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

  • EMC2012 Special Issue - Original Paper
  • Published:
Journal of Muscle Research and Cell Motility Aims and scope Submit manuscript

Abstract

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.

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References

  • Adams GR, McCue SA (1998) Localized infusion of IGF-I results in skeletal muscle hypertrophy in rats. J Appl Physiol 84(5):1716–1722

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Allen RE, Temm-Grove CJ, Sheehan SM, Rice G (1997) Skeletal muscle satellite cell cultures. Methods Cell Biol 52:155–176

    Article  PubMed  CAS  Google Scholar 

  • 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):1057–1070

    PubMed  CAS  Google Scholar 

  • 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–E390

    PubMed  CAS  Google Scholar 

  • Barton ER (2006) Viral expression of insulin-like growth factor-I isoforms promotes different responses in skeletal muscle. J Appl Physiol 100(6):1778–1784

    Article  PubMed  CAS  Google Scholar 

  • 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):1069–1076

    Article  PubMed  CAS  Google Scholar 

  • 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):763–776

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Broholm C, Pedersen BK (2010) Leukaemia inhibitory factor—an exercise-induced myokine. Exerc Immunol Rev 16:77–85

    PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Cannon JG, St Pierre BA (1998) Cytokines in exertion-induced skeletal muscle injury. Mol Cell Biochem 179(1–2):159–167

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Cotman CW, Berchtold NC, Christie LA (2007) Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 30(9):464–472

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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):189–197

    PubMed  CAS  Google Scholar 

  • Darr KC, Schultz E (1987) Exercise-induced satellite cell activation in growing and mature skeletal muscle. J Appl Physiol 63(5):1816–1821

    PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Doherty TJ (2003) Invited review: aging and sarcopenia. J Appl Physiol 95(4):1717–1727. doi:10.1152/japplphysiol.00347.2003

    PubMed  CAS  Google Scholar 

  • 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):819–821

    Article  PubMed  CAS  Google Scholar 

  • 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):6982–6988

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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):2803–2812

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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):39–51

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Grounds MD (1998) Age-associated changes in the response of skeletal muscle cells to exercise and regeneration. Ann N Y Acad Sci 854:78–91

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Hawke TJ, Garry DJ (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91(2):534–551

    PubMed  CAS  Google Scholar 

  • Hoch RV, Soriano P (2003) Roles of PDGF in animal development. Development 130(20):4769–4784. doi:10.1242/dev.00721

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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):1442–1450

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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):655–660

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Macaluso F, Isaacs AW, Myburgh KH (2012) Preferential type II muscle fiber damage from plyometric exercise. J Athl Train 47(4)

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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):3844–3849

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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):8630–8635

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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):395–403

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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):1657–1664

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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):7894–7900

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Silva H, Conboy IM (2008) Aging and stem cell renewal. StemBook [Internet]. Harvard Stem Cell Institute, Cambridge

  • Smith C, Kruger MJ, Smith RM, Myburgh KH (2008) The inflammatory response to skeletal muscle injury: illuminating complexities. Sports Med 38(11):947–969

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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–P96

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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):12–23

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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):23–42

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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):327–335

    Article  PubMed  CAS  Google Scholar 

  • 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):533–541

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Dipartimento di Biomedicina Sperimentale e Neuroscienze Cliniche, Università di Palermo, Via del Vespro, 129, Palermo, Italy

    F. Macaluso

  2. Department of Physiological Sciences, Stellenbosch University, Private Bag X1, Matieland, Stellenbosch, 7602, South Africa

    F. Macaluso & K. H. Myburgh

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  1. F. Macaluso
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  2. K. H. Myburgh
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Correspondence to F. Macaluso.

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Macaluso, F., Myburgh, K.H. Current evidence that exercise can increase the number of adult stem cells. J Muscle Res Cell Motil 33, 187–198 (2012). https://doi.org/10.1007/s10974-012-9302-0

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  • DOI: https://doi.org/10.1007/s10974-012-9302-0

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