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PMID: 16554047 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Satellite-cell pool size does matter: defining the myogenic potency of aging skeletal muscle.

Developmental biology ·Vol. 294 ·No. 1 ·2006-06-01 ·Pages 50-66

Shefer G, Van de Mark DP, Richardson JB, Yablonka-Reuveni Z

Abstract

The deteriorating in vivo environment is thought to play a major role in reduced stem cell function with age. The capacity of stem cells to support tissue maintenance depends not only on their response to cues from the surrounding niche, but also on their abundance. Here, we investigate satellite cell (myogenic stem cell) pool size and its potential to participate in muscle maintenance through old age. The numbers and performance of mouse satellite cells have been analyzed using molecular markers that exclusively characterize quiescent satellite cells and their progeny as they transit through proliferation, differentiation and generation of reserve cells. The study establishes that abundance of resident satellite cells declines with age in myofibers from both fast- and slow-twitch muscles. Nevertheless, the inherent myogenic potential of satellite cells does not diminish with age. Furthermore, the aging satellite cell niche retains the capacity to support effective myogenesis upon enrichment of the mitogenic milieu with FGF. Altogether, satellite cell abundance, but not myogenic potential, deteriorates with age. This study suggests that the population of satellite cells that participate in myofiber maintenance during routine muscle utilization is not fully replenished throughout life.

MeSH Terms
Aging/physiology Animals Cell Count Cell Culture Techniques Male Mice Mice, Inbred C57BL Muscle Development Muscle Fibers, Fast-Twitch/cytology Muscle Fibers, Slow-Twitch/cytology Muscle, Skeletal/cytology Satellite Cells, Skeletal Muscle/cytology,physiology
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Shefer Gabi
Department of Biological Structure, School of Medicine, University of Washington, Magnuson Health Sciences Center, Room G514, Box 357420, Seattle, WA 98195, USA.
Van de Mark Daniel P
Richardson Joshua B
Yablonka-Reuveni Zipora
References (67)
67 references, click to expand
  1. Satellite cells from dystrophic (mdx) mice display accelerated differentiation in primary cultures and in isolated myofibers.
    Dev Dyn. 2006 Jan;235(1):203-12 PMID: 16258933
  2. Primary rat muscle progenitor cells have decreased proliferation and myotube formation during passages.
    Cell Prolif. 2004 Aug;37(4):267-77 PMID: 15245563
  3. Alterations in the TGFbeta signaling pathway in myogenic progenitors with age.
    Aging Cell. 2004 Dec;3(6):353-61 PMID: 15569352
  4. Human skeletal muscle fiber type classifications.
    Phys Ther. 2001 Nov;81(11):1810-6 PMID: 11694174
  5. Myogenesis in the Chicken: the Onset of Differentiation of Adult Myoblasts is Influenced by Tissue Factors.
    Basic Appl Myol. 1995;5(1):33-41 PMID: 26412965
  6. Satellite cells and myonuclei in young and elderly women and men.
    Muscle Nerve. 2004 Jan;29(1):120-7 PMID: 14694507
  7. Life-span and the inheritance of longevity of inbred mice.
    J Gerontol. 1975 May;30(3):257-63 PMID: 1120887
  8. Age-associated decrease in muscle precursor cell differentiation.
    Am J Physiol Cell Physiol. 2006 Feb;290(2):C609-15 PMID: 16192302
  9. The mitotic clock in skeletal muscle regeneration, disease and cell mediated gene therapy.
    Acta Physiol Scand. 2005 May;184(1):3-15 PMID: 15847639
  10. Myosin heavy chain isoforms in postnatal muscle development of mice.
    Biol Cell. 2003 Sep;95(6):399-406 PMID: 14519557
  11. Human aging, muscle mass, and fiber type composition.
    J Gerontol A Biol Sci Med Sci. 1995 Nov;50 Spec No:11-6 PMID: 7493202
  12. Gerontological data of C57BL/6J mice. I. Sex differences in survival curves.
    J Gerontol. 1975 Mar;30(2):157-62 PMID: 1123533
  13. Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells.
    J Cell Biol. 2000 Dec 11;151(6):1221-34 PMID: 11121437
  14. IGF-I restores satellite cell proliferative potential in immobilized old skeletal muscle.
    J Appl Physiol (1985). 2000 Oct;89(4):1365-79 PMID: 11007571
  15. Transgenic mouse models of muscle aging.
    Exp Gerontol. 1999 Apr;34(2):147-56 PMID: 10363783
  16. Myogenic satellite cells: physiology to molecular biology.
    J Appl Physiol (1985). 2001 Aug;91(2):534-51 PMID: 11457764
  17. Sarcopenia of aging and its metabolic impact.
    Curr Top Dev Biol. 2005;68:123-48 PMID: 16124998
  18. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis.
    Dev Cell. 2002 Sep;3(3):397-409 PMID: 12361602
  19. Satellite cell proliferative compartments in growing skeletal muscles.
    Dev Biol. 1996 Apr 10;175(1):84-94 PMID: 8608871
  20. Cold-induced thermoregulation and biological aging.
    Physiol Rev. 1998 Apr;78(2):339-58 PMID: 9562032
  21. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche.
    Cell. 2005 Jul 29;122(2):289-301 PMID: 16051152
  22. The magnitude of the initial injury induced by stretches of maximally activated muscle fibres of mice and rats increases in old age.
    J Physiol. 1996 Dec 1;497 ( Pt 2):573-80 PMID: 8961197
  23. Myogenic potential of satellite cells in skeletal muscle of old rats. A brief note.
    Mech Ageing Dev. 1980 Jun;13(2):105-9 PMID: 7431999
  24. Pax7 is required for the specification of myogenic satellite cells.
    Cell. 2000 Sep 15;102(6):777-86 PMID: 11030621
  25. Fibroblast growth factor promotes recruitment of skeletal muscle satellite cells in young and old rats.
    J Histochem Cytochem. 1999 Jan;47(1):23-42 PMID: 9857210
  26. Viral mediated expression of insulin-like growth factor I blocks the aging-related loss of skeletal muscle function.
    Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15603-7 PMID: 9861016
  27. Kinetics of myoblast proliferation show that resident satellite cells are competent to fully regenerate skeletal muscle fibers.
    Exp Cell Res. 2002 Nov 15;281(1):39-49 PMID: 12441128
  28. Sarcopenia is not due to lack of regenerative drive in senescent skeletal muscle.
    Aging Cell. 2005 Apr;4(2):65-77 PMID: 15771610
  29. Changes in fibre type, number and diameter in developing and ageing skeletal muscle.
    J Anat. 1987 Aug;153:31-45 PMID: 3429325
  30. Activation of skeletal muscle satellite cells and the role of fibroblast growth factor receptors.
    Exp Cell Res. 1995 Aug;219(2):449-53 PMID: 7641796
  31. Age-related differences in absolute numbers of skeletal muscle satellite cells.
    Muscle Nerve. 1983 Oct;6(8):574-80 PMID: 6646160
  32. Stem cells in postnatal myogenesis: molecular mechanisms of satellite cell quiescence, activation and replenishment.
    Trends Cell Biol. 2005 Dec;15(12):666-73 PMID: 16243526
  33. Muscle satellite cells adopt divergent fates: a mechanism for self-renewal?
    J Cell Biol. 2004 Aug 2;166(3):347-57 PMID: 15277541
  34. Mutation of the IIB myosin heavy chain gene results in muscle fiber loss and compensatory hypertrophy.
    Am J Physiol Cell Physiol. 2001 Mar;280(3):C637-45 PMID: 11171584
  35. Influence of PDGF-BB on proliferation and transition through the MyoD-myogenin-MEF2A expression program during myogenesis in mouse C2 myoblasts.
    Growth Factors. 1997;15(1):1-27 PMID: 9401815
  36. Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers.
    Dev Biol. 1994 Aug;164(2):588-603 PMID: 7913900
  37. Evidence that satellite cell decrement contributes to preferential decline in nuclear number from large fibres during murine age-related muscle atrophy.
    J Cell Sci. 2005 Oct 15;118(Pt 20):4813-21 PMID: 16219688
  38. Notch-mediated restoration of regenerative potential to aged muscle.
    Science. 2003 Nov 28;302(5650):1575-7 PMID: 14645852
  39. Reasons for the degeneration of ageing skeletal muscle: a central role for IGF-1 signalling.
    Biogerontology. 2002;3(1-2):19-24 PMID: 12014835
  40. Skeletal muscle weakness in old age: underlying mechanisms.
    Med Sci Sports Exerc. 1994 Apr;26(4):432-9 PMID: 8201898
  41. Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro.
    J Cell Physiol. 1995 Nov;165(2):307-12 PMID: 7593208
  42. Molecular and cell biology of skeletal muscle regeneration.
    Mol Cell Biol Hum Dis Ser. 1993;3:210-56 PMID: 8111541
  43. Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle.
    Nat Genet. 2001 Feb;27(2):195-200 PMID: 11175789
  44. Skeletal muscle regeneration in very old rats.
    J Gerontol A Biol Sci Med Sci. 2001 May;56(5):B224-33 PMID: 11320103
  45. Age-associated changes in the response of skeletal muscle cells to exercise and regeneration.
    Ann N Y Acad Sci. 1998 Nov 20;854:78-91 PMID: 9928422
  46. Satellite cells as the source of nuclei in muscles of growing rats.
    Anat Rec. 1971 Aug;170(4):421-35 PMID: 5118594
  47. Skeletal muscle satellite cells: changes in proliferation potential as a function of age.
    Mech Ageing Dev. 1982 Dec;20(4):377-83 PMID: 7166986
  48. Skeletal muscle satellite cell populations in healthy young and older men and women.
    Anat Rec. 2000 Dec 1;260(4):351-8 PMID: 11074399
  49. Satellite cell regulation of muscle mass is altered at old age.
    J Appl Physiol (1985). 2004 Sep;97(3):1082-90 PMID: 15121742
  50. Rejuvenation of aged progenitor cells by exposure to a young systemic environment.
    Nature. 2005 Feb 17;433(7027):760-4 PMID: 15716955
  51. The transition from proliferation to differentiation is delayed in satellite cells from mice lacking MyoD.
    Dev Biol. 1999 Jun 15;210(2):440-55 PMID: 10357902
  52. Pax3/Pax7 mark a novel population of primitive myogenic cells during development.
    Genes Dev. 2005 Jun 15;19(12):1426-31 PMID: 15964993
  53. Muscle transplantation between young and old rats: age of host determines recovery.
    Am J Physiol. 1989 Jun;256(6 Pt 1):C1262-6 PMID: 2735398
  54. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells.
    Nature. 2005 Jun 16;435(7044):948-53 PMID: 15843801
  55. Regenerative potential of human skeletal muscle during aging.
    Aging Cell. 2002 Dec;1(2):132-9 PMID: 12882343
  56. Muscle regeneration in the prolonged absence of myostatin.
    Proc Natl Acad Sci U S A. 2005 Feb 15;102(7):2519-24 PMID: 15699335
  57. Longevity and gross pathology at death in 22 inbred mouse strains.
    J Gerontol. 1966 Jul;21(3):404-9 PMID: 5944803
  58. Role of genotype and dopamine receptors in behaviour of inbred mice in a forced swimming test.
    Psychopharmacology (Berl). 1991;105(4):525-9 PMID: 1685251
  59. Isolation and culture of skeletal muscle myofibers as a means to analyze satellite cells.
    Methods Mol Biol. 2005;290:281-304 PMID: 15361669
  60. Aging normal and dystrophic mouse muscle: analysis of myogenicity in cultures of living single fibers.
    Muscle Nerve. 1998 Feb;21(2):173-83 PMID: 9466592
  61. The biology of aging.
    Mt Sinai J Med. 2003 Jan;70(1):3-22 PMID: 12516005
  62. What insights into age-related changes in skeletal muscle are provided by animal models?
    J Gerontol A Biol Sci Med Sci. 1995 Nov;50 Spec No:137-41 PMID: 7493207
  63. Gene expression patterns of the fibroblast growth factors and their receptors during myogenesis of rat satellite cells.
    J Histochem Cytochem. 2000 Aug;48(8):1079-96 PMID: 10898801
  64. Activation of an adipogenic program in adult myoblasts with age.
    Mech Ageing Dev. 2002 Mar 31;123(6):649-61 PMID: 11850028
  65. Skeletal muscle satellite cells can spontaneously enter an alternative mesenchymal pathway.
    J Cell Sci. 2004 Oct 15;117(Pt 22):5393-404 PMID: 15466890
  66. Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal.
    Dev Dyn. 2004 Nov;231(3):489-502 PMID: 15390217
  67. Proliferative Dynamics and the Role of FGF2 During Myogenesis of Rat Satellite Cells on Isolated Fibers.
    Basic Appl Myol. 1997;7(3-amp4):189-202 PMID: 26052220
Article Info
Journal
Developmental biology
Abbr.
Dev Biol
ISSN
0012-1606
DOI
10.1016/j.ydbio.2006.02.022
Published
2006-06-01
Epub
2006-00-22
Pages
50-66
Language
English
Region
United States
NLM ID
0372762
PMCID
PMC2710453
Subset
IM
Grants
NIA NIH HHS · AG13798 · United States
NIA NIH HHS · R01 AG021566-02 · United States
NIA NIH HHS · R01 AG013798-10A2 · United States
NIA NIH HHS · R01 AG013798 · United States
NIA NIH HHS · R01 AG021566-04 · United States
NIA NIH HHS · R01 AG013798-12 · United States
NIA NIH HHS · R01 AG013798-11 · United States
NIA NIH HHS · AG21566 · United States
NIA NIH HHS · R01 AG021566 · United States
NIA NIH HHS · R01 AG021566-01 · United States
NIA NIH HHS · R01 AG021566-03 · United States
External Links
PubMed source DOI: 10.1016/j.ydbio.2006.02.022 PMC Full Text View journal details
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