Skip to main content

Advertisement

SpringerLink
Log in

The skeletal muscle satellite cell response to a single bout of resistance-type exercise is delayed with aging in men

  • Published:
AGE Aims and scope Submit manuscript

Abstract

Skeletal muscle satellite cells (SCs) have been shown to be instrumental in the muscle adaptive response to exercise. The present study determines age-related differences in SC content and activation status following a single bout of exercise. Ten young (22 ± 1 years) and 10 elderly (73 ± 1 years) men performed a single bout of resistance-type exercise. Muscle biopsies were collected before and 12, 24, 48, and 72 h after exercise. SC content and activation status were assessed in type I and type II muscle fibers by immunohistochemistry. Myostatin and MyoD protein and messenger RNA (mRNA) expression were determined by Western blotting and rtPCR, respectively. In response to exercise, it took 48 h (young) and 72 h (elderly) for type II muscle fiber SC content to exceed baseline values (P < 0.01). The number of myostatin + SC in type I and II muscle fibers was significantly reduced after 12, 24, and 48 h of post-exercise recovery in both groups (P < 0.01), with a greater reduction observed at 24 and 48 h in the young compared with that in the elderly men (P < 0.01). In conclusion, the increase in type II muscle fiber SC content during post-exercise recovery is delayed with aging and is accompanied by a blunted SC activation response.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Adams GR, Caiozzo VJ, Haddad F, Baldwin KM (2002) Cellular and molecular responses to increased skeletal muscle loading after irradiation. Am J physiol Cell Physiol 283(4):C1182–1195

    Article  CAS  PubMed  Google Scholar 

  • Bergström J (1975) Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest 35(7):609–916

  • Bish LT, Morine KJ, Sleeper MM, Sweeney HL (2010) Myostatin is upregulated following stress in an Erk-dependent manner and negatively regulates cardiomyocyte growth in culture and in a mouse model. PLoS One 5(4):e10230

    Article  PubMed Central  PubMed  Google Scholar 

  • Cermak NM, Snijders T, McKay BR, Parise G, Verdijk LB, Tarnopolsky MA, Gibala MJ, Loon LJ (2013) Eccentric exercise increases satellite cell content in type II muscle fibers. Med Sci Sports Exerc 45(2):230–237

    Article  PubMed  Google Scholar 

  • Costa A, Dalloul H, Hegyesi H, Apor P, Csende Z, Racz L, Vaczi M, Tihanyi J (2007) Impact of repeated bouts of eccentric exercise on myogenic gene expression. Eur J Appl Physiol 101(4):427–436

    Article  PubMed  Google Scholar 

  • Dreyer HC, Blanco CE, Sattler FR, Schroeder ET, Wiswell RA (2006) Satellite cell numbers in young and older men 24 hours after eccentric exercise. Muscle Nerve 33(2):242–253

    Article  PubMed  Google Scholar 

  • Drummond MJ, Miyazaki M, Dreyer HC, Pennings B, Dhanani S, Volpi E, Esser KA, Rasmussen BB (2009) Expression of growth-related genes in young and older human skeletal muscle following an acute stimulation of protein synthesis. J Appl Physiol 106(4):1403–1411

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fiatarone MA, O’Neill EF, Ryan ND, Clements KM, Solares GR, Nelson ME, Roberts SB, Kehayias JJ, Lipsitz LA, Evans WJ (1994) Exercise training and nutritional supplementation for physical frailty in very elderly people. N Engl J Med 330(25):1769–1775

    Article  CAS  PubMed  Google Scholar 

  • Forbes D, Jackman M, Bishop A, Thomas M, Kambadur R, Sharma M (2006) Myostatin auto-regulates its expression by feedback loop through Smad7 dependent mechanism. J Cell Physiol 206(1):264–272

    Article  CAS  PubMed  Google Scholar 

  • Frontera WR, Meredith CN, O’Reilly KP, Knuttgen HG, Evans WJ (1988) Strength conditioning in older men: skeletal muscle hypertrophy and improved function. J Appl Physiol 64(3):1038–1044

    CAS  PubMed  Google Scholar 

  • Hameed M, Orrell RW, Cobbold M, Goldspink G, Harridge SD (2003) Expression of IGF-I splice variants in young and old human skeletal muscle after high resistance exercise. J Physiol 547(Pt 1):247–254

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Harris JA, Benedict FG (1918) A biometric study of human basal metabolism. Proc Natl Acad Sci U S A 4(12):370–373

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jespersen JG, Nedergaard A, Andersen LL, Schjerling P, Andersen JL (2011) Myostatin expression during human muscle hypertrophy and subsequent atrophy: increased myostatin with detraining. Scand J Med Sci Sports 21(2):215–223

    Article  CAS  PubMed  Google Scholar 

  • Kadi F, Thornell LE (2000) Concomitant increases in myonuclear and satellite cell content in female trapezius muscle following strength training. Histochem Cell Biol 113(2):99–103

    Article  CAS  PubMed  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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kim JS, Cross JM, Bamman MM (2005) Impact of resistance loading on myostatin expression and cell cycle regulation in young and older men and women. Am J Physiol Endocrinol Metab 288(6):E1110–1119

    Article  CAS  PubMed  Google Scholar 

  • Kim JS, Petrella JK, Cross JM, Bamman MM (2007) Load-mediated downregulation of myostatin mRNA is not sufficient to promote myofiber hypertrophy in humans: a cluster analysis. J Appl Physiol 103(5):1488–1495

    Article  CAS  PubMed  Google Scholar 

  • Kosek DJ, Kim JS, Petrella JK, Cross JM, Bamman MM (2006) Efficacy of 3 days/wk resistance training on myofiber hypertrophy and myogenic mechanisms in young vs. older adults. J Appl Physiol 101(2):531–544

    Article  CAS  PubMed  Google Scholar 

  • Kovacheva EL, Hikim AP, Shen R, Sinha I, Sinha-Hikim I (2010) Testosterone supplementation reverses sarcopenia in aging through regulation of myostatin, c-Jun NH2-terminal kinase, Notch, and Akt signaling pathways. Endocrinology 151(2):628–638

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Langley B, Thomas M, Bishop A, Sharma M, Gilmour S, Kambadur R (2002) Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. J Biol Chem 277(51):49831–49840

    Article  CAS  PubMed  Google Scholar 

  • Lee SJ (2004) Regulation of muscle mass by myostatin. Annu Rev Cell Dev Biol 20:61–86

    Article  CAS  PubMed  Google Scholar 

  • Lee S-J, Huynh T, Lee Y-S, Sebald S, Wilcox-Adelman S, Iwamori N, Lepper C, Matzuk M, Fan C-M (2012) Role of satellite cells versus myofibers in muscle hypertrophy induced by inhibition of the myostatin/activin signaling pathway. Proc Natl Acad Sci U S A 109(35):60

    Article  Google Scholar 

  • Leenders M, Verdijk LB, Hoeven LV, Kranenburg JV, Nilwik R, Wodzig WK, Senden JM, Keizer HA, Loon LJ (2013) Protein supplementation during resistance-type exercise training in the elderly. Med Sci Sports Exerc 45(3):542–552

    Article  CAS  PubMed  Google Scholar 

  • Leger B, Derave W, De Bock K, Hespel P, Russell AP (2008) Human sarcopenia reveals an increase in SOCS-3 and myostatin and a reduced efficiency of Akt phosphorylation. Rejuvenation Res 11(1):163–175B

    Article  PubMed  Google Scholar 

  • Lexell J, Taylor CC, Sjostrom M (1988) 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 84(2–3):275–294

    Article  CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Mackey A, Kjaer M, Charifi N, Henriksson J, Bojsen-Moller J, Holm L, Kadi F (2009) Assessment of satellite cell number and activity status in human skeletal muscle biopsies. Muscle Nerve 40(3):455–465

    Article  PubMed  Google Scholar 

  • Mayhew JL, Prinster JL, Ware JS, Zimmer DL, Arabas JR, Bemben MG (1995) Muscular endurance repetitions to predict bench press strength in men of different training levels. J Sports Med Phys Fitness 35(2):108–113

    CAS  PubMed  Google Scholar 

  • McCarthy JJ, Mula J, Miyazaki M, Erfani R, Garrison K, Farooqui AB, Srikuea R, Lawson BA, Grimes B, Keller C, Van Zant G, Campbell KS, Esser KA, Dupont-Versteegden EE, Peterson CA (2011) Effective fiber hypertrophy in satellite cell-depleted skeletal muscle. Development 138(17):3657–3666

    Article  CAS  PubMed Central  PubMed  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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • McFarlane C, Hui GZ, Amanda WZ, Lau HY, Lokireddy S, Xiaojia G, Mouly V, Butler-Browne G, Gluckman PD, Sharma M, Kambadur R (2011) Human myostatin negatively regulates human myoblast growth and differentiation. Am J Physiol Cell Physiol 301(1):C195–203

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • McKay BR, O’Reilly CE, Phillips SM, Tarnopolsky MA, Parise G (2008) Co-expression of IGF-1 family members with myogenic regulatory factors following acute damaging muscle-lengthening contractions in humans. J Physiol 586(Pt 22):5549–5560

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • McKay BR, De Lisio M, Johnston AP, O’Reilly CE, Phillips SM, Tarnopolsky MA, Parise G (2009) Association of interleukin-6 signalling with the muscle stem cell response following muscle-lengthening contractions in humans. PLoS One 4(6):e6027

    Article  PubMed Central  PubMed  Google Scholar 

  • McKay BR, Ogborn DI, Bellamy LM, Tarnopolsky MA, Parise G (2012) Myostatin is associated with age-related human muscle stem cell dysfunction. FASEB J 26(6):2509–2521

    Article  CAS  PubMed  Google Scholar 

  • McPherron AC, Lee SJ (1997) Double muscling in cattle due to mutations in the myostatin gene. Proc Natl Acad Sci U S A 94(23):12457–12461

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Megeney LA, Kablar B, Garrett K, Anderson JE, Rudnicki MA (1996) MyoD is required for myogenic stem cell function in adult skeletal muscle. Genes Dev 10(10):1173–1183

    Article  CAS  PubMed  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

    Article  PubMed  Google Scholar 

  • Petrella JK, Kim JS, Cross JM, Kosek DJ, Bamman MM (2006) Efficacy of myonuclear addition may explain differential myofiber growth among resistance-trained young and older men and women. Am J Physiol Endocrinol Metab 291(5):E937–946

    Article  CAS  PubMed  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

    Article  PubMed  Google Scholar 

  • Phillips SM, Tipton KD, Aarsland A, Wolf SE, Wolfe RR (1997) Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am J Physiol 273(1 Pt 1):E99–107

    CAS  PubMed  Google Scholar 

  • Raue U, Slivka D, Jemiolo B, Hollon C, Trappe S (2006) Myogenic gene expression at rest and after a bout of resistance exercise in young (18-30 yr) and old (80-89 yr) women. J Appl Physiol 101(1):53–59

    Article  CAS  PubMed  Google Scholar 

  • Rosenblatt J, Parry D (1992) Gamma irradiation prevents compensatory hypertrophy of overloaded mouse extensor digitorum longus muscle. J Appl Physiol (Bethesda, Md : 1985) 73(6):2538–2543

    CAS  Google Scholar 

  • Rosenblatt J, Parry D (1993) Adaptation of rat extensor digitorum longus muscle to gamma irradiation and overload. Pflugers Arch - Eur J Physiol 423(3–4):255–264

    Article  CAS  Google Scholar 

  • Rosenblatt J, Yong D, Parry D (1994) Satellite cell activity is required for hypertrophy of overloaded adult rat muscle. Muscle Nerve 17(6):608–613

    Article  CAS  PubMed  Google Scholar 

  • Siriett V, Platt L, Salerno MS, Ling N, Kambadur R, Sharma M (2006) Prolonged absence of myostatin reduces sarcopenia. J Cell Physiol 209(3):866–873

    Article  CAS  PubMed  Google Scholar 

  • Snijders T, Verdijk LB, Beelen M, McKay BR, Parise G, Kadi F, van Loon LJ (2012) A single bout of exercise activates skeletal muscle satellite cells during subsequent overnight recovery. Exp Physiol 97(6):762–773

    CAS  PubMed  Google Scholar 

  • Snijders T, Verdijk LB, McKay BR, Smeets JS, van Kranenburg J, Groen BB, Parise G, Greenhaff P, van Loon LJ (2014) Acute dietary protein intake restriction is associated with changes in myostatin expression after a single bout of resistance exercise in healthy young men. J Nutr 144(2):137–145

    Article  CAS  PubMed  Google Scholar 

  • Taylor WE, Bhasin S, Artaza J, Byhower F, Azam M, Willard DH Jr, Kull FC Jr, Gonzalez-Cadavid N (2001) Myostatin inhibits cell proliferation and protein synthesis in C2C12 muscle cells. Am J Physiol Endocrinol Metab 280(2):E221–228

    CAS  PubMed  Google Scholar 

  • Thomas M, Langley B, Berry C, Sharma M, Kirk S, Bass J, Kambadur R (2000) Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J Biol Chem 275(51):40235–40243

    Article  CAS  PubMed  Google Scholar 

  • Tieland M, Dirks ML, van der Zwaluw N, Verdijk LB, van de Rest O, de Groot LC, van Loon LJ (2012) Protein supplementation increases muscle mass gain during prolonged resistance-type exercise training in frail elderly people: a randomized, double-blind, placebo-controlled trial. J Am Med Dir Assoc 13(8):713–719

    Article  PubMed  Google Scholar 

  • Verdijk LB, Koopman R, Schaart G, Meijer K, Savelberg HH, van Loon LJ (2007) Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly. Am J Physiol Endocrinol Metab 292(1):E151–157

    Article  CAS  PubMed  Google Scholar 

  • Verdijk LB, Gleeson BG, Jonkers RA, Meijer K, Savelberg HH, Dendale P, van Loon LJ (2009a) 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

    Article  PubMed  Google Scholar 

  • Verdijk LB, Jonkers RA, Gleeson BG, Beelen M, Meijer K, Savelberg HH, Wodzig WK, Dendale P, van Loon LJ (2009b) Protein supplementation before and after exercise does not further augment skeletal muscle hypertrophy after resistance training in elderly men. Am J Clin Nutr 89(2):608–616

    Article  CAS  PubMed  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

    Article  PubMed  Google Scholar 

  • Wagner KR, Liu X, Chang X, Allen RE (2005) Muscle regeneration in the prolonged absence of myostatin. Proc Natl Acad Sci U S A 102(7):2519–2524

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Witard OC, Tieland M, Beelen M, Tipton KD, van Loon LJ, Koopman R (2009) Resistance exercise increases postprandial muscle protein synthesis in humans. Med Sci Sports Exerc 41(1):144–154

    Article  CAS  PubMed  Google Scholar 

  • Yablonka-Reuveni Z, Rivera AJ (1994) Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Dev Biol 164(2):588–603

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yang Y, Creer A, Jemiolo B, Trappe S (2005) Time course of myogenic and metabolic gene expression in response to acute exercise in human skeletal muscle. J Appl Physiol 98(5):1745–1752

    Article  CAS  PubMed  Google Scholar 

  • Yin H, Price F, Rudnicki M (2013) Satellite cells and the muscle stem cell niche. Physiol Rev 93(1):23–67

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Human Movement Sciences, Faculty of Health, Medicine and Life Sciences, Maastricht University, P.O. Box 616, 6200 MD, Maastricht, The Netherlands

    Tim Snijders, Lex B. Verdijk, Joey S. J. Smeets, Joan M. G. Senden & Luc J. C. van Loon

  2. Department of Kinesiology, McMaster University, Hamilton, Ontario, Canada

    Bryon R. McKay & Gianni Parise

  3. Department of Epidemiology, Maastricht University, Maastricht, The Netherlands

    Fred Hartgens

  4. Department of Surgery, Maastricht University, Maastricht, The Netherlands

    Fred Hartgens

  5. MRC/ARUK Centre for Musculoskeletal Ageing Research, The University of Nottingham, Queen’s Medical Centre, Nottingham, UK

    Paul Greenhaff

Authors
  1. Tim Snijders
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lex B. Verdijk
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joey S. J. Smeets
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bryon R. McKay
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joan M. G. Senden
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fred Hartgens
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gianni Parise
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Paul Greenhaff
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Luc J. C. van Loon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luc J. C. van Loon.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Snijders, T., Verdijk, L.B., Smeets, J.S.J. et al. The skeletal muscle satellite cell response to a single bout of resistance-type exercise is delayed with aging in men. AGE 36, 9699 (2014). https://doi.org/10.1007/s11357-014-9699-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11357-014-9699-z

Keywords

Search

Navigation