A single bout of exercise activates skeletal muscle satellite cells during subsequent overnight recovery

Experimental Physiology

Volumn 97, Issue 6, 2012, Pages 762-773

  Snijders, Tim ^a   Verdijk, Lex B ^a   Beelen, Milou ^a   McKay, Bryon R ^b   Parise, Gianni ^b   Kadi, Fawzi ^c   Van Loon, Luc J C ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b MCMASTER UNIVERSITY   (Canada)

^c ÖREBRO UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

DELTA LIKE HOMOLOGUE 1; KI 67 ANTIGEN; MESSENGER RNA; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CELL ACTIVATION; CONVALESCENCE; ENDURANCE TRAINING; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MUSCLE BIOPSY; MUSCLE CELL; NORMAL HUMAN; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RESISTANCE TRAINING; SATELLITE CELL; SKELETAL MUSCLE; STAINING;

EID: 84862607312     PISSN: 09580670     EISSN: 1469445X     Source Type: Journal    
DOI: 10.1113/expphysiol.2011.063313     Document Type: Article

References (53)

1. Adams GR, Caiozzo VJ, Haddad F & Baldwin KM (2002). Cellular and molecular responses to increased skeletal muscle loading after irradiation. Am J Physiol Cell Physiol 283, C1182-C1195.
2. Allen DL, Roy RR & Edgerton VR (1999). Myonuclear domains in muscle adaptation and disease. Muscle Nerve 22, 1350-1360.
3. + cells emerging during skeletal muscle remodeling in response to myositis, myopathies, and acute injury. Stem Cells 27, 898-908.
4. Beelen M, Koopman R, Gijsen AP, Vandereyt H, Kies AK, Kuipers H, Saris WH & van Loon LJ (2008). Protein coingestion stimulates muscle protein synthesis during resistance-type exercise. Am J Physiol Endocrinol Metab 295, E70-E77.
5. Bergstrom J (1975). Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest 35, 609-616.
6. 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.
7. Cheek DB (1985). The control of cell mass and replication. The DNA unit-a personal 20-year study. Early Hum Dev 12, 211-239.
8. Christov C, Chretien F, Abou-Khalil R, Bassez G, Vallet G, Authier FJ, Bassaglia Y, Shinin V, Tajbakhsh S, Chazaud B & Gherardi RK (2007). Muscle satellite cells and endothelial cells: close neighbors and privileged partners. Mol Biol Cell 18, 1397-1409.
9. Conboy IM, Conboy MJ, Smythe GM & Rando TA (2003). Notch-mediated restoration of regenerative potential to aged muscle. Science 302, 1575-1577.
10. Crameri RM, Aagaard P, Qvortrup K, Langberg H, Olesen J & Kjaer M (2007). Myofibre damage in human skeletal muscle: effects of electrical stimulation versus voluntary contraction. J Physiol 583, 365-380.
11. Crameri RM, Langberg H, Magnusson P, Jensen CH, Schrøder 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 558, 333-340.
12. Dhawan J & Rando TA (2005). Stem cells in postnatal myogenesis: molecular mechanisms of satellite cell quiescence, activation and replenishment. Trends Cell Biol 15, 666-673.
13. 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, 242-253.
14. Edgerton VR & Roy RR (1991). Regulation of skeletal muscle fiber size, shape and function. J Biomech 24(Suppl 1), 123-133.
15. 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, 49-59.
16. Gerdes J, Lemke H, Baisch H, Wacker HH, Schwab U & Stein H (1984). Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J Immunol 133, 1710-1715.
17. Harris JA & Benedict FG (1918). A biometric study of human basal metabolism. Proc Natl Acad Sci U S A 4, 370-373.
18. Hawke TJ & Garry DJ (2001). Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91, 534-551.
19. 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, B347-354.
20. Jones PR & Pearson J (1969). Anthropometric determination of leg fat and muscle plus bone volumes in young male and female adults. J Physiol 204, 63P-66P.
21. 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, 319-327.
22. 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.
23. 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 558, 1005-1012.
24. Kadi F & Thornell LE (2000). Concomitant increases in myonuclear and satellite cell content in female trapezius muscle following strength training. Histochem Cell Biol 113, 99-103.
25. Kuipers H, Verstappen FT, Keizer HA, Geurten P & van Kranenburg G (1985). Variability of aerobic performance in the laboratory and its physiologic correlates. Int J Sports Med 6, 197-201.
26. Lindström M, Pedrosa-Domellöf F & Thornell LE (2010). Satellite cell heterogeneity with respect to expression of MyoD, myogenin, Dlk1 and c-Met in human skeletal muscle: application to a cohort of power lifters and sedentary men. Histochem Cell Biol 134, 371-385.
27. Livak KJ & Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the method. Methods 25, 402-408.
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, 3657-3666.
29. McKay BR, De Lisio M, Johnston AP, O'Reilly CE, Phillips SM, Tarnopolsky MA & Parise G (2009). Association of interleukin-6 signalling with the muscle stem cell response following muscle-lengthening contractions in humans. PLoS One 4, e6027.
30. 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, 455-465.
31. Mackey AL, Kjaer M, Dandanell S, Mikkelsen KH, Holm L, Døssing S, Kadi F, Koskinen SO, Jensen CH, Schrøder HD & Langberg H (2007). The influence of anti-inflammatory medication on exercise-induced myogenic precursor cell responses in humans. J Appl Physiol 103, 425-431.
32. McLoon LK & Wirtschafter J (2003). Activated satellite cells in extraocular muscles of normal adult monkeys and humans. Invest Ophthalmol Vis Sci 44, 1927-1932.
33. Mayhew JL, Prinster JL, Ware JS, Zimmer DL, Arabas JR & Bemben MG (1995). Muscular endurance repetitions to predict bench press strength in men of different training levels. J Sports Med Phys Fitness 35, 108-113.
34. Mikkelsen UR, Langberg H, Helmark IC, Skovgaard D, Andersen LL, Kjaer M & Mackey AL (2009). Local NSAID infusion inhibits satellite cell proliferation in human skeletal muscle after eccentric exercise. J Appl Physiol 107, 1600-1611.
35. Olsen S, Aagaard P, Kadi F, Tufekovic G, Verney J, Olesen JL, Suetta C & Kjaer M (2006). Creatine supplementation augments the increase in satellite cell and myonuclei number in human skeletal muscle induced by strength training. J Physiol 573, 525-534.
36. O'Reilly C, McKay B, Phillips S, Tarnopolsky M & Parise G (2008). Hepatocyte growth factor (HGF) and the satellite cell response following muscle lengthening contractions in humans. Muscle Nerve 38, 1434-1442.
37. 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, E937-E946.
38. 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, 1736-1742.
39. Plasqui G & Westerterp KR (2004). Seasonal variation in total energy expenditure and physical activity in Dutch young adults. Obes Res 12, 688-694.
40. Psilander N, Damsgaard R & Pilegaard H (2003). Resistance exercise alters MRF and IGF-I mRNA content in human skeletal muscle. J Appl Physiol 95, 1038-1044.
41. Rosenblatt JD, Yong D & Parry DJ (1994). Satellite cell activity is required for hypertrophy of overloaded adult rat muscle. Muscle Nerve 17, 608-613.
42. 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, B240-B247.
43. Scholzen T & Gerdes J (2000). The Ki-67 protein: from the known and the unknown. J Cell Physiol 182, 311-322.
44. Siri WE (1956). The gross composition of the body. Adv Biol Med Phys 4, 239-280.
45. Snijders T, Verdijk LB & van Loon LJ (2009). The impact of sarcopenia and exercise training on skeletal muscle satellite cells. Ageing Res Rev 8, 328-338.
46. 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, 332-339.
47. 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, 608-616.
48. 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, E151-E157.
49. Verdijk LB, van Loon L, Meijer K & Savelberg HH (2009c). One-repetition maximum strength test represents a valid means to assess leg strength in vivo in humans. J Sports Sci 27, 59-68.
50. 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, 1147-1154.
51. Waddell JN, Zhang P, Wen Y, Gupta SK, Yevtodiyenko A, Schmidt JV, Bidwell CA, Kumar A & Kuang S (2010). Dlk1 is necessary for proper skeletal muscle development and regeneration. PLoS One 5, e15055.
52. Yang Y, Creer A, Jemiolo B & Trappe S (2005). Time course of myogenic and metabolic gene expression in response to acute exercise in human skeletal muscle. J Appl Physiol 98, 1745-1752.
53. 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, 347-357.