCrossRefGoogle Scholar
  52. Laufs U, Werner N, Link A, Endres M, Wassmann S, Jurgens K, Miche E, Bohm M, Nickenig G (2004) Physical training increases endothelial progenitor cells, inhibits neointima formation, and enhances angiogenesis. Circulation 109(2):220–226. doi: 10.1161/01.CIR.0000109141.48980.37 PubMedCrossRefGoogle Scholar
  53. Lauritzen F, Paulsen G, Raastad T, Bergersen LH, Owe SG (2009) Gross ultrastructural changes and necrotic fiber segments in elbow flexor muscles after maximal voluntary eccentric action in humans. J Appl Physiol 107(6):1923–1934. doi: 10.1152/japplphysiol.00148.2009 PubMedCrossRefGoogle Scholar
  54. Lee JS, Bruce CR, Spurrell BE, Hawley JA (2002) Effect of training on activation of extracellular signal-regulated kinase 1/2 and p38 mitogen-activated protein kinase pathways in rat soleus muscle. Clin Exp Pharmacol Physiol 29(8):655–660PubMedCrossRefGoogle Scholar
  55. Leiter JR, Anderson JE (2010) Satellite cells are increasingly refractory to activation by nitric oxide and stretch in aged mouse-muscle cultures. Int J Biochem Cell Biol 42(1):132–136. doi: 10.1016/j.biocel.2009.09.021 PubMedCrossRefGoogle Scholar
  56. Li L, Clevers H (2010) Coexistence of quiescent and active adult stem cells in mammals. Science 327(5965):542–545. doi: 10.1126/science.1180794 PubMedCrossRefGoogle Scholar
  57. Lysy PA, Smets F, Najimi M, Sokal EM (2008) Leukemia inhibitory factor contributes to hepatocyte-like differentiation of human bone marrow mesenchymal stem cells. Differentiation 76(10):1057–1067. doi: 10.1111/j.1432-0436.2008.00287.x PubMedCrossRefGoogle Scholar
  58. Macaluso F, Brooks NE, van de Vyver M, Van Tubbergh K, Niesler CU, Myburgh KH (2011) Satellite cell count, VO(2max), and p38 MAPK in inactive to moderately active young men. Scand J Med Sci Sports. doi: 10.1111/j.1600-0838.2011.01389.x PubMedGoogle Scholar
  59. Macaluso F, Isaacs AW, Myburgh KH (2012) Preferential type II muscle fiber damage from plyometric exercise. J Athl Train 47(4)Google Scholar
  60. Machida S, Spangenburg EE, Booth FW (2003) Forkhead transcription factor FoxO1 transduces insulin-like growth factor’s signal to p27Kip1 in primary skeletal muscle satellite cells. J Cell Physiol 196(3):523–531. doi: 10.1002/jcp10339 PubMedCrossRefGoogle Scholar
  61. Mackey AL, Esmarck B, Kadi F, Koskinen SO, Kongsgaard M, Sylvestersen A, Hansen JJ, Larsen G, Kjaer M (2007) Enhanced satellite cell proliferation with resistance training in elderly men and women. Scand J Med Sci Sports 17(1):34–42. doi: 10.1111/j.1600-0838.2006.00534.x PubMedGoogle Scholar
  62. Mackey AL, Holm L, Reitelseder S, Pedersen TG, Doessing S, Kadi F, Kjaer M (2010) Myogenic response of human skeletal muscle to 12 weeks of resistance training at light loading intensity. Scand J Med Sci Sports. doi: 10.1111/j.1600-0838.2010.01178.x PubMedGoogle Scholar
  63. Malm C, Sjodin TL, Sjoberg B, Lenkei R, Renstrom P, Lundberg IE, Ekblom B (2004) Leukocytes, cytokines, growth factors and hormones in human skeletal muscle and blood after uphill or downhill running. J Physiol 556(Pt 3):983–1000. doi: 10.1113/jphysiol.2003.056598 PubMedCrossRefGoogle Scholar
  64. Mathieu ME, Saucourt C, Mournetas V, Gauthereau X, Theze N, Praloran V, Thiebaud P, Boeuf H (2011) LIF-Dependent Signaling: new Pieces in the Lego. Stem Cell Rev. doi: 10.1007/s12015-011-9261-7 Google Scholar
  65. Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495PubMedCrossRefGoogle Scholar
  66. McCroskery S, Thomas M, Maxwell L, Sharma M, Kambadur R (2003) Myostatin negatively regulates satellite cell activation and self-renewal. J Cell Biol 162(6):1135–1147. doi: 10.1083/jcb.200207056 PubMedCrossRefGoogle Scholar
  67. Mirzapour T, Movahedin M, Tengku Ibrahim TA, Haron AW, Nowroozi MR, Rafieian SH (2011) Effects of basic fibroblast growth factor and leukaemia inhibitory factor on proliferation and short-term culture of human spermatogonial stem cells. Andrologia. doi: 10.1111/j.1439-0272.2010.01135.x PubMedGoogle Scholar
  68. Mobius-Winkler S, Hilberg T, Menzel K, Golla E, Burman A, Schuler G, Adams V (2009) Time-dependent mobilization of circulating progenitor cells during strenuous exercise in healthy individuals. J Appl Physiol 107(6):1943–1950. doi: 10.1152/japplphysiol.00532.2009 PubMedCrossRefGoogle Scholar
  69. Moreau JF, Bonneville M, Godard A, Gascan H, Gruart V, Moore MA, Soulillou JP (1987) Characterization of a factor produced by human T cell clones exhibiting eosinophil-activating and burst-promoting activities. J Immunol 138(11):3844–3849PubMedGoogle Scholar
  70. Morici G, Zangla D, Santoro A, Pelosi E, Petrucci E, Gioia M, Bonanno A, Profita M, Bellia V, Testa U, Bonsignore MR (2005) Supramaximal exercise mobilizes hematopoietic progenitors and reticulocytes in athletes. Am J Physiol 289(5):R1496–R1503. doi: 10.1152/ajpregu.00338.2005 Google Scholar
  71. Nagata Y, Partridge TA, Matsuda R, Zammit PS (2006) Entry of muscle satellite cells into the cell cycle requires sphingolipid signaling. J Cell Biol 174(2):245–253. doi: 10.1083/jcb.200605028 PubMedCrossRefGoogle Scholar
  72. O’Reilly C, McKay B, Phillips S, Tarnopolsky M, Parise G (2008) Hepatocyte growth factor (HGF) and the satellite cell response following muscle lengthening contractions in humans. Muscle Nerve 38(5):1434–1442. doi: 10.1002/mus.21146 PubMedCrossRefGoogle Scholar
  73. Petrella JK, Kim JS, Mayhew DL, Cross JM, Bamman MM (2008) Potent myofiber hypertrophy during resistance training in humans is associated with satellite cell-mediated myonuclear addition: a cluster analysis. J Appl Physiol 104(6):1736–1742. doi: 10.1152/japplphysiol.01215.2007 PubMedCrossRefGoogle Scholar
  74. Reiss K, Cheng W, Ferber A, Kajstura J, Li P, Li B, Olivetti G, Homcy CJ, Baserga R, Anversa P (1996) Overexpression of insulin-like growth factor-1 in the heart is coupled with myocyte proliferation in transgenic mice. Proc Natl Acad Sci USA 93(16):8630–8635PubMedCrossRefGoogle Scholar
  75. Riekstina U, Muceniece R, Cakstina I, Muiznieks I, Ancans J (2008) Characterization of human skin-derived mesenchymal stem cell proliferation rate in different growth conditions. Cytotechnology 58(3):153–162. doi: 10.1007/s10616-009-9183-2 PubMedCrossRefGoogle Scholar
  76. Rubin MR, Kraemer WJ, Maresh CM, Volek JS, Ratamess NA, Vanheest JL, Silvestre R, French DN, Sharman MJ, Judelson DA, Gomez AL, Vescovi JD, Hymer WC (2005) High-affinity growth hormone binding protein and acute heavy resistance exercise. Med Sci Sports Exerc 37(3):395–403PubMedCrossRefGoogle Scholar
  77. Schabort EJ, Myburgh KH, Wiehe JM, Torzewski J, Niesler CU (2009) Potential myogenic stem cell populations: sources, plasticity, and application for cardiac repair. Stem cells and development 18(6):813–830. doi: 10.1089/scd.2008.0387 PubMedCrossRefGoogle Scholar
  78. Schabort EJ, van der Merwe M, Niesler CU (2011) TGF-beta isoforms inhibit IGF-1-induced migration and regulate terminal differentiation in a cell-specific manner. J Muscle Res Cell Motil 31(5–6):359–367. doi: 10.1007/s10974-011-9241-1 PubMedCrossRefGoogle Scholar
  79. Schertzer JD, Lynch GS (2006) Comparative evaluation of IGF-I gene transfer and IGF-I protein administration for enhancing skeletal muscle regeneration after injury. Gene Ther 13(23):1657–1664PubMedCrossRefGoogle Scholar
  80. Schmalbruch H, Hellhammer U (1976) The number of satellite cells in normal human muscle. Anat Rec 185(3):279–287. doi: 10.1002/ar.1091850303 PubMedCrossRefGoogle Scholar
  81. Serrano AL, Baeza-Raja B, Perdiguero E, Jardi M, Munoz-Canoves P (2008) Interleukin-6 is an essential regulator of satellite cell-mediated skeletal muscle hypertrophy. Cell Metab 7(1):33–44. doi: 10.1016/j.cmet.2007.11.011 PubMedCrossRefGoogle Scholar
  82. Shefer G, Van de Mark DP, Richardson JB, Yablonka-Reuveni Z (2006) Satellite-cell pool size does matter: defining the myogenic potency of aging skeletal muscle. Dev Biol 294(1):50–66. doi: 10.1016/j.ydbio.2006.02.022 PubMedCrossRefGoogle Scholar
  83. Shimatsu A, Rotwein P (1987) Mosaic evolution of the insulin-like growth factors. Organization, sequence, and expression of the rat insulin-like growth factor I gene. J Biol Chem 262(16):7894–7900PubMedGoogle Scholar
  84. Shinin V, Gayraud-Morel B, Gomes D, Tajbakhsh S (2006) Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol 8(7):677–687. doi: 10.1038/ncb1425 PubMedCrossRefGoogle Scholar
  85. Silva H, Conboy IM (2008) Aging and stem cell renewal. StemBook [Internet]. Harvard Stem Cell Institute, CambridgeGoogle Scholar
  86. Smith C, Kruger MJ, Smith RM, Myburgh KH (2008) The inflammatory response to skeletal muscle injury: illuminating complexities. Sports Med 38(11):947–969PubMedCrossRefGoogle Scholar
  87. Snijders T, Verdijk LB, Hansen D, Dendale P, van Loon LJ (2011) Continuous endurance-type exercise training does not modulate satellite cell content in obese type 2 diabetes patients. Muscle Nerve 43(3):393–401. doi: 10.1002/mus.21891 PubMedCrossRefGoogle Scholar
  88. Soltow QA, Lira VA, Betters JL, Long JH, Sellman JE, Zeanah EH, Criswell DS (2010) Nitric oxide regulates stretch-induced proliferation in C2C12 myoblasts. J Muscle Res Cell Motil 31(3):215–225. doi: 10.1007/s10974-010-9227-4 PubMedCrossRefGoogle Scholar
  89. Steiner S, Niessner A, Ziegler S, Richter B, Seidinger D, Pleiner J, Penka M, Wolzt M, Huber K, Wojta J, Minar E, Kopp CW (2005) Endurance training increases the number of endothelial progenitor cells in patients with cardiovascular risk and coronary artery disease. Atherosclerosis 181(2):305–310. doi: 10.1016/j.atherosclerosis.2005.01.006 PubMedCrossRefGoogle Scholar
  90. Sun L, Ma K, Wang H, Xiao F, Gao Y, Zhang W, Wang K, Gao X, Ip N, Wu Z (2007) JAK1-STAT1-STAT3, a key pathway promoting proliferation and preventing premature differentiation of myoblasts. J Cell Biol 179(1):129–138. doi: 10.1083/jcb.200703184 PubMedCrossRefGoogle Scholar
  91. Sun Y, Pollard S, Conti L, Toselli M, Biella G, Parkin G, Willatt L, Falk A, Cattaneo E, Smith A (2008) Long-term tripotent differentiation capacity of human neural stem (NS) cells in adherent culture. Mol Cell Neurosci 38(2):245–258. doi: 10.1016/j.mcn.2008.02.014 PubMedCrossRefGoogle Scholar
  92. Suzuki S, Yamanouchi K, Soeta C, Katakai Y, Harada R, Naito K, Tojo H (2002) Skeletal muscle injury induces hepatocyte growth factor expression in spleen. Biochem Biophys Res Commun 292(3):709–714. doi: 10.1006/bbrc.2002.6706 PubMedCrossRefGoogle Scholar
  93. Tatsumi R (2010) Mechano-biology of skeletal muscle hypertrophy and regeneration: possible mechanism of stretch-induced activation of resident myogenic stem cells. Anim Sci J 81(1):11–20. doi: 10.1111/j.1740-0929.2009.00712.x PubMedCrossRefGoogle Scholar
  94. Tatsumi R, Anderson JE, Nevoret CJ, Halevy O, Allen RE (1998) HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev Biol 194(1):114–128. doi: 10.1006/dbio.1997.8803 PubMedCrossRefGoogle Scholar
  95. Tatsumi R, Sheehan SM, Iwasaki H, Hattori A, Allen RE (2001) Mechanical stretch induces activation of skeletal muscle satellite cells in vitro. Exp Cell Res 267(1):107–114. doi: 10.1006/excr.2001.5252 PubMedCrossRefGoogle Scholar
  96. Tatsumi R, Wuollet AL, Tabata K, Nishimura S, Tabata S, Mizunoya W, Ikeuchi Y, Allen RE (2009) A role for calcium-calmodulin in regulating nitric oxide production during skeletal muscle satellite cell activation. Am J Physiol Cell Physiol 296(4):C922–C929. doi: 10.1152/ajpcell.00471.2008 PubMedCrossRefGoogle Scholar
  97. Ten Broek RW, Grefte S, Von den Hoff JW (2010) Regulatory factors and cell populations involved in skeletal muscle regeneration. J Cell Physiol 224(1):7–16. doi: 10.1002/jcp.22127 PubMedGoogle Scholar
  98. Trenerry MK, Della Gatta PA, Larsen AE, Garnham AP, Cameron-Smith D (2011a) Impact of resistance exercise training on interleukin-6 and JAK/STAT in young men. Muscle Nerve 43(3):385–392. doi: 10.1002/mus.21875 PubMedCrossRefGoogle Scholar
  99. Trenerry MK, Gatta PA, Cameron-Smith D (2011b) JAK/STAT signaling and human in vitro myogenesis. BMC Physiol 11:6. doi: 10.1186/1472-6793-11-6 PubMedCrossRefGoogle Scholar
  100. Turtikova OV, Altaeva EG, Tarakina MV, Malashenko AM, Nemirovskaya TL, Shenkman BS (2007) Muscle progenitor cell proliferation during passive stretch of unweighted soleus in dystrophin deficient mice. J Gravit Physiol 14(1):P95–P96PubMedGoogle Scholar
  101. Verdijk LB, Gleeson BG, Jonkers RA, Meijer K, Savelberg HH, Dendale P, van Loon LJ (2009) 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 64(3):332–339. doi: 10.1093/gerona/gln050 PubMedCrossRefGoogle Scholar
  102. Verney J, Kadi F, Charifi N, Feasson L, Saafi MA, Castells J, Piehl-Aulin K, Denis C (2008) Effects of combined lower body endurance and upper body resistance training on the satellite cell pool in elderly subjects. Muscle Nerve 38(3):1147–1154. doi: 10.1002/mus.21054 PubMedCrossRefGoogle Scholar
  103. Volonte D, Liu Y, Galbiati F (2005) The modulation of caveolin-1 expression controls satellite cell activation during muscle repair. FASEB J 19(2):237–239. doi: 10.1096/fj.04-2215fje PubMedGoogle Scholar
  104. Wahl P, Brixius K, Bloch W (2008) Exercise-induced stem cell activation and its implication for cardiovascular and skeletal muscle regeneration. Minim Invasive Ther Allied Technol 17(2):91–99. doi: 10.1080/13645700801969816 PubMedCrossRefGoogle Scholar
  105. Wallis M (2009) New insulin-like growth factor (IGF)-precursor sequences from mammalian genomes: the molecular evolution of IGFs and associated peptides in primates. Growth Horm IGF Res 19(1):12–23PubMedCrossRefGoogle Scholar
  106. Wozniak AC, Anderson JE (2007) Nitric oxide-dependence of satellite stem cell activation and quiescence on normal skeletal muscle fibers. Dev Dyn 236(1):240–250. doi: 10.1002/dvdy.21012 PubMedCrossRefGoogle Scholar
  107. Yablonka-Reuveni Z, Seger R, Rivera AJ (1999) Fibroblast growth factor promotes recruitment of skeletal muscle satellite cells in young and old rats. J Histochem Cytochem 47(1):23–42PubMedCrossRefGoogle Scholar
  108. Yamada M, Tatsumi R, Kikuiri T, Okamoto S, Nonoshita S, Mizunoya W, Ikeuchi Y, Shimokawa H, Sunagawa K, Allen RE (2006) Matrix metalloproteinases are involved in mechanical stretch-induced activation of skeletal muscle satellite cells. Muscle Nerve 34(3):313–319. doi: 10.1002/mus.20601 PubMedCrossRefGoogle Scholar
  109. Yamada M, Sankoda Y, Tatsumi R, Mizunoya W, Ikeuchi Y, Sunagawa K, Allen RE (2008) Matrix metalloproteinase-2 mediates stretch-induced activation of skeletal muscle satellite cells in a nitric oxide-dependent manner. Int J Biochem Cell Biol 40(10):2183–2191. doi: 10.1016/j.biocel.2008.02.017 PubMedCrossRefGoogle Scholar
  110. Yu M, Stepto NK, Chibalin AV, Fryer LG, Carling D, Krook A, Hawley JA, Zierath JR (2003) Metabolic and mitogenic signal transduction in human skeletal muscle after intense cycling exercise. J Physiol 546(Pt 2):327–335PubMedCrossRefGoogle Scholar
  111. Zoladz JA, Pilc A (2010) The effect of physical activity on the brain derived neurotrophic factor: from animal to human studies. J Physiol Pharmacol 61(5):533–541PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Dipartimento di Biomedicina Sperimentale e Neuroscienze ClinicheUniversità di PalermoPalermoItaly
  2. 2.Department of Physiological SciencesStellenbosch UniversityStellenboschSouth Africa

Personalised recommendations