Differential satellite cell density of type I and II fibres with lifelong endurance running in old men

Acta Physiologica

Volumn 210, Issue 3, 2014, Pages 612-627

  Mackey, A L ^a,b   Karlsen, A ^a,b   Couppe C ^a,b   Mikkelsen, U R ^a,b   Nielsen, R H ^a,b   Magnusson, S P ^a,b   Kjaer, M ^a,b  

^a BISPEBJERG HOSPITAL   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Ageing muscle; Central nuclei; Master athlete; Pax7; Satellite cell density

Indexed keywords

LAMININ; MYOSIN I; TRANSCRIPTION FACTOR PAX7;

ADULT; AGED; ARTICLE; CELL DENSITY; CELL NUCLEUS; CONTROLLED STUDY; ENDURANCE TRAINING; FROZEN SECTION; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; MUSCLE BIOPSY; MYONUCLEUS; NORMAL HUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; RUNNING; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; YOUNG ADULT;

AGEING MUSCLE; CENTRAL NUCLEI; MASTER ATHLETE; PAX7; SATELLITE CELL DENSITY;

AGED; ATHLETES; CELL COUNT; CHILD; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; PHYSICAL ENDURANCE; RUNNING; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 84893442195     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/apha.12195     Document Type: Article

References (58)

1. Aagaard, P., Magnusson, P.S., Larsson, B., Kjaer, M. & Krustrup, P. 2007. Mechanical muscle function, morphology, and fiber type in lifelong trained elderly. Med Sci Sports Exerc 39, 1989-1996.
2. Andersen, J.L. 2003. Muscle fibre type adaptation in the elderly human muscle. Scand J Med Sci Sports 13, 40-47.
3. Bergstrom, J. 1975. Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest 35, 609-616.
4. Bruusgaard, J.C., Liestol, K., Ekmark, M., Kollstad, K. & Gundersen, K. 2003. Number and spatial distribution of nuclei in the muscle fibres of normal mice studied in vivo. J Physiol 551, 467-478.
5. Bruusgaard, J.C., Liestol, K. & Gundersen, K. 2006. Distribution of myonuclei and microtubules in live muscle fibers of young, middle-aged, and old mice. J Appl Physiol 100, 2024-2030.
6. Butler-Browne, G.S. & Whalen, R.G. 1984. Myosin isozyme transitions occurring during the postnatal development of the rat soleus muscle. Dev Biol 102, 324-334.
7. CDC. 2011. Behavioral Risk Factor Surveillance System Survey Data. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, Atlanta, GA. Accessed on 8 December 2012.
8. Chakravarty, E.F., Hubert, H.B., Lingala, V.B. & Fries, J.F. 2008. Reduced disability and mortality among aging runners: a 21-year longitudinal study. Arch Intern Med 168, 1638-1646.
9. 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.
10. Cristea, A., Qaisar, R., Edlund, P.K., 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, 685-697.
11. Decary, S., Hamida, C.B., Mouly, V., Barbet, J.P., Hentati, F. & Butler-Browne, G.S. 2000. Shorter telomeres in dystrophic muscle consistent with extensive regeneration in young children. Neuromuscul Disord 10, 113-120.
12. Dreyer, H.C., Blanco, C.E., Sattler, F.R., Schroeder, E.T. & Wiswell, R.A. 2006. Satellite cell numbers in young and older men 24 hours after eccentric exercise. Muscle Nerve 33, 242-253.
13. Grounds, M.D. & McGeachie, J.K. 1987. A model of myogenesis in vivo, derived from detailed autoradiographic studies of regenerating skeletal muscle, challenges the concept of quantal mitosis. Cell Tissue Res 250, 563-569.
14. Haskell, W.L., Lee, I.M., Pate, R.R., Powell, K.E., Blair, S.N., Franklin, B.A., Macera, C.A., Heath, G.W., Thompson, P.D. & Bauman, A. 2007. Physical activity and public health: updated recommendation for adults from the American College of Sports Medicine and the American Heart Association. Med Sci Sports Exerc 39, 1423-1434.
15. Kadi, F., Eriksson, A., Holmner, S., Butler-Browne, G.S. & Thornell, L.E. 1999. Cellular adaptation of the trapezius muscle in strength-trained athletes. Histochem Cell Biol 111, 189-195.
16. 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.
17. Kadi, F., Charifi, N. & Henriksson, J. 2006. The number of satellite cells in slow and fast fibres from human vastus lateralis muscle. Histochem Cell Biol 126, 83-87.
18. Klitgaard, H., Mantoni, M., Schiaffino, S., Ausoni, S., Gorza, L., Laurent-Winter, C., Schnohr, P. & Saltin, B. 1990. Function, morphology and protein expression of ageing skeletal muscle: a cross-sectional study of elderly men with different training backgrounds. Acta Physiol Scand 140, 41-54.
19. Kraemer, W.J., Patton, J.F., Gordon, S.E., Harman, E.A., Deschenes, M.R., Reynolds, K., Newton, R.U., Triplett, N.T. & Dziados, J.E. 1995. Compatibility of high-intensity strength and endurance training on hormonal and skeletal muscle adaptations. J Appl Physiol 78, 976-989.
20. Kurosaka, M., Naito, H., Ogura, Y., Machida, S. & Katamoto, S. 2012. Satellite cell pool enhancement in rat plantaris muscle by endurance training depends on intensity rather than duration. Acta Physiol (Oxf) 205, 159-166.
21. 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, 31-39.
22. Lexell, J., Taylor, C.C. & 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, 275-294.
23. Mackey, A.L., Esmarck, B., Kadi, F., Koskinen, S.O.A., Kongsgaard, M., Sylvestersen, A., Hansen, J.J., Larsen, G. & Kjaer, M. 2007. Enhanced satellite cell proliferation with resistance training in elderly men and women. Scand J Med Sci Sports 17, 34-42.
24. Mackey, A.L., 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, 455-465.
25. Mackey, A.L., Andersen, L.L., Frandsen, U., Suetta, C. & Sjøgaard, G. 2010. Distribution of myogenic progenitor cells and myonuclei is altered in women with vs. those without chronically painful trapezius muscle. J Appl Physiol 109, 1920-1929.
26. Mackey, A.L., Andersen, L.L., Frandsen, U. & Sjøgaard, G. 2011. Strength training increases the size of the satellite cell pool in type I and II fibres of chronically painful trapezius muscle in females. J Physiol (Lond) 589, 5503-5515.
27. Manta, P., Vassilopoulos, D. & Spengos, M. 1987. Nucleo-cytoplasmic ratio in ageing skeletal muscle. Eur Arch Psychiatry Neurol Sci 236, 235-236.
28. Marklund, P., Mattsson, C.M., Wahlin-Larsson, B., Ponsot, E., Lindvall, B., Lindvall, L., Ekblom, B. & Kadi, F. 2013. Extensive inflammatory cell infiltration in human skeletal muscle in response to an ultraendurance exercise bout in experienced athletes. J Appl Physiol 114, 66-72.
29. McGeachie, J.K., Grounds, M.D., Partridge, T.A. & Morgan, J.E. 1993. Age-related changes in replication of myogenic cells in mdx mice: quantitative autoradiographic studies. J Neurol Sci 119, 169-179.
30. Mikkelsen, U.R., Couppé, C., Karlsen, A., Grosset, J.F., Schjerling, P., Mackey, A.L., Klausen, H.H., Magnusson, S.P. & Kjær, M. Life-long endurance exercise in humans: circulating levels of inflammatory markers and leg muscle size. Mech Ageing Dev, doi:10.1016/j.mad.2013.11.004.
31. Nilwik, R., Snijders, T., Leenders, M., Groen, B.B., van Kranenburg, J., Verdijk, L.B. & van Loon, L.J. 2013. The decline in skeletal muscle mass with aging is mainly attributed to a reduction in type II muscle fiber size. Exp Gerontol 48, 492-498.
32. Ohira, Y., Yoshinaga, T., Ohara, M., Nonaka, I., Yoshioka, T., Yamashita-Goto, K., Shenkman, B.S., Kozlovskaya, I.B., Roy, R.R. & Edgerton, V.R. 1999. Myonuclear domain and myosin phenotype in human soleus after bed rest with or without loading. J Appl Physiol 87, 1776-1785.
33. Pavlath, G.K., Rich, K., Webster, S.G. & Blau, H.M. 1989. Localization of muscle gene products in nuclear domains. Nature 337, 570-573.
34. Petrella, J.K., Kim, J.S., Mayhew, D.L., Cross, J.M. & Bamman, M.M. 2008. Potent myofiber hypertrophy during resistance training in humans is associated with satellite cell-mediated myonuclear addition: a cluster analysis. J Appl Physiol 104, 1736-1742.
35. Ponsot, E., Echaniz-Laguna, A., Delis, A.M. & Kadi, F. 2012. Telomere length and regulatory proteins in human skeletal muscle with and without ongoing regenerative cycles. Exp Physiol 97, 774-784.
36. Porter, M.M., Vandervoort, A.A. & Lexell, J. 1995. Aging of human muscle: structure, function and adaptability. Scand J Med Sci Sports 5, 129-142.
37. Ralston, E., Lu, Z., Biscocho, N., Soumaka, E., Mavroidis, M., Prats, C., Lomo, T., Capetanaki, Y. & Ploug, T. 2006. Blood vessels and desmin control the positioning of nuclei in skeletal muscle fibers. J Cell Physiol 209, 874-882.
38. Renault, V., Piron-Hamelin, G., Forestier, C., DiDonna, S., Decary, S., Hentati, F., Saillant, G., Butler-Browne, G.S. & Mouly, V. 2000. Skeletal muscle regeneration and the mitotic clock. Exp Gerontol 35, 711-719.
39. Renault, V., Thornell, L.E., Eriksson, P.O., Butler-Browne, G. & Mouly, V. 2002. Regenerative potential of human skeletal muscle during aging. Aging Cell 1, 132-139.
40. Running USA. 2012. Running USA's annual marathon report. http://www.runningusa.org/ [accessed on 8 December 2012].
41. Saltin, B. & Grimby, G. 1968. Physiological analysis of middle-aged and old former athletes. Comparison with still active athletes of the same ages. Circulation 38, 1104-1115.
42. Schiaffino, S., Bormioli, S.P. & Aloisi, M. 1976. The fate of newly formed satellite cells during compensatory muscle hypertrophy. Virchows Arch B Cell Pathol 21, 113-118.
43. Schmalbruch, H. & Lewis, D.M. 2000. Dynamics of nuclei of muscle fibers and connective tissue cells in normal and denervated rat muscles. Muscle Nerve 23, 617-626.
44. Shefer, G., Van de Mark, D.P., Richardson, J.B. & Yablonka-Reuveni, Z. 2006. Satellite-cell pool size does matter: defining the myogenic potency of aging skeletal muscle. Dev Biol 294, 50-66.
45. Shefer, G., Rauner, G., Yablonka-Reuveni, Z. & Benayahu, D. 2010. Reduced satellite cell numbers and myogenic capacity in aging can be alleviated by endurance exercise. PLoS ONE 5, e13307.
46. Shefer, G., Rauner, G., Stuelsatz, P., Benayahu, D. & Yablonka-Reuveni, Z. 2013. Moderate-intensity treadmill running promotes expansion of the satellite cell pool in young and old mice. FEBS J 280, 4063-4073.
47. Snijders, T., Verdijk, L.B., Hansen, D., Dendale, P. & van Loon, L.J. 2011. Continuous endurance-type exercise training does not modulate satellite cell content in obese type 2 diabetes patients. Muscle Nerve 43, 393-401.
48. Thornell, L.E., Lindström, M., Renault, V., Klein, A., Mouly, V., Ansved, T., Butler-Browne, G. & Furling, D. 2009. Satellite cell dysfunction contributes to the progressive muscle atrophy in myotonic dystrophy type 1. Neuropathol Appl Neurobiol 35, 603-613.
49. Trappe, S., Harber, M., Creer, A., Gallagher, P., Slivka, D., Minchev, K. & Whitsett, D. 2006. Single muscle fiber adaptations with marathon training. J Appl Physiol 101, 721-727.
50. Verdijk, L.B., Koopman, R., Schaart, G., Meijer, K., Savelberg, H.H. & van Loon, L.J. 2007. Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly. Am J Physiol Endocrinol Metab 292, E151-E157.
51. Verdijk, L.B., Gleeson, B.G., Jonkers, R.A., Meijer, K., Savelberg, H.H., Dendale, P. & van Loon, L.J. 2009. 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, 332-339.
52. Verdijk, L.B., Snijders, T., Beelen, M., Savelberg, H.H., Meijer, K., Kuipers, H. & Van Loon, L.J. 2010. Characteristics of muscle fiber type are predictive of skeletal muscle mass and strength in elderly men. J Am Geriatr Soc 58, 2069-2075.
53. Verdijk, L.B., Dirks, M.L., Snijders, T., Prompers, J.J., Beelen, M., Jonkers, R.A., Thijssen, D.H., Hopman, M.T. & Van Loon, L.J. 2012. Reduced satellite cell numbers with spinal cord injury and aging in humans. Med Sci Sports Exerc 44, 2322-2330.
54. Verney, J., Kadi, F., Charifi, N., Feasson, L., Saafi, M.A., 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, 1147-1154.
55. Wakayama, Y., Schotland, D.L., Bonilla, E. & Orecchio, E. 1979. Quantitative ultrastructural study of muscle satellite cells in Duchenne dystrophy. Neurology 29, 401-407.
56. Wang, B.W., Ramey, D.R., Schettler, J.D., Hubert, H.B. & Fries, J.F. 2002. Postponed development of disability in elderly runners: a 13-year longitudinal study. Arch Intern Med 162, 2285-2294.
57. Widrick, J.J., Trappe, S.W., Costill, D.L. & Fitts, R.H. 1996. Force-velocity and force-power properties of single muscle fibers from elite master runners and sedentary men. Am J Physiol 271, C676-C683.
58. Zammit, P.S., Heslop, L., Hudon, V., Rosenblatt, J.D., Tajbakhsh, S., Buckingham, M.E., Beauchamp, J.R. & Partridge, T.A. 2002. Kinetics of myoblast proliferation show that resident satellite cells are competent to fully regenerate skeletal muscle fibers. Exp Cell Res 281, 39-49.