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Pflügers Archiv

, Volume 451, Issue 2, pp 319–327 | Cite as

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

  • Fawzi KadiEmail author
  • Nadia Charifi
  • Christian Denis
  • Jan Lexell
  • Jesper L. Andersen
  • Peter Schjerling
  • Steen Olsen
  • Michael Kjaer
Invited Review

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.

Keywords

Skeletal muscle Satellite cell biology Myonuclei Strength training Human Fibre type Aging Hypertrophy 

References

  1. 1.
    Anderson JE, Wozniak AC (2004) Satellite cell activation on fibers: modeling events in vivo—an invited review. Can J Physiol Pharmacol 82:300–310CrossRefPubMedGoogle Scholar
  2. 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 9:297–299PubMedGoogle Scholar
  3. 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–E390Google Scholar
  4. 4.
    Bornemann A, Schmalbruch H (1994) Immunocytochemistry of M-cadherin in mature and regenerating rat muscle. Anat Rec 239:119–125CrossRefPubMedGoogle Scholar
  5. 5.
    Campion DR (1984) The muscle satellite cell: a review. Int Rev Cytol 87:225–251PubMedGoogle Scholar
  6. 6.
    Charge SB, Rudnicki MA (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev 84:209–238CrossRefPubMedGoogle Scholar
  7. 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 28:87–92CrossRefPubMedGoogle Scholar
  8. 8.
    Cornelison DD, Wold BJ (1997) Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191:270–283CrossRefPubMedGoogle Scholar
  9. 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 102:731–739CrossRefPubMedGoogle Scholar
  10. 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, LondonGoogle Scholar
  11. 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) 558:333–340CrossRefGoogle Scholar
  12. 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 66:49–59CrossRefPubMedGoogle Scholar
  13. 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–R801Google Scholar
  14. 14.
    Garry DJ, Yang Q, Bassel-Duby R, Williams RS (1997) Persistent expression of MNF identifies myogenic stem cells in postnatal muscles. Dev Biol 188:280–294CrossRefPubMedGoogle Scholar
  15. 15.
    Goldring K, Partridge T, Watt D (2002) Muscle stem cells. J Pathol 197:457–467CrossRefPubMedGoogle Scholar
  16. 16.
    Hall ZW, Ralston E (1989) Nuclear domains in muscle cells. Cell 59:771–772CrossRefPubMedGoogle Scholar
  17. 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) 547:247–245CrossRefGoogle Scholar
  18. 18.
    Hawke TJ, Garry DJ (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91:534–551PubMedGoogle Scholar
  19. 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 157:191–197CrossRefPubMedGoogle Scholar
  20. 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 55:347–354Google Scholar
  21. 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 8:419–427Google Scholar
  22. 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 31:46–52CrossRefPubMedGoogle Scholar
  23. 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 199:326–337PubMedGoogle Scholar
  24. 24.
    Kadi F (2000) Adaptation of human skeletal muscle to training and anabolic steroids. Acta Physiol Scand 646:1–52Google Scholar
  25. 25.
    Kadi F, Charifi N, Denis C, Lexell J (2004) Satellite cells and myonuclei in young and elderly women and men. Muscle Nerve 29:120–127CrossRefPubMedGoogle Scholar
  26. 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 111:189–195CrossRefPubMedGoogle Scholar
  27. 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 31:1528–1534CrossRefPubMedGoogle Scholar
  28. 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 121:329–334CrossRefPubMedGoogle Scholar
  29. 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) 558:1005–1012CrossRefGoogle Scholar
  30. 30.
    Kadi F, Thornell LE (1999) Training affects myosin heavy chain phenotype in the trapezius muscle of women. Histochem Cell Biol 112:73–78CrossRefPubMedGoogle Scholar
  31. 31.
    Kadi F, Thornell LE (2000) Concomitant increases in myonuclear and satellite cell content in female trapezius muscle following strength training. Histochem Cell Biol 113:99–103CrossRefPubMedGoogle Scholar
  32. 32.
    Kjaer M (2004) Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev 84:649–698CrossRefPubMedGoogle Scholar
  33. 33.
    Maier F, Bornemann A (1999) Comparison of the muscle fiber diameter and satellite cell frequency in human muscle biopsies. Muscle Nerve 22:578–583CrossRefPubMedGoogle Scholar
  34. 34.
    Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495PubMedGoogle Scholar
  35. 35.
    McLoon LK, Wirtschafter J (2003) Activated satellite cells in extraocular muscles of normal adult monkeys and humans. Invest Ophthalmol Vis Sci 44:1927–1923CrossRefPubMedGoogle Scholar
  36. 36.
    Moss FP, Leblond CP (1971) Satellite cells as the source of nuclei in muscles of growing rats. Anat Rec 170:421–435CrossRefPubMedGoogle Scholar
  37. 37.
    Pavlath GK, Rich K, Webster SG, Blau HM (1989) Localization of muscle gene products in nuclear domains. Nature 337:570–573CrossRefPubMedGoogle Scholar
  38. 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 315:233–242CrossRefPubMedGoogle Scholar
  39. 39.
    Renault V, Thornell LE, Eriksson PO, Butler-Browne G, Mouly V (2002) Regenerative potential of human skeletal muscle during aging. Aging Cell 1:132–139CrossRefPubMedGoogle Scholar
  40. 40.
    Rennie MJ, Wackerhage H, Spangenburg EE, Booth FW (2004) Control of the size of the human muscle mass. Annu Rev Physiol 66:799–828CrossRefPubMedGoogle Scholar
  41. 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 56:240–247Google Scholar
  42. 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 322:637–639CrossRefPubMedGoogle Scholar
  43. 43.
    Schmalbruch H, Hellhammer U (1976) The number of satellite cells in normal human muscle. Anat Rec 185:279–287CrossRefPubMedGoogle Scholar
  44. 44.
    Schmalbruch H, Lewis DM (2000) Dynamics of nuclei of muscle fibers and connective tissue cells in normal and denervated rat muscles. Muscle Nerve 23:617–626CrossRefPubMedGoogle Scholar
  45. 45.
    Schroder HD, Jensen CH, Jensen PB, Jorgensen LH, Andersen DC (2004) FA1/dlk1, a novel participant in muscle regeneration (Abstract). Neuromuscular Disorders 14:574Google Scholar
  46. 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 86:307–311PubMedGoogle Scholar
  47. 47.
    Schultz E, McCormick KM (1994) Skeletal muscle satellite cells. Rev Physiol Biochem Pharmacol 123:213–257PubMedGoogle Scholar
  48. 48.
    Seale P, Asakura A, Rudnicki MA (2001) The potential of muscle stem cells. Dev Cell 1:333–342CrossRefPubMedGoogle Scholar
  49. 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 102:777–786CrossRefPubMedGoogle Scholar
  50. 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–E143PubMedGoogle Scholar
  51. 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 222:6–11CrossRefPubMedGoogle Scholar
  52. 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 522:156–160CrossRefPubMedGoogle Scholar
  53. 53.
    Zammit P, Beauchamp J (2001) The skeletal muscle satellite cell: stem cell or son of stem cell? Differentiation 68:193–204CrossRefPubMedGoogle Scholar
  54. 54.
    Zhang M, McLennan IS (1994) Use of antibodies to identify satellite cells with a light microscope. Muscle Nerve 17:987–994CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Fawzi Kadi
    • 1
    Email author
  • Nadia Charifi
    • 1
    • 2
  • Christian Denis
    • 2
  • Jan Lexell
    • 3
  • Jesper L. Andersen
    • 4
  • Peter Schjerling
    • 4
  • Steen Olsen
    • 5
  • Michael Kjaer
    • 5
  1. 1.Department of Physical Education and HealthÖrebro UniversityÖrebroSweden
  2. 2.Laboratory of Physiology, GIP Exercise Sports& HealthUniversity Jean-MonnetSaint-EtienneFrance
  3. 3.Department of RehabilitationLund University HospitalLundSweden
  4. 4.Department of Molecular Muscle BiologyCopenhagen Muscle Research CentreCopenhagenDenmark
  5. 5.Institute of Sports MedicineBispebjerg HospitalCopenhagenDenmark

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