Muscle Stem Cell and Physical Activity: What Point is the Debate at?

Gabriele Ceccarelli, Laura Benedetti, Maria Luisa Arcari, Cecilia Carubbi, Daniela Galli, Gabriele Ceccarelli, Laura Benedetti, Maria Luisa Arcari, Cecilia Carubbi, Daniela Galli

Abstract

In the last 15 years, it emerged that the practice of regular physical activity reduces the risks of many diseases (cardiovascular diseases, diabetes, etc.) and it is fundamental in weight control and energy consuming to contrast obesity. Different groups proposed many molecular mechanisms as responsible for the positive effects of physical activity in healthy life. However, many points remain to be clarified. In this mini-review we reported the latest observations on the effects of physical exercise on healthy skeletal and cardiac muscle focusing on muscle stem cells. The last ones represent the fundamental elements for muscle regeneration post injury, but also for healthy muscle homeostasis. Interestingly, in both muscle tissues the morphological consequence of physical activity is a physiological hypertrophy that depends on different phenomena both in differentiated cells and stem cells. The signaling pathways for physical exercise effects present common elements in skeletal and cardiac muscle, like activation of specific transcription factors, proliferative pathways, and cytokines. More recently, post translational (miRNAs) or epigenetic (DNA methylation) modifications have been demonstrated. However, several points remain unresolved thus requiring new research on the effect of exercise on muscle stem cells.

Keywords: Cardiac muscle; Physical exercise; Skeletal muscle; Stem cell.

Conflict of interest statement

Conflict of interests: No authors report any conflict of interest.

Figures

Figure 1
Figure 1
Schematic representation of the effects of physical activity on skeletal muscle and heart. Panel A: muscle is shown like a cylinder with inside poly-nucleated fibers. Physical activity determines a morphological hypertrophy of muscle due to the increase in fiber numbers, in nuclei number per fiber and fiber size. Together with muscle hypertrophy, exercise induces proliferation of endothelial cells and release of proangiogenic and anti-angiogenic factors whose balance contributes to muscle adaptation to physical exercise. SC, Satellite Cells; Panel B: A schematic heart section is shown. Physical exercise determines cardiac hypertrophy (due to the increase of cardiomyocyte length, activation of cardiac stem cells and microvascular remodeling). RV, Right Ventricle; LV, Left Ventricle; IGF, Insulin Like Growth Factor 1; NRG-2, Neuregulin-2; NO, Nitric Oxide; CSCs, Cardiac Stem Cells; EPCs, Endothelial Progenitor Cells. In both panels, possible molecular mediators are reported.

References

    1. World Health Organization. Global recommandation of physical activity for health 2010. :1–58.
    1. Pedersen B. K., Saltin B.. Exercise as medicine - evidence for prescribing exercise as therapy in 26 different chronic diseases. Scand J Med Sci Sports. 2015;25:1–72. doi: 10.1111/sms.12581.
    1. Kemi OJ., Wisl⊘ff U.. Mechanisms of exercise-induced improvements in the contractile apparatus of the mammalian myocardium. Acta Physiol (Oxf) 2010;199:425–39. doi: 10.1111/j.1748-1716.2010.02132.x.
    1. Farup J., S⊘rensen H., Kj⊘lhede T.. Similar changes in muscle fiber phenotype with differentiated consequences for rate of force development: endurance versus resistance training. Hum Mov Sci. 2014;34:109–19. doi: 10.1016/j.humov.2014.01.005.
    1. Snijders T., Nederveen JP., Joanisse S., Leenders M., Verdijk LB., van Loon LJ., Parise G.. Muscle fibre capillarization is a critical factor in muscle fibre hypertrophy during resistance exercise training in older men. J Cachexia Sarcopenia Muscle. 2017;8:267–276. doi: 10.1002/jcsm.12137.
    1. Kingsley JD., Figueroa A.. Acute and training effects of resistance exercise on heart rate variability. Clin Physiol Funct Imaging. 2016;36:179–87. doi: 10.1111/cpf.12223.
    1. Isner-Horobeti ME., Dufour SP., Vautravers P., Geny B., Coudeyre E., Richard R.. Eccentric exercise training: modalities, applications and perspectives. Sports Med. 2013;43:483–512. doi: 10.1007/s40279-013-0052-y.
    1. Reid K.F., Fielding R.A.. Skeletal muscle power: a critical determinant of physical functioning in older adults. Exerc Sport Sci Rev. 2012;40:4–12. doi: 10.1097/JES.0b013e31823b5f13.
    1. Shulman G.I., Rothman D.L., Jue T., Stein P., DeFronzo R.A., Shulman R.G.. Quantitation of muscle glycogen synthesis in normal subjects and subjects with non-insulin-dependent diabetes by 13C nuclear magnetic resonance spectroscopy. N Engl J Med. 1990;322:223–228. doi: 10.1056/NEJM199001253220403.
    1. Pozefsky T., Tancredi R.G., Moxley R.T., Dupre J., Tobin J.D.. Effects of brief starvation on muscle amino acid metabolism in nonobese man. J Clin Invest. 1976;57:444–9. doi: 10.1172/JCI108295.
    1. Canepari M., Pellegrino M.A., D’Antona G., Bottinelli R.. Skeletal muscle fibre diversity and the underlying mechanisms. Acta Physiol (Oxf) 2010;199:465–76. doi: 10.1111/j.1748-1716.2010.02118.x.
    1. Schiaffino S., Dyar K.A., Ciciliot S., Blaauw B., Sandri M.. Mechanisms regulating skeletal muscle growth and atrophy. FEBS J. 2013;280:4294–314. doi: 10.1111/febs.12253.
    1. Brook M.S., Wilkinson D.J., Phillips B.E., Perez-Schindler J., Philp A., Smith K., Atherton P. J.. Skeletal muscle homeostasis and plasticity in youth and ageing: impact of nutrition and exercise. Acta Physiol (Oxf) 2016;2016;216:15–41. doi: 10.1111/apha.12532.
    1. Damas F., Phillips S., Vechin F.C., Ugrinowitsch C.. A review of resistance training-induced changes in skeletal muscle protein synthesis and their contribution to hypertrophy. Sports Med. 2015;45:801–7. doi: 10.1007/s40279-015-0320-0.
    1. Ozaki H., Loenneke J.P., Thiebaud R.S., Abe T.. Cycle training induces muscle hypertrophy and strength gain: strategies and mechanisms. Acta Physiol Hung. 2015;102:1–22. doi: 10.1556/APhysiol.102.2015.1.1.
    1. Abruzzo P.M., Esposito F., Marchionni C., di Tullio S., Belia S., Fulle S.. et al. Moderate exercise training induces ROS-related adaptations to skeletal muscles. Int J Sports Med. 2013;34:676–87. doi: 10.1055/s-0032-1323782.
    1. Lexell J., Taylor C.C., Sjöström M.. What is the cause of the ageing atrophy, Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci. 1988;84:275–94.
    1. Verdijk L.B., Koopman R., Schaart G., Meijer K., Savelberg H.H., van Loon L.J.. Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly. Am J Physiol Endocrinol Metab. 2007;292:E151–7. doi: 10.1152/ajpendo.00278.2006.
    1. Wang X., Pickrell AM., Rossi SG., Pinto M., Dillon LM., Hida A.. et al. Transient systemic mtDNA damage leads to muscle wasting by reducing the satellite cell pool. Hum Mol Genet. 2013;22:3976–86. doi: 10.1093/hmg/ddt251.
    1. Zampieri S., Mammucari C., Romanello V., Barberi L., Pietrangelo L., Fusella A.. et al. Physical exercise in aging human skeletal muscle increases mitochondrial calcium uniporter expression levels and affects mitochondria dynamics. Physiol Rep. 2016;4(24):e13005. doi: 10.14814/phy2.13005. Erratum in: Physiol Rep. 2017 Mar,5(6)
    1. Matsakas A., Macharia R., Otto A., Elashry M.I., Mouisel E., Romanello V.. et al. Exercise training attenuates the hypermuscular phenotype and restores skeletal muscle function in the myostatin null mouse. Exp Physiol. 2012;97:125–40. doi: 10.1113/expphysiol.2011.063008.
    1. Konopka A.R., Harber M.P.. Skeletal muscle hypertrophy after aerobic exercise training. Exerc Sport Sci Rev. 2014;42:53–61. doi: 10.1249/JES.0000000000000007.
    1. McGregor R.A., Poppitt S.D., Cameron-Smith D.. Role of microRNAs in the age-related changes in skeletal muscle and diet or exercise interventions to promote healthy aging in humans. Ageing Res Rev. 2014;17:25–33. doi: 10.1016/j.arr.2014.05.001.
    1. McCarthy J.J., Esser K.A., Andrade F.H.. MicroRNA-206 is overexpressed in the diaphragm but not the hindlimb muscle of mdx mouse. Am J Physiol Cell Physiol. 2007;293:C451–7. doi: 10.1152/ajpcell.00077.2007.
    1. Davidsen P.K., Gallagher I.J., Hartman J.W., Tarnopolsky M.A., Dela F., Helge J.W.. et al. High responders to resistance exercise training demonstrate differential regulation of skeletal muscle microRNA expression. J Appl Physiol. 1985;2011;110:309–17. doi: 10.1152/japplphysiol.00901.2010.
    1. Mueller M., Breil F.A., Lurman G., Klossner S., Flück M., Billeter R., Däpp C., Hoppeler H.. Different molecular and structural adaptations with eccentric and conventional strength training in elderly men and women. Gerontology. 2011;57:528–38. doi: 10.1159/000323267.
    1. Camera D.M., Ong J.N., Coffey V.G., Hawley J.A.. Selective Modulation of MicroRNA Expression with Protein Ingestion Following Concurrent Resistance and Endurance Exercise in Human Skeletal Muscle. Front Physiol. 2016;7:87. doi: 10.3389/fphys.2016.00087.
    1. Masi LN., Serdan TD., Levada-Pires AC., Hatanaka E., Silveira LD., Cury-Boaventura MF.. et al. Regulation of Gene Expression by Exercise-Related Micrornas. Cell Physiol Biochem. 2016;39:2381–2397. doi: 10.1159/000452507.
    1. Barrès R., Yan J., Egan B., Treebak J.T., Rasmussen M., Fritz T.. et al. Acute exercise remodels promoter methylation in human skeletal muscle. Cell Metab. 2012;15:405–11. doi: 10.1016/j.cmet.2012.01.001.
    1. Laker R.C., Ryall J.G.. DNA Methylation in Skeletal Muscle Stem Cell Specification, Proliferation, and Differentiation. Stem Cells Int. 2016:5725927. doi: 10.1155/2016/5725927.
    1. Gehlert S., Klinz F.J., Willkomm L., Schiffer T., Suhr F., Bloch W.. Intense Resistance Exercise Promotes the Acute and Transient Nuclear Translocation of Small Ubiquitin-Related Modifier (SUMO)-1 in Human Myofibres. Int J Mol Sci. 2016;17:pii:E646. doi: 10.3390/ijms17050646.
    1. Mauro A.. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol. 1961;9:493–5.
    1. Yin H., Price F., Rudnicki M.A.. Satellite cells and the muscle stem cell niche. Physiol Rev. 2013;93:23–67. doi: 10.1152/physrev.00043.2011.
    1. Snijders T., Verdijk L.B., Beelen M., McKay B.R., Parise G., Kadi F., van Loon L.J.. A single bout of exercise activates skeletal muscle satellite cells during subsequent overnight recovery. Exp Physiol. 2012;97:762–73. doi: 10.1113/expphysiol.2011.063313.
    1. van de Vyver M., Myburgh K.H.. Cytokine and satellite cell responses to muscle damage: interpretation and possible confounding factors in human studies. J Muscle Res Cell Motil. 2012;33:177–85. doi: 10.1007/s10974-012-9303-z.
    1. Walker D.K., Fry C.S., Drummond M.J., Dickinson J.M., Timmerman K.L., Gundermann D.M.. et al. PAX7+ satellite cells in young and older adults following resistance exercise. Muscle Nerve. 2012;46:51–9. doi: 10.1002/mus.23266.
    1. Cermak N.M., Snijders T., McKay B.R., Parise G., Verdijk L.B., Tarnopolsky M.A.. et al. Eccentric exercise increases satellite cell content in type II muscle fibers. Med Sci Sports Exerc. 2013;45:230–7. doi: 10.1249/MSS.0b013e318272cf47.
    1. Hanssen K.E., Kvamme N.H., Nilsen T.S., R⊘nnestad B., Ambj⊘rnsen I.K., Norheim F.. et al. The effect of strength training volume on satellite cells, myogenic regulatory factors, and growth factors. Scand J Med Sci Sports. 2013;23:728–39. doi: 10.1111/j.1600-0838.2012.01452.x.
    1. Mangan G., Bombardier E., Mitchell A.S., Quadrilatero J., Tiidus P.M.. Oestrogen-dependent satellite cell activation and proliferation following a running exercise occurs via the PI3K signalling pathway and not IGF-1. Acta Physiol (Oxf) 2014;212:75–85. doi: 10.1111/apha.12317.
    1. Oishi Y., Tsukamoto H., Yokokawa T., Hirotsu K., Shimazu M., Uchida K.. et al. Mixed lactate and caffeine compound increases satellite cell activity and anabolic signals for muscle hypertrophy. J Appl Physiol (1985) 2015;118:742–9. doi: 10.1152/japplphysiol.00054.2014.
    1. Caldow M.K., Thomas E.E., Dale M.J., Tomkinson G.R., Buckley J.D., Cameron-Smith D.. Early myogenic responses to acute exercise before and after resistance training in young men. Physiol Rep. 2015 Sep;3;9:pii: e12511. doi: 10.14814/phy2.12511.
    1. Macaluso F., Brooks N.E., van de Vyver M., Van Tubbergh K., Niesler C.U., Myburgh K.H.. Satellite cell count, VO(2max), and p38 MAPK in inactive to moderately active young men. Scand J Med Sci Sports. 2012;22:e38–44. doi: 10.1111/j.1600-0838.2011.01389.x.
    1. Frese S., Ruebner M., Suhr F., Konou T.M., Tappe K.A., Toigo M.. et al. Long-Term Endurance Exercise in Humans Stimulates Cell Fusion of Myoblasts along with Fusogenic Endogenous Retroviral Genes In Vivo. PLoS One. 2015;10:e0132099. doi: 10.1371/journal.pone.0132099.
    1. McKenzie AI., D’Lugos AC., Saunders MJ., Gworek KD., Luden ND.. Fiber Type-Specific Satellite Cell Content in Cyclists Following Heavy Training with Carbohydrate and Carbohydrate-Protein Supplementation. Front Physiol. 2016;7:550. doi: 10.3389/fphys.2016.00550. eCollection 2016.
    1. Dinulovic I., Furrer R., Beer M., Ferry A., Cardel B., Handschin C.. Muscle PGC-1α modulates satellite cell number and proliferation by remodeling the stem cell niche. Skelet Muscle. 2016;6:39. doi: 10.1186/s13395-016-0111-9.
    1. Friday B..B, Mitchell P.O., Kegley K.M., Pavlath G.K.. Calcineurin initiates skeletal muscle differentiation by activating MEF2 and MyoD. Differentiation. 2003;71:217–27. doi: 10.1046/j.1432-0436.2003.710303.x.
    1. Gehlert S., Bloch W., Suhr F.. Ca2+-dependent regulations and signaling in skeletal muscle: from electro-mechanical coupling to adaptation. Int J Mol Sci. 2015;16:1066–95. doi: 10.3390/ijms16011066.
    1. Dalbo V.J., Roberts M.D.. The activity of satellite cells and myonuclei during 8 weeks of strength training in young men with suppressed testosterone. Acta Physiol (Oxf) 2015;213:556–8. doi: 10.1111/apha.12411.
    1. Vahidi Ferdousi L., Rocheteau P., Chayot R., Montagne B., Chaker Z., Flamant P.. et al. More efficient repair of DNA double-strand breaks in skeletal muscle stem cells compared to their committed progeny. Stem Cell Res. 2014;13:492–507. doi: 10.1016/j.scr.2014.08.005.
    1. Taivassalo T., Fu K., Johns T., Arnold D., Karpati G., Shoubridge EA.. Gene shifting: a novel therapy for mitochondrial myopathy. Hum Mol Genet. 1999;8:1047–52. .
    1. Schultz E., McCormick KM.. Skeletal muscle satellite cells. Rev Physiol Biochem Pharmacol. 1994;123:213–57.
    1. Murphy JL., Blakely EL., Schaefer AM., He L., Wyrick P., Haller RG.. et al. Resistance training in patients with single, large-scale deletions of mitochondrial DNA. Brain. 2008;131:2832–40. doi: 10.1093/brain/awn252.
    1. Spendiff S., Reza M., Murphy JL., Gorman G., Blakely EL., Taylor RW.. et al. Mitochondrial DNA deletions in muscle satellite cells: implications for therapies. Hum Mol Genet. 2013;22:4739–47. doi: 10.1093/hmg/ddt327.
    1. Murach KA., Walton RG., Fry CS., Michaelis SL., Groshong JS., Finlin BS.. et al. Cycle training modulates satellite cell and transcriptional responses to a bout of resistance exercise. Physiol Rep. 2016:pii: e12973. doi: 10.14814/phy2.12973. Sep;4(18)
    1. Nederveen JP., Snijders T., Joanisse S., Wavell CG., Mitchell CJ., Johnston LM.. et al. Altered muscle satellite cell activation following 16 wk of resistance training in young men. Am J Physiol Regul Integr Comp Physiol. 2017;312:R–85. doi: 10.1152/ajpregu.00221.2016.
    1. Rowlands D.S., Nelson A.R., Raymond F., Metairon S., Mansourian R., Clarke J.. et al. Protein-leucine ingestion activates a regenerative inflammo-myogenic transcriptome in skeletal muscle following intense endurance exercise. Physiol Genomics. 2016;48:21–32. doi: 10.1152/physiolgenomics.00068.2015.
    1. Peake J.M., Della Gatta P., Suzuki K., Nieman D.C.. Cytokine expression and secretion by skeletal muscle cells: regulatory mechanisms and exercise effects. Exerc Immunol Rev. 2015;21:8–25.
    1. Hiscock N., Chan M.H., Bisucci T., Darby I.A., Febbraio M.A.. Skeletal myocytes are a source of interleukin-6 mRNA expression and protein release during contraction: evidence of fiber type specificity. FASEB J. 2004;18:992–4. doi: 10.1096/fj.03-1259fje.
    1. Hoier B., Walker M., Passos M., Walker P.J., Green A., Bangsbo J.. et al. Angiogenic response to passive movement and active exercise in individuals with peripheral arterial disease. J Appl Physiol (1985) 2013;115:1777–87. doi: 10.1152/japplphysiol.00979.2013.
    1. Hubal M.J., Chen T.C., Thompson P.D., Clarkson P.M.. Inflammatory gene changes associated with the repeated-bout effect. Am J Physiol Regul Integr Comp Physiol. 2008;294:R1628–37. doi: 10.1152/ajpregu.00853.2007.
    1. Paulsen G., Mikkelsen U.R., Raastad T., Peake J.M.. Leucocytes, cytokines and satellite cells: what role do they play in muscle damage and regeneration following eccentric exercise? Exerc Immunol Rev. 2012;18:42–97.
    1. Saclier M., Cuvellier S., Magnan M., Mounier R., Chazaud B.. Monocyte/macrophage interactions with myogenic precursor cells during skeletal muscle regeneration. FEBS J. 2013;Sep;280(17):4118–30. doi: 10.1111/febs.12166.
    1. Olfert I.M., Baum O., Hellsten Y., Egginton S.. Advances and challenges in skeletal muscle angiogenesis. Am J Physiol Heart Circ Physiol. 2016;310:H326–36. doi: 10.1152/ajpheart.00635.2015.
    1. Polesskaya A., Degerny C., Pinna G., Maury Y., Kratassiouk G., Mouly V.. et al. Genome-wide exploration of miRNA function in mammalian muscle cell differentiation. PLoS One. 2013;8:e71927. doi: 10.1371/journal.pone.0071927.
    1. Hashemi Gheinani A., Burkhard F.C., Rehrauer H., Aquino Fournier C., Monastyrskaya K.. MicroRNA MiR-199a-5p regulates smooth muscle cell proliferation and morphology by targeting WNT2 signaling pathway. J Biol Chem. 2015;290:7067–86. doi: 10.1074/jbc.M114.618694.
    1. Bentzinger CF., Wang YX., von Maltzahn J., Rudnicki MA.. The emerging biology of muscle stem cells: implications for cell-based therapies. Bioessays. 2013;35:231–41. doi: 10.1002/bies.201200063.
    1. De Lisio M., Farup J., Sukiennik R.A., Clevenger N., Nallabelli J., Nelson B.. et al. The acute response of pericytes to muscledamaging eccentric contraction and protein supplementation in human skeletal muscle. J Appl Physiol (1985) 2015;119:900–7. doi: 10.1152/japplphysiol.01112.2014.
    1. Farup J., De Lisio M., Rahbek S.K., Bjerre J., Vendelbo M.H., Boppart M.D., Vissing K.. Pericyte response to contraction mode-specific resistance exercise training in human skeletal muscle. J Appl Physiol. 1985;2015;119:1053–63. doi: 10.1152/japplphysiol.01108.2014. Epub 2015 Sep 24. PubMed PMID: 26404620.
    1. Zou K., Huntsman H.D., Carmen Valero M., Adams J., Skelton J., De Lisio M.. et al. Mesenchymal stem cells augment the adaptive response to eccentric exercise. Med Sci Sports Exerc. 2015;47:315–25. doi: 10.1249/MSS.0000000000000405.
    1. Sacchetti B., Funari A., Remoli C., Giannicola G., Kogler G., Liedtke S.. et al. No Identical “Mesenchymal Stem Cells” at Different Times and Sites: Human Committed Progenitors of Distinct Origin and Differentiation Potential Are Incorporated as Adventitial Cells in Microvessels. Stem Cell Reports. 2016;6:897–913. doi: 10.1016/j.stemcr.2016.05.011.
    1. Kostallari E., Baba-Amer Y., Alonso-Martin S., Ngoh P., Relaix F., Lafuste P., Gherardi R.K.. Pericytes in the myovascular niche promote post-natal myofiber growth and satellite cell quiescence. Development. 2015;142:1242–53. doi: 10.1242/dev.115386.
    1. Hyldahl R.D., Xin L., Hubal M.J., Moeckel-Cole S., Chipkin S., Clarkson P.M.. Activation of nuclear factor-κB following muscle eccentric contractions in humans is localized primarily to skeletal muscle-residing pericytes. FASEB J. 2011;25:2956–66. doi: 10.1096/fj.10-177105.
    1. LaBarbera K.E., Hyldahl R.D., O’Fallon K.S., Clarkson P.M., Witkowski S.. Pericyte NF-κB activation enhances endothelial cell proliferation and proangiogenic cytokine secretion in vitro. Physiol Rep. 2015;3:pii: e12309. doi: 10.14814/phy2.12309.
    1. Valero M.C., Huntsman H.D., Liu J., Zou K., Boppart M.D.. Eccentric exercise facilitates mesenchymal stem cell appearance in skeletal muscle. PLoS One. 2012;7:e29760. doi: 10.1371/journal.pone.0029760.
    1. Valero M.C., Huntsman H.D., Liu J., Zou K., Boppart M.D.. Eccentric exercise facilitates mesenchymal stem cell appearance in skeletal muscle. PLoS One. 2012;7:e29760. doi: 10.1371/journal.pone.0029760.
    1. Liese A.D., Krebs-Smith S.M., Subar A.F., George S.M., Harmon B.E., Neuhouser M.L.. et al. The Dietary Patterns Methods Project: synthesis of findings across cohorts and relevance to dietary guidance. J Nutr. 2015;145:393–402. doi: 10.3945/jn.114.205336.
    1. Wilson M.G., Ellison G.M., Cable N.T.. Basic science behind the cardiovascular benefits of exercise. Br J Sports Med. 2016;50:93–9. doi: 10.1136/bjsports-2014-306596rep.
    1. Nayor M., Vasan R.S.. Preventing heart failure: the role of physical activity. Curr Opin Cardiol. 2015;30:543–50. doi: 10.1097/HCO.0000000000000206.
    1. Després J.P.. Physical Activity, Sedentary Behaviours, and Cardiovascular Health: When Will Cardiorespiratory Fitness Become a Vital Sign? Can J Cardiol. 2016;32:505–13. doi: 10.1016/j.cjca.2015.12.006.
    1. Fernandes T., Baraúna V.G., Negrão C.E., Phillips M.I., Oliveira E.M.. Aerobic exercise training promotes physiological cardiac remodeling involving a set of microRNAs. Am J Physiol Heart Circ Physiol. 2015;309:H543–52. doi: 10.1152/ajpheart.00899.2014.
    1. Kwak H.B.. Aging, exercise, and extracellular matrix in the heart. J Exerc Rehabil. 2013;9:338–47. doi: 10.12965/jer.130049.
    1. Wasfy M.M., Weiner R.B.. Differentiating the athlete’s heart from hypertrophic cardiomyopathy. Curr Opin Cardiol. 2015;30:500–5. doi: 10.1097/HCO.0000000000000203.Review.
    1. Izumo S., Lompré A.M., Matsuoka R., Koren G., Schwartz K., Nadal-Ginard B., Mahdavi V.. Myosin heavy chain messenger RNA and protein isoform transitions during cardiac hypertrophy. Interaction between hemodynamic and thyroid hormone-induced signals. J Clin Invest. 1987;79:970–7. doi: 10.1172/JCI112908.
    1. Izumo S., Nadal-Ginard B., Mahdavi V.. Protooncogene induction and reprogramming of cardiac gene expression produced by pressure overload. Proc Natl Acad Sci U S A. 1988;85:339–43. PMID: 2963328.
    1. MacLellan WR., Schneider MD.. Genetic dissection of cardiac growth control pathways. Annu Rev Physiol. 2000;62:289–319. doi: 10.1146/annurev.physiol.62.1.289.
    1. McMullen J.R., Shioi T., Zhang L., Tarnavski O., Sherwood M.C., Kang P.M., Izumo S.. Phosphoinositide 3-kinase(p110alpha) plays a critical role for the induction of physiological, but not pathological, cardiac hypertrophy. Proc Natl Acad Sci U S A. 2003;100:12355–60. doi: 10.1073/pnas.1934654100.
    1. Sadoshima J., Izumo S.. The cellular and molecular response of cardiac myocytes to mechanical stress. Annu Rev Physiol. 1997;59:551–71. doi: 10.1146/annurev.physiol.59.1.551.
    1. Akazawa H., Komuro I.. Roles of cardiac transcription factors in cardiac hypertrophy. Circ Res. 2003;92:1079–88. doi: 10.1161/01.RES.0000072977.86706.23.
    1. Kwak H.B., Song W., Lawler J.M.. Exercise training attenuates age-induced elevation in Bax/Bcl-2 ratio, apoptosis, and remodeling in the rat heart. FASEB J. 2006;20:791–3. doi: 10.1096/fj.05-5116fje.
    1. Kwak H.B., Kim J.H., Joshi K., Yeh A., Martinez D.A., Lawler J.M.. Exercise training reduces fibrosis and matrix metalloproteinase dysregulation in the aging rat heart. FASEB J. 2011;25:1106–17. doi: 10.1096/fj.10-172924.
    1. Tao L., Bei Y., Zhang H., Xiao J., Li X.. Exercise for the heart: signaling pathways. Oncotarget. 2015;6:20773–84. doi: 10.18632/oncotarget.4770.
    1. Marini M., Lapalombella R., Margonato V., Ronchi R., Samaja M., Scapin C.. et al. Mild exercise training, cardioprotection and stress genes profile. Eur J Appl Physiol. 2007;99:503–10. doi: 10.1007/s00421-006-0369-4.
    1. Nizielski S.E., Arizmendi C., Shteyngarts A.R., Farrell C.J., Friedman J.E.. Involvement of transcription factor C/EBP-beta in stimulation of PEPCK gene expression during exercise. Am J Physiol. 1996 May;270;:1005–12. (5 Pt 2):R. PubMed PMID: 8928898.
    1. Weeks K.L., McMullen J.R.. The athlete’s heart vs. the failing heart: can signaling explain the two distinct outcomes? Physiology (Bethesda) 2011;26:97–105. doi: 10.1152/physiol.00043.2010.
    1. van Rooij E., Sutherland L.B., Liu N., Williams A.H., McAnally J., Gerard R.D.. et al. A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure. Proc Natl Acad Sci U S A. 2006;103:18255–60. doi: 10.1073/pnas.0608791103.
    1. Zhao Y., Ransom J.F., Li A., Vedantham V., von Drehle M., Muth A.N.. et al. Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell. 2007;129:303–17. doi: 10.1016/j.ce11.2007.03.030.
    1. Eulalio A., Mano M., Dal Ferro M., Zentilin L., Sinagra G., Zacchigna S., Giacca M.. Functional screening identifies miRNAs inducing cardiac regeneration. Nature. 2012;492:376–81. doi: 10.1038/nature11739.
    1. Xu J., Liu Y., Xie Y., Zhao C., Wang H.. Bioinformatics Analysis Reveals MicroRNAs Regulating Biological Pathways in Exercise-Induced Cardiac Physiological Hypertrophy. Biomed Res Int. 2017;2017:2850659. doi: 10.1155/2017/2850659.
    1. Melo S.F., Barauna V.G., Júnior M.A., Bozi L.H., Drummond L.R., Natali A.J., de Oliveira E.M.. Resistance training regulates cardiac function through modulation of miRNA-214. Int J Mol Sci. 2015;16:6855–67. doi: 10.3390/ijms16046855.
    1. Baggish A.L., Hale A., Weiner R.B., Lewis G.D., Systrom D., Wang F.. et al. Dynamic regulation of circulating microRNA during acute exhaustive exercise and sustained aerobic exercise training. J Physiol. 2011;589:3983–94. doi: 10.1113/jphysiol.2011.213363.
    1. Sawada S., Kon M., Wada S., Ushida T., Suzuki K., Akimoto T.. Profiling of circulating microRNAs after a bout of acute resistance exercise in humans. PLoS One. 2013;8:e70823. doi: 10.1371/journal.pone.0070823.
    1. Leite C.F., Lopes C.S., Alves A.C., Fuzaro C.S., Silva M.V., Oliveira L.F.. et al. Endogenous resident c-Kit cardiac stem cells increase in mice with an exercise-induced, physiologically hypertrophied heart. Stem Cell Res. 2015;15:151–64. doi: 10.1016/j.scr.2015.05.011.
    1. Torella D., Ellison G.M., Méndez-Ferrer S., Ibanez B., Nadal-Ginard B.. Resident human cardiac stem cells: role in cardiac cellular homeostasis and potential for myocardial regeneration. Nat Clin Pract Cardiovasc Med. 2006;3:S8–13. doi: 10.1038/ncpcardio0409.
    1. Bergmann O., Bhardwaj R.D., Bernard S., Zdunek S., Barnabe-Heider F., Walsh S.. et al. Evidence for cardiomyocyte renewal in humans. Science. 2009;324:98–102. doi: 10.1126/science.1164680.
    1. Ellison G.M., Waring C.D., Vicinanza C., Torella D.. Physiological cardiac remodelling in response to endurance exercise training: cellular and molecular mechanisms. Heart. 2012;98:5–10. doi: 10.1136/heartjnl-2011-300639.
    1. Schuler G., Adams V., Goto Y.. Role of exercise in the prevention of cardiovascular disease: results, mechanisms, and new perspectives. Eur Heart J. 2013;34:1790–9. doi: 10.1093/eurheartj/eht111.
    1. Dimmeler S., Burchfield J., Zeiher A.M.. Cell-based therapy of myocardial infarction. Arterioscler Thromb Vasc Biol. 2008;28:208–16. doi: 10.1161/ATVBAHA.107.155317.
    1. Landers-Ramos R.Q., Sapp R.M., Jenkins N.T., Murphy A.E., Cancre L., Chin E.R.. et al. Chronic endurance exercise affects paracrine action of CD31+ and CD34+ cells on endothelial tube formation. Am J Physiol Heart Circ Physiol. 2015;309:H407–20. doi: 10.1152/ajpheart.00123.2015.
    1. Galli D., Vitale M., Vaccarezza M.. Bone marrow-derived mesenchymal cell differentiation toward myogenic lineages: facts and perspectives. Biomed Res Int. 2014;2014:762695. doi: 10.1155/2014/762695.

Source: PubMed

3
구독하다