Skip to main content

Advertisement

Log in

The behaviour of satellite cells in response to exercise: what have we learned from human studies?

  • Invited Review
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

Understanding the complex role played by satellite cells in the adaptive response to exercise in human skeletal muscle has just begun. The development of reliable markers for the identification of satellite cell status (quiescence/activation/proliferation) is an important step towards the understanding of satellite cell behaviour in exercised human muscles. It is hypothesised currently that exercise in humans can induce (1) the activation of satellite cells without proliferation, (2) proliferation and withdrawal from differentiation, (3) proliferation and differentiation to provide myonuclei and (4) proliferation and differentiation to generate new muscle fibres or to repair segmental fibre injuries. In humans, the satellite cell pool can increase as early as 4 days following a single bout of exercise and is maintained at higher level following several weeks of training. Cessation of training is associated with a gradual reduction of the previously enhanced satellite cell pool. In the elderly, training counteracts the normal decline in satellite cell number seen with ageing. When the transcriptional activity of existing myonuclei reaches its maximum, daughter cells generated by satellite cell proliferation are involved in protein synthesis by enhancing the number of nuclear domains. Clearly, delineating the events and the mechanisms behind the activation of satellite cells both under physiological and pathological conditions in human skeletal muscles remains an important challenge.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Anderson JE, Wozniak AC (2004) Satellite cell activation on fibers: modeling events in vivo—an invited review. Can J Physiol Pharmacol 82:300–310

    Article  PubMed  Google Scholar 

  2. Appell HJ, Forsberg S, Hollmann W (1988) Satellite cell activation in human skeletal muscle after training: evidence for muscle fiber neoformation. Int J Sports Med 9:297–299

    PubMed  Google Scholar 

  3. Bamman MM, Shipp JR, Jiang J, Gower BA, Hunter GR, Goodman A, McLafferty CL, Urban RJ (2001) Mechanical load increases muscle IGF-I and androgen receptor mRNA concentrations in humans. Am J Physiol 280:E383–E390

    Google Scholar 

  4. Bornemann A, Schmalbruch H (1994) Immunocytochemistry of M-cadherin in mature and regenerating rat muscle. Anat Rec 239:119–125

    Article  PubMed  Google Scholar 

  5. Campion DR (1984) The muscle satellite cell: a review. Int Rev Cytol 87:225–251

    PubMed  Google Scholar 

  6. Charge SB, Rudnicki MA (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev 84:209–238

    Article  PubMed  Google Scholar 

  7. 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 28:87–92

    Article  PubMed  Google Scholar 

  8. Cornelison DD, Wold BJ (1997) Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191:270–283

    Article  PubMed  Google Scholar 

  9. Covault J, Merlie JP, Goridis C, Sanes JR (1986) Molecular forms of N-CAM and its RNA in developing and denervated skeletal muscle. J Cell Biol 102:731–739

    Article  PubMed  Google Scholar 

  10. Crameri R, Aagaard P, Qvortrup K, Møller M, Kjáer M (2004) N-CAM and Pax-7 immunoreactive cells are expressed differently in the human vastus lateralis after a single bout of exhaustive eccentric exercise (Abstract). Physiological society, Kings College, London

  11. 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 (Lond) 558:333–340

    Article  Google Scholar 

  12. Floridon C, Jensen CH, Thorsen P, Nielsen O, Sunde L, Westergaard JG, Thomsen SG, Teisner B (2000) Does fetal antigen 1 (FA1) identify cells with regenerative, endocrine and neuroendocrine potentials? A study of FA1 in embryonic, fetal, and placental tissue and in maternal circulation. Differentiation 66:49–59

    Article  PubMed  Google Scholar 

  13. Flück M, Chiquet M, Schmutz S, Mayet-Sornay MH, Desplanches D (2003) Reloading of atrophied rat soleus muscle induces tenascin-C expression around damaged muscle fibers. Am J Physiol 284:R792–R801

    Google Scholar 

  14. Garry DJ, Yang Q, Bassel-Duby R, Williams RS (1997) Persistent expression of MNF identifies myogenic stem cells in postnatal muscles. Dev Biol 188:280–294

    Article  PubMed  Google Scholar 

  15. Goldring K, Partridge T, Watt D (2002) Muscle stem cells. J Pathol 197:457–467

    Article  PubMed  Google Scholar 

  16. Hall ZW, Ralston E (1989) Nuclear domains in muscle cells. Cell 59:771–772

    Article  PubMed  Google Scholar 

  17. 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 (Lond) 547:247–245

    Article  Google Scholar 

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

    PubMed  Google Scholar 

  19. Hellsten Y, Hansson HA, Johnson L, Frandsen U, Sjodin B (1996) Increased expression of xanthine oxidase and insulin-like growth factor I (IGF-I) immunoreactivity in skeletal muscle after strenuous exercise in humans. Acta Physiol Scand 157:191–197

    Article  PubMed  Google Scholar 

  20. Hikida RS, Staron RS, Hagerman FC, Walsh S, Kaiser E, Shell S, Hervey S (2000) Effects of high-intensity resistance training on untrained older men. II. Muscle fiber characteristics and nucleo-cytoplasmic relationships. J Gerontol A Biol Sci Med Sci 55:347–354

    Google Scholar 

  21. Hikida RS, Walsh S, Barylski N, Campos G, Hagerman FC, Staron RS (1998) Is hypertrophy limited in elderly muscle fibers? A comparison of elderly and young strength-trained men. Basic Appl Myol 8:419–427

    Google Scholar 

  22. Illa I, Leon-Monzon M, Dalakas MC (1992) Regenerating and denervated human muscle fibers and satellite cells express neural cell adhesion molecule recognized by monoclonal antibodies to natural killer cells. Ann Neurol 31:46–52

    Article  PubMed  Google Scholar 

  23. Irintchev A, Zeschnigk M, Starzinski-Powitz A, Wernig A (1994) Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles. Dev Dyn 199:326–337

    PubMed  Google Scholar 

  24. Kadi F (2000) Adaptation of human skeletal muscle to training and anabolic steroids. Acta Physiol Scand 646:1–52

    Google Scholar 

  25. Kadi F, Charifi N, Denis C, Lexell J (2004) Satellite cells and myonuclei in young and elderly women and men. Muscle Nerve 29:120–127

    Article  PubMed  Google Scholar 

  26. Kadi F, Eriksson A, Holmner S, Butler-Browne GS, Thornell LE (1999) Cellular adaptation of the trapezius muscle in strength-trained athletes. Histochem Cell Biol 111:189–195

    Article  PubMed  Google Scholar 

  27. Kadi F, Eriksson A, Holmner S, Thornell L-E (1999) Effects of anabolic steroids on the muscle cells of strength-trained athletes. Med Sci Sports Exerc 31:1528–1534

    Article  PubMed  Google Scholar 

  28. Kadi F, Johansson F, Johansson R, Sjostrom M, Henriksson J (2004) Effects of one bout of endurance exercise on the expression of myogenin in human quadriceps muscle. Histochem Cell Biol 121:329–334

    Article  PubMed  Google Scholar 

  29. 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 (Lond) 558:1005–1012

    Article  Google Scholar 

  30. Kadi F, Thornell LE (1999) Training affects myosin heavy chain phenotype in the trapezius muscle of women. Histochem Cell Biol 112:73–78

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  32. Kjaer M (2004) Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev 84:649–698

    Article  PubMed  Google Scholar 

  33. Maier F, Bornemann A (1999) Comparison of the muscle fiber diameter and satellite cell frequency in human muscle biopsies. Muscle Nerve 22:578–583

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  35. McLoon LK, Wirtschafter J (2003) Activated satellite cells in extraocular muscles of normal adult monkeys and humans. Invest Ophthalmol Vis Sci 44:1927–1923

    Article  PubMed  Google Scholar 

  36. Moss FP, Leblond CP (1971) Satellite cells as the source of nuclei in muscles of growing rats. Anat Rec 170:421–435

    Article  PubMed  Google Scholar 

  37. Pavlath GK, Rich K, Webster SG, Blau HM (1989) Localization of muscle gene products in nuclear domains. Nature 337:570–573

    Article  PubMed  Google Scholar 

  38. Reimann J, Brimah K, Schroder R, Wernig A, Beauchamp JR, Partridge TA (2004) Pax7 distribution in human skeletal muscle biopsies and myogenic tissue cultures. Cell Tissue Res 315:233–242

    Article  PubMed  Google Scholar 

  39. Renault V, Thornell LE, Eriksson PO, Butler-Browne G, Mouly V (2002) Regenerative potential of human skeletal muscle during aging. Aging Cell 1:132–139

    Article  PubMed  Google Scholar 

  40. Rennie MJ, Wackerhage H, Spangenburg EE, Booth FW (2004) Control of the size of the human muscle mass. Annu Rev Physiol 66:799–828

    Article  PubMed  Google Scholar 

  41. Roth SM, Martel GF, Ivey FM, Lemmer JT, Tracy BL, Metter EJ, Hurley BF, Rogers MA (2001) Skeletal muscle satellite cell characteristics in young and older men and women after heavy resistance strength training. J Gerontol A Biol Sci Med Sci 56:240–247

    Google Scholar 

  42. Salviati G, Biasia E, Aloisi M (1986) Synthesis of fast myosin induced by fast ectopic innervation of rat soleus muscle is restricted to the ectopic endplate region. Nature 322:637–639

    Article  PubMed  Google Scholar 

  43. Schmalbruch H, Hellhammer U (1976) The number of satellite cells in normal human muscle. Anat Rec 185:279–287

    Article  PubMed  Google Scholar 

  44. Schmalbruch H, Lewis DM (2000) Dynamics of nuclei of muscle fibers and connective tissue cells in normal and denervated rat muscles. Muscle Nerve 23:617–626

    Article  PubMed  Google Scholar 

  45. Schroder HD, Jensen CH, Jensen PB, Jorgensen LH, Andersen DC (2004) FA1/dlk1, a novel participant in muscle regeneration (Abstract). Neuromuscular Disorders 14:574

    Google Scholar 

  46. Schubert W, Zimmermann K, Cramer M, Starzinski-Powitz A (1989) Lymphocyte antigen Leu-19 as a molecular marker of regeneration in human skeletal muscle. Proc Natl Acad Sci USA 86:307–311

    PubMed  Google Scholar 

  47. Schultz E, McCormick KM (1994) Skeletal muscle satellite cells. Rev Physiol Biochem Pharmacol 123:213–257

    PubMed  Google Scholar 

  48. Seale P, Asakura A, Rudnicki MA (2001) The potential of muscle stem cells. Dev Cell 1:333–342

    Article  PubMed  Google Scholar 

  49. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102:777–786

    Article  PubMed  Google Scholar 

  50. Singh MA, Ding W, Manfredi TJ, Solares GS, O’Neill EF, Clements KM, Ryan ND, Kehayias JJ, Fielding RA, Evans WJ (1999) Insulin-like growth factor I in skeletal muscle after weight-lifting exercise in frail elders. Am J Physiol 277:E135–E143

    PubMed  Google Scholar 

  51. Watkins SC, Cullen MJ (1988) A quantitative study of myonuclear and satellite cell nuclear size in Duchenne’s muscular dystrophy, polymyositis and normal human skeletal muscle. Anat Rec 222:6–11

    Article  PubMed  Google Scholar 

  52. Yang SY, Goldspink G (2002) Different roles of the IGF-I Ec peptide (MGF) and mature IGF-I in myoblast proliferation and differentiation. FEBS Lett 522:156–160

    Article  PubMed  Google Scholar 

  53. Zammit P, Beauchamp J (2001) The skeletal muscle satellite cell: stem cell or son of stem cell? Differentiation 68:193–204

    Article  PubMed  Google Scholar 

  54. Zhang M, McLennan IS (1994) Use of antibodies to identify satellite cells with a light microscope. Muscle Nerve 17:987–994

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fawzi Kadi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kadi, F., Charifi, N., Denis, C. et al. The behaviour of satellite cells in response to exercise: what have we learned from human studies?. Pflugers Arch - Eur J Physiol 451, 319–327 (2005). https://doi.org/10.1007/s00424-005-1406-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-005-1406-6

Keywords

Navigation