Skip to main content
SpringerLink
Log in

Satellite cell depletion in degenerative skeletal muscle

  • Published:
Apoptosis Aims and scope Submit manuscript

Abstract

Adult skeletal muscle has the striking ability to repair and regenerate itself after injury. This would not be possible without satellite cells, a subpopulation of cells existing at the margin of the myofiber. Under most conditions, satellite cells are quiescent, but they are activated in response to trauma, enabling them to guide skeletal muscle regeneration. In degenerative skeletal muscle states, including motor nerve denervation, advanced age, atrophy secondary to deconditioning or immobilization, and Duchenne muscular dystrophy, satellite cell numbers and proliferative potential significantly decrease, contributing to a diminution of skeletal muscle's regenerative capacity and contractility. This review will highlight the fate of satellite cells in several degenerative conditions involving skeletal muscle, and will attempt to gauge the relative contributions of apoptosis, senescence, impaired proliferative potential, and host factors to satellite cell dysfunction.

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

Similar content being viewed by others

References

  1. Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 1961; 9: 493–495.

    Google Scholar 

  2. Hawke TJ, Garry DJ. Myogenic satellite cells: Physiology to molecular biology. J Appl Physiol 2001; 91: 534–551.

    Google Scholar 

  3. Lu DX, Huang SK, Carlson BM. Electron microscopic study of long-term denervated rat skeletal muscle. Anat Rec 1997; 248: 355–365.

    Google Scholar 

  4. Bischoff R. The satellite cell and muscle regeneration. In: Engel AG and Frazini-Armstrong C, ed. Myology. New York: McGraw-Hill 1994: 97–118.

    Google Scholar 

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

    Google Scholar 

  6. Gibson MC, Schultz E. Age-related differences in absolute numbers of skeletal muscle satellite cells. Muscle Nerve 1983; 6: 574–580.

    Google Scholar 

  7. Webster C, Blau HM. Accelerated age-related decline in replicative life-span of Duchenne muscular dystrophy myoblasts: Implications for cell and gene therapy. Somatic Cell Mol Genet 1990; 16: 557–565.

    Google Scholar 

  8. Heslop L, Morgan JE, Partridge TA. Evidence for a myogenic stem cell that is exhausted in dystrophic muscle. J Cell Sci 2000; 113: 2299–2308.

    Google Scholar 

  9. de Castro Rodrigues A, Schmalbruch H. Satellite cells and myonuclei in long-term denervated rat muscles. Anat Rec 1995; 243: 430–437.

    Google Scholar 

  10. Snow MH. The effects of aging on satellite cells in skeletal muscles of mice and rats. Cell Tissue Res 1977; 185: 399–408.

    Google Scholar 

  11. Schultz E, Jaryszak DL. Effects of skeletal muscle regeneration on the proliferation potential of satellite cells. Mech Ageing Dev 1985; 30: 63–72.

    Google Scholar 

  12. Darr KC, Schultz E. Hindlimb suspension suppresses muscle growth and satellite cell proliferation. J Appl Physiol 1989; 67: 1827–1834.

    Google Scholar 

  13. Schultz E, Darr KC, Marius A. Acute effects of hindlimb unweighting on satellite cells of growing skeletal muscle. J Appl Physiol 1994; 76: 266–270.

    Google Scholar 

  14. Schultz E, Lipton BH. Skeletal muscle satellite cells: Changes in proliferation potential as a function of age. Mech Ageing Dev 1982; 20: 377–383.

    Google Scholar 

  15. Carlson BM, Faulkner JA. Muscle regeneration in young and old rats: Effects of motor nerve transection with and without marcaine treatment. J Gerontol A Biol Sci Med Sci 1998; 53: B52–B57.

    Google Scholar 

  16. Brooks SV, Faulkner, JA. Contraction-induced injury: Recovery of skeletal muscles in young and old mice. Am J Physiol 1990; 258: C436–C442.

    Google Scholar 

  17. Grounds MD. Age-associated changes in the response of skeletal muscle to exercise and regeneration. Ann NY Acad Sci 1998; 854: 78–91.

    Google Scholar 

  18. Roth SM, Martel GF, Ivey FM, et al. Skeletal muscle satellite cell populations in healthy young and older men and women. Anat Rec 2000; 260: 351–358.

    Google Scholar 

  19. Renault V, Piron-Hamelin G, Forestier C, et al. Skeletal muscle regeneration and the mitotic clock. Exp Gerontol 2000; 35: 711–719.

    Google Scholar 

  20. Jejurikar SS, Cederna PS, Marcelo CL, Kuzon WM. Aging promotes satellite cell apoptosis (abstract). J Am Coll Surg 2002; 195: S46.

    Google Scholar 

  21. Carlson BM, Faulkner JA. Muscle transplantation between young and old rats: Age of host determines recovery. Am J Physiol Cell Physiol 1989; 256: C1262–C1266.

    Google Scholar 

  22. Carlson BM, Faulkner JA. The regeneration of noninnervated muscle grafts and marcaine-treated muscles in young and old rats. J Gerontol A Biol Sci Med Sci 1996; 51: B43–B49.

    Google Scholar 

  23. Danon D, Kowatch MA, Roth GS. Promotion of wound repair in old mice by local injection of macrophages. Proc Natl Acad Sci USA 1989; 86: 2018–2020.

    Google Scholar 

  24. Ullman M, Ullman A, Sommerland H, Skottner A, Oldfors A. Effects of growth hormone on muscle regeneration and IGF-I concentration in old rats. Acta Physiol Scand 1990; 140: 521–525.

    Google Scholar 

  25. Chakravarthy MV, Davis BS, Booth FW. IGF-I restores satellite cell proliferative potential in immobilized old skeletal muscle. J Appl Physiol 2000; 89: 1365–1379.

    Google Scholar 

  26. Napier JR, Thomas MF, Sharma M, Hodgkinson SC, Bass JJ. Insulin-like growth factor-I protects myoblasts from apoptosis but requires other factors to stimulate proliferation. J Endocrinology 1999; 163: 63–68.

    Google Scholar 

  27. Sunderland S, Ray LJ. Denervation changes in mammalian striated muscle. J Neurology Neurosurg Psych 1950; 13: 159–177.

    Google Scholar 

  28. Tower S. The reaction of muscle to denervation. Physiol Rev 1939; 19: 1–48.

    Google Scholar 

  29. Viguie CA, Lu DX, Huang SK, Rengen H, Carlson BM. Quantitative study of the effects of long-term denervation on the extensor digitorum longus muscle of the rat. Anat Rec 1997; 248: 346–354

    Google Scholar 

  30. Sunderland S. Traumatized nerves, roots and ganglia: Musculoskeletal factors and neuropathological consequences. In: Korr IM, ed. The Neurobiologic Mechanisms in Manipulative Therapy. New York: Plenum 1978: 137–166.

    Google Scholar 

  31. Borisov AB, Carlson BM. Cell death in denervated skeletal muscle is distinct from classical apoptosis. Anat Rec 2000; 258: 305–318.

    Google Scholar 

  32. Jejurikar SS, Marcelo CL, Kuzon WM. Skeletal muscle denervation increases satellite cell susceptibility to apoptosis. Plast Recons Surg 2001; 110: 160–168.

    Google Scholar 

  33. Raff MC, Barres BA, Burne JF, Coles HS, Ishizaki Y, Jacobson MD. Programmed cell death and the control of cell survival: Lessons from the nervous system. Science 1993; 262: 695–700.

    Google Scholar 

  34. Oppenheim RW. Cell death during development of the nervous system. Ann Rev Neurosci 1991; 14: 453–501.

    Google Scholar 

  35. Grounds MD. Muscle regeneration: Molecular aspects and therapeutic implications. Curr Opin Neurol 1999; 12: 535–543.

    Google Scholar 

  36. Winograd CH, Gerety MB, Chung M, Goldstein MK, Dominguez F, Vallone R. Screening for frailty: Criteria and predictors of outcome. J Am Geriatr Soc 1991; 39: 778–784.

    Google Scholar 

  37. Fitts RH, Metzger JM, Riley DA, Unsworth BR. Models of disuse: A comparison of hindlimb suspension and immobilization. J Appl Physiol 1986; 60: 1946–1953.

    Google Scholar 

  38. Mozdziak PE, Pulvermacher PM, Schultz E. Unloading of juvenile muscle results in a reduced muscle size 9 weeks after reloading. J Appl Physiol 2000; 88: 158–164.

    Google Scholar 

  39. Booth FW. Regrowth of atrophied skeletal muscle in adult rats after ending immobilization. J Appl Physiol 1978; 44: 225–230.

    Google Scholar 

  40. Wanek LJ, Snow MH. Activity-induced fiber regeneration in rat soleus muscle. Anat Rec 2000; 258: 176–185.

    Google Scholar 

  41. Rosenblatt JD, Yong D, Parry DJ. Satellite cell activity is required for hypertrophy of overloaded adult rat muscle. Muscle Nerve 1994; 17: 608–613.

    Google Scholar 

  42. Schultz E, Jaryszak DL, Valliere CR. Response of satellite cells to focal skeletal muscle injury. Muscle Nerve 1985; 8: 217–222.

    Google Scholar 

  43. Nathan CF. Secretory products of macrophages. J Clin Invest 1987; 79: 319–326.

    Google Scholar 

  44. Lescaudron L, Peltekian E, Fontaine-Perus J, et al. Blood borne macrophages are essential for the triggering of muscle regeneration following muscle transplant. Neuromuscul Disord 1999; 9: 72–80.

    Google Scholar 

  45. Vierck J, O'Reilly B, Hossner K, et al. Satellite cell regulation following myotrauma caused by resistance exercise. Cell Biol Int 2000; 24: 263–272.

    Google Scholar 

  46. Tatsumi R, Anderson JE, Nevoret CJ, Halevy O, Allen RE. HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev Biol 1998; 194: 114–128.

    Google Scholar 

  47. Sheehan SM, Allen RE. Skeletal muscle satellite cell proliferation in response to members of the fibroblast growth factor family and hepatocyte growth factor. J Cell Physiol 1999; 181: 499–506.

    Google Scholar 

  48. Kurek JB, Bower JJ, Romanella M, Koentgen F, Murphy M, Austin L. The role of leukemia inhibitory factor in skeletal muscle regeneration. Muscle Nerve 1997; 20: 815–822.

    Google Scholar 

  49. Martin JF, Li L, Olson EN. Repression of myogenin function by TGF-?1 is targeted at the basic helix-loop-helix motif and is independent of E2A products. J Biol Chem 1992; 267: 10956–10960.

    Google Scholar 

  50. Kami K, Senba E. Localization of leukemia inhibitory factor and interleukin-6 messenger ribonucleic acids in regenerating rat skeletal muscle. Muscle Nerve 1998; 21: 819–822.

    Google Scholar 

  51. Brooks SV, Opiteck JA, Faulkner JA. Conditioning of skeletal muscle in adult and old mice for protection from contractioninduced injury. J Gerontol A Biol Sci 2001; 56A: B163–B171.

    Google Scholar 

  52. McCully KK, Faulkner JA. Injury to skeletal muscle fibers of mice following lengthening contractions. J Appl Physiol 1985; 59: 119–126.

    Google Scholar 

  53. Newham DJ, McPhail G, Mills DR, Edwards RHT. Ultrastructural changes after concentric and eccentric contractions. J Neurol Sci 1983; 61: 109–122.

    Google Scholar 

  54. Brooks SV, Faulkner JA. The magnitude of the initial injury induced by stretches of maximally activated muscle fibres of mice and rats increases in old age. J Physiol (London) 1996; 497: 573–580.

    Google Scholar 

  55. Faulkner JA, Brooks SV, Zerba E. Muscle atrophy and weakness with aging: Contraction-induced injury as an underlying mechanism. J Gerontol A Biol Sci Med Sci 1995; 50A: 124–129.

    Google Scholar 

  56. England SB, Nicholson LV, Johnson MA, et al. Very mild muscular dystrophy associated with the deletion of 46% of dystrphin. Nature 1990; 343: 180–182.

    Google Scholar 

  57. Rybakova IN, Patel JR, Ervasti JM. The dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin. J Cell Biol 2000; 150: 1209–1214.

    Google Scholar 

  58. Cossu G, Mavilio F. Myogenic stem cells for the therapy of primary myopathies:Wishful thinking or therapeutic perspective? J Clin Invest 2000; 105: 1669–1674.

    Google Scholar 

  59. McDonald CM, Abresch RT, Carter GT, et al. Profiles of neuromuscular diseases: Duchenne muscular dystrophy. Am J Phys Med Rehabil 1995; 74(suppl): S70–S92.

    Google Scholar 

  60. Decary S, Hamida CB, Mouly V, Barbet JP, Hentati F, Butler-Browne GS. Shorter telomeres in dystrophic muscle consistent with extensive regeneration in young children. Neuromuscul Disord 2000; 10: 113–120.

    Google Scholar 

  61. Melone MA, Peluso G, Galderisi U, Petillo O, Cotrufo R. Increased expression of IGF-binding protein-5 in Duchenne muscular dystrophy (DMD) fibroblasts correlates with the fibroblast-induced downregulation of DMD myoblast growth: An in vitro analysis. J Cell Physiol 2000; 185: 143–153.

    Google Scholar 

  62. Doumit ME, Cook DR, Merkel RA. Fibroblast growth factor, epidermal growth factor, insulin-like growth factors, and platelet-derived growth factor-BB stimulate proliferation of clonally derived porcine myogenic satellite cells. J Cell Physiol 1993; 157: 326–332.

    Google Scholar 

  63. Haugk KL, Roeder RA, Garber MJ, Schelling GT. Regulation of muscle cell proliferation by extracts from crushed muscle. J Anim Sci 1995; 73: 1972–1981.

    Google Scholar 

  64. Smith J, Fowkes G, Schofield PN. Programmed cell death in dystrophic (mdx) muscle is inhibited by IGF-II. Cell Death Differ 1995; 2: 243–251.

    Google Scholar 

  65. Sandri M, Carraro U, Podhorska-Okolow M, et al. Apoptosis, DNA damage and ubiquitin expression in normal and mdx muscle fibers after exercise. FEBS Letters 1995; 373: 291–295.

    Google Scholar 

  66. Tidball JG, Albrecht DE, Lokensgard BE, Spencer MJ. Apoptosis precedes necrosis of dystrophin-deficient muscle. J Cell Sci 1995; 108: 2197–2204.

    Google Scholar 

  67. Matsuda R, Nishikawa A, Tanaka H. Visualization of dystrophic muscle fibers in mdx mouse by vital staining with Evens Blue: Evidence of apoptosis in dystrophin-deficient muscle. J Biochem (Tokyo) 1995; 118: 959–964.

    Google Scholar 

  68. Tews DS, Goebel HH. DNA-fragmentation and expression of apoptosis-related proteins in muscular dystrophies. Neuropathol Appl Neurobiol 1997; 23: 331–338.

    Google Scholar 

  69. Sandri M, Minetti C, Pedemonte M, Carraro U. Apoptotic myonuclei in human Duchenne muscular dystrophy. Lab Invest 1998; 78: 1005–1016.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Section of Plastic and Reconstructive Surgery, Department of Surgery, University of Michigan Health Systems, Ann Arbor, Michigan, USA

    S. S. Jejurikar & W. M. Kuzon Jr.

  2. Institute of Gerontology, University of Michigan, Ann Arbor, Michigan, USA

    W. M. Kuzon Jr.

Authors
  1. S. S. Jejurikar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. W. M. Kuzon Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to W. M. Kuzon Jr..

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jejurikar, S.S., Kuzon, W.M. Satellite cell depletion in degenerative skeletal muscle. Apoptosis 8, 573–578 (2003). https://doi.org/10.1023/A:1026127307457

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1026127307457

Search

Navigation