AGE

, Volume 36, Issue 2, pp 545–557 | Cite as

Satellite cells in human skeletal muscle; from birth to old age

  • Lex B. Verdijk
  • Tim Snijders
  • Maarten Drost
  • Tammo Delhaas
  • Fawzi Kadi
  • Luc J. C. van Loon
Article

Abstract

Changes in satellite cell content play a key role in regulating skeletal muscle growth and atrophy. Yet, there is little information on changes in satellite cell content from birth to old age in humans. The present study defines muscle fiber type-specific satellite cell content in human skeletal muscle tissue over the entire lifespan. Muscle biopsies were collected in 165 subjects, from different muscles of children undergoing surgery (<18 years; n = 13) and from the vastus lateralis muscle of young adult (18–49 years; n = 50), older (50–69 years; n = 53), and senescent subjects (70–86 years; n = 49). In a subgroup of 51 aged subjects (71 ± 6 years), additional biopsies were collected after 12 weeks of supervised resistance-type exercise training. Immunohistochemistry was applied to assess skeletal muscle fiber type-specific composition, size, and satellite cell content. From birth to adulthood, muscle fiber size increased tremendously with no major changes in muscle fiber satellite cell content, and no differences between type I and II muscle fibers. In contrast to type I muscle fibers, type II muscle fiber size was substantially smaller with increasing age in adults (r = −0.56; P < 0.001). This was accompanied by an age-related reduction in type II muscle fiber satellite cell content (r = −0.57; P < 0.001). Twelve weeks of resistance-type exercise training significantly increased type II muscle fiber size and satellite cell content. We conclude that type II muscle fiber atrophy with aging is accompanied by a specific decline in type II muscle fiber satellite cell content. Resistance-type exercise training represents an effective strategy to increase satellite cell content and reverse type II muscle fiber atrophy.

Keywords

Muscle stem cells Skeletal muscle Development Sarcopenia Exercise 

Supplementary material

11357_2013_9583_MOESM1_ESM.doc (119 kb)
Online Resource 1Plots of regression relationship showing significant predictors for the increase in type II muscle fiber cross-sectional area (CSA) following 3 months of resistance type exercise training in healthy elderly men (n = 51, total R = 0.73). A: change in type II muscle fiber satellite cell (SC) content (standardized B = 0.44; P = 0.001); B: change in type II muscle fiber myonuclear content (standardized B = 0.44; P = 0.004); C: baseline myonuclear content (standardized B = 0.30; P = 0.030). (DOC 119 kb)

References

  1. Andersen JL, Terzis G, Kryger A (1999) Increase in the degree of coexpression of myosin heavy chain isoforms in skeletal muscle fibers of the very old. Muscle Nerve 22(4):449–454PubMedCrossRefGoogle Scholar
  2. Baumgartner RN, Waters DL, Gallagher D, Morley JE, Garry PJ (1999) Predictors of skeletal muscle mass in elderly men and women. Mech Ageing Dev 107(2):123–136PubMedCrossRefGoogle Scholar
  3. Bergstrom J (1975) Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest 35(7):609–616PubMedCrossRefGoogle Scholar
  4. Brooke MH, Engel WK (1969) The histographic analysis of human muscle biopsies with regard to fiber types. 4. Children's biopsies. Neurology 19(6):591–605PubMedCrossRefGoogle Scholar
  5. Brown SC, Stickland NC (1993) Satellite cell content in muscles of large and small mice. J Anat 183(Pt 1):91–96PubMedCentralPubMedGoogle Scholar
  6. Bruusgaard JC, Johansen IB, Egner IM, Rana ZA, Gundersen K (2010) Myonuclei acquired by overload exercise precede hypertrophy and are not lost on detraining. Proc Natl Acad Sci U S A 107(34):15111–15116PubMedCentralPubMedCrossRefGoogle Scholar
  7. Cardasis CA, Cooper GW (1975) An analysis of nuclear numbers in individual muscle fibers during differentiation and growth: a satellite cell-muscle fiber growth unit. J Exp Zool 191(3):347–358PubMedCrossRefGoogle Scholar
  8. Cristea A, Qaisar R, Edlund PK, Lindblad J, Bengtsson E, Larsson L (2010) Effects of aging and gender on the spatial organization of nuclei in single human skeletal muscle cells. Aging Cell 9(5):685–697PubMedCrossRefGoogle Scholar
  9. Delhaas T, Van der Meer SF, Schaart G, Degens H, Drost MR (2013) Steep increase in myonuclear domain size during infancy. Anat Rec (Hoboken) 296(2):192–197Google Scholar
  10. Dhawan J, Rando TA (2005) Stem cells in postnatal myogenesis: molecular mechanisms of satellite cell quiescence, activation and replenishment. Trends Cell Biol 15(12):666–673PubMedCrossRefGoogle Scholar
  11. 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):242–253PubMedCrossRefGoogle Scholar
  12. Evans W (1997) Functional and metabolic consequences of sarcopenia. J Nutr 127(5 Suppl):998S–1003SPubMedGoogle Scholar
  13. Fiatarone MA, Marks EC, Ryan ND, Meredith CN, Lipsitz LA, Evans WJ (1990) High-intensity strength training in nonagenarians. Effects on skeletal muscle. JAMA 263(22):3029–3034PubMedCrossRefGoogle Scholar
  14. 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):1038–1044PubMedGoogle Scholar
  15. Hawke TJ, Garry DJ (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91(2):534–551PubMedGoogle Scholar
  16. Janssen I, Heymsfield SB, Wang ZM, Ross R (2000) Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J Appl Physiol 89(1):81–88PubMedGoogle Scholar
  17. Kadi F, Charifi N, Denis C, Lexell J (2004) Satellite cells and myonuclei in young and elderly women and men. Muscle Nerve 29(1):120–127PubMedCrossRefGoogle Scholar
  18. Kadi F, Charifi N, Denis C, Lexell J, Andersen JL, Schjerling P, Olsen S, Kjaer M (2005) The behaviour of satellite cells in response to exercise: what have we learned from human studies? Pflugers Arch 451(2):319–327PubMedCrossRefGoogle Scholar
  19. Klitgaard H, Zhou M, Schiaffino S, Betto R, Salviati G, Saltin B (1990) Ageing alters the myosin heavy chain composition of single fibres from human skeletal muscle. Acta Physiol Scand 140(1):55–62PubMedCrossRefGoogle Scholar
  20. Larsson L, Sjodin B, Karlsson J (1978) Histochemical and biochemical changes in human skeletal muscle with age in sedentary males, age 22–65 years. Acta Physiol Scand 103(1):31–39PubMedCrossRefGoogle Scholar
  21. 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):275–294PubMedCrossRefGoogle Scholar
  22. Lindle RS, Metter EJ, Lynch NA, Fleg JL, Fozard JL, Tobin J, Roy TA, Hurley BF (1997) Age and gender comparisons of muscle strength in 654 women and men aged 20–93 yr. J Appl Physiol 83(5):1581–1587PubMedGoogle Scholar
  23. Lindstrom M, Thornell LE (2009) New multiple labelling method for improved satellite cell identification in human muscle: application to a cohort of power-lifters and sedentary men. Histochem Cell Biol 132(2):141–157PubMedCrossRefGoogle Scholar
  24. 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):34–42PubMedGoogle Scholar
  25. Mackey AL, 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):455–465PubMedCrossRefGoogle Scholar
  26. Martel GF, Roth SM, Ivey FM, Lemmer JT, Tracy BL, Hurlbut DE, Metter EJ, Hurley BF, Rogers MA (2006) Age and sex affect human muscle fibre adaptations to heavy-resistance strength training. Exp Physiol 91(2):457–464PubMedCrossRefGoogle Scholar
  27. Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495PubMedCentralPubMedCrossRefGoogle Scholar
  28. 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):3657–3666PubMedCentralPubMedCrossRefGoogle Scholar
  29. McKay BR, Toth KG, Tarnopolsky MA, Parise G (2010) Satellite cell number and cell cycle kinetics in response to acute myotrauma in humans: immunohistochemistry versus flow cytometry. J Physiol 588(Pt 17):3307–3320PubMedCentralPubMedCrossRefGoogle Scholar
  30. Monemi M, Kadi F, Liu JX, Thornell LE, Eriksson PO (1999) Adverse changes in fibre type and myosin heavy chain compositions of human jaw muscle vs. limb muscle during ageing. Acta Physiol Scand 167(4):339–345PubMedCrossRefGoogle Scholar
  31. Oertel G (1988) Morphometric analysis of normal skeletal muscles in infancy, childhood and adolescence. An autopsy study. J Neurol Sci 88(1–3):303–313PubMedCrossRefGoogle Scholar
  32. Osterlund C, Lindstrom M, Thornell LE, Eriksson PO (2012) Remarkable heterogeneity in myosin heavy-chain composition of the human young masseter compared with young biceps brachii. Histochem Cell Biol 138(4):669–682PubMedCrossRefGoogle Scholar
  33. 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–E946PubMedCrossRefGoogle Scholar
  34. 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):1736–1742PubMedCrossRefGoogle Scholar
  35. Renault V, Thornell LE, Eriksson PO, Butler-Browne G, Mouly V (2002) Regenerative potential of human skeletal muscle during aging. Aging Cell 1(2):132–139PubMedCrossRefGoogle Scholar
  36. Roth SM, Martel GF, Ivey FM, Lemmer JT, Metter EJ, Hurley BF, Rogers MA (2000) Skeletal muscle satellite cell populations in healthy young and older men and women. Anat Rec 260(4):351–358PubMedCrossRefGoogle Scholar
  37. 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(6):B240–B247PubMedCrossRefGoogle Scholar
  38. Schmalbruch H, Hellhammer U (1976) The number of satellite cells in normal human muscle. Anat Rec 185(3):279–287PubMedCrossRefGoogle Scholar
  39. Shefer G, Van de Mark DP, Richardson JB, Yablonka-Reuveni Z (2006) Satellite-cell pool size does matter: defining the myogenic potency of aging skeletal muscle. Dev Biol 294(1):50–66PubMedCentralPubMedCrossRefGoogle Scholar
  40. 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(1 Pt 1):E135–E143PubMedGoogle Scholar
  41. Snijders T, Verdijk LB, van Loon LJ (2009) The impact of sarcopenia and exercise training on skeletal muscle satellite cells. Ageing Res Rev 8(4):328–338PubMedCrossRefGoogle Scholar
  42. Thornell LE, Lindstrom M, Renault V, Mouly V, Butler-Browne GS (2003) Satellite cells and training in the elderly. Scand J Med Sci Sports 13(1):48–55PubMedCrossRefGoogle Scholar
  43. Vassilopoulos D, Lumb EM, Emery AE (1977) Karyometric changes in human muscle with age. Eur Neurol 16(1–6):31–34PubMedCrossRefGoogle Scholar
  44. 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–E157PubMedCrossRefGoogle Scholar
  45. 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):332–339PubMedCrossRefGoogle Scholar
  46. 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):608–616PubMedCrossRefGoogle Scholar
  47. 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):1147–1154PubMedCrossRefGoogle Scholar
  48. Visser M, Kritchevsky SB, Goodpaster BH, Newman AB, Nevitt M, Stamm E, Harris TB (2002) Leg muscle mass and composition in relation to lower extremity performance in men and women aged 70 to 79: the health, aging and body composition study. J Am Geriatr Soc 50(5):897–904PubMedCrossRefGoogle Scholar
  49. Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR (2004) Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J Cell Biol 166(3):347–357PubMedCentralPubMedCrossRefGoogle Scholar
  50. Zammit PS, Partridge TA, Yablonka-Reuveni Z (2006) The skeletal muscle satellite cell: the stem cell that came in from the cold. J Histochem Cytochem 54(11):1177–1191PubMedCrossRefGoogle Scholar

Copyright information

© American Aging Association 2013

Authors and Affiliations

  • Lex B. Verdijk
    • 1
  • Tim Snijders
    • 1
  • Maarten Drost
    • 1
  • Tammo Delhaas
    • 2
    • 3
  • Fawzi Kadi
    • 4
  • Luc J. C. van Loon
    • 1
  1. 1.Department of Human Movement Sciences, NUTRIM School for Nutrition, Toxicology and MetabolismMaastricht University Medical Centre+MaastrichtThe Netherlands
  2. 2.Department of Biomedical Engineering, Cardiovascular Research Institute MaastrichtMaastricht University Medical Centre+MaastrichtThe Netherlands
  3. 3.Department of Pediatric CardiologyUniversity Hospital GasthuisbergLeuvenBelgium
  4. 4.Division of Sport Sciences, School of Health and Medical SciencesÖrebro UniversityÖrebroSweden

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