Evidence that satellite cell decrement contributes to preferential decline in nuclear number from large fibres during murine age-related muscle atrophy

Journal of Cell Science

Volumn 118, Issue 20, 2005, Pages 4813-4821

  Brack, Andrew S ^a,b   Bildsoe, Heidi ^a   Hughes, Simon M ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ageing; Fibre; Muscle; Myoblast; MyoD; Satellite cell

Indexed keywords

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL FUNCTION; CELL NUCLEUS; CELL SIZE; CONTROLLED STUDY; CYTOPLASM; HYPOTHESIS; MOUSE; MUSCLE ATROPHY; NONHUMAN; PRIORITY JOURNAL; SKELETAL MUSCLE SATELLITE CELL;

AGING; ANIMALS; CELL NUCLEUS; MICE; MUSCLE FIBERS; MUSCULAR ATROPHY; MYOD PROTEIN; RNA, MESSENGER; SATELLITE CELLS, SKELETAL MUSCLE;

ANIMALIA; MURINAE;

EID: 27844595300     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02602     Document Type: Article

References (49)

1. Allen, D. L., Yasui, W., Tanaka, T., Ohira, Y., Nagaoka, S., Sekiguchi, C., Hinds, W. E., Roy, R. R. and Edgerton, V. R. (1996). Myonuclear number and myosin heavy chain expression in rat soleus single muscle fibers after spaceflight. J. Appl. Physiol. 81, 145-151.
2. Allen, D. L., Linderman, J. K., Roy, R. R., Grindeland, R. E., Mukku, V. and Edgerton, V. R. (1997). Growth hormone/IGF-I and/or resistive exercise maintains myonuclear number in hindlimb unweighted muscles. J. Appl. Physiol. 83, 1857-1861.
3. Allen, D. L., Roy, R. R. and Edgerton, V. R. (1999). Myonuclear domains in muscle adaptation and disease. Muscle Nerve 22, 1350-1360.
4. Alway, S. E., Degens, H., Krishnamurthy, G. and Smith, C. A. (2002a). Potential role for Id myogenic repressors in apoptosis and attenuation of hypertrophy in muscles of aged rats. Am. J. Physiol. Cell Physiol. 283, C66-C76.
5. Alway, S. E., Degens, H., Lowe, D. A. and Krishnamurthy, G. (2002b). Increased myogenic repressor Id mRNA and protein levels in hindlimb muscles of aged rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282, R411-R422.
6. Asahara, T. and Kawamoto, A. (2004). Endothelial progenitor cells for postnatal vasculogenesis. Am J. Physiol. Cell Physiol. 287, C572-C579.
7. Asakura, A., Lyons, G. E. and Tapscott, S. J. (1995). The regulation of myoD gene expression: conserved elements mediate expression in embryonic axial muscle. Dev. Biol. 171, 386-398.
8. Barton, E. and Morris, C. (2003). Mechanisms and strategies to counter muscle atrophy. J. Gerontol. A 58, 923-926.
9. Beauchamp, J. R., Heslop, L., Yu, D. S., Tajbakhsh, S., Kelly, R. G., Wernig, A., Buckingham, M. E., Partridge, T. A. and Zammit, P. S. (2000). Expression of CD34 and myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J. Cell Biol. 151, 1221-1234.
10. Bockhold, K. J., Rosenblatt, J. D. and Partridge, T. A. (1998). Aging normal and dystrophic mouse muscle: analysis of myogenicity in cultures of living single fibers. Muscle Nerve 21, 173-183.
11. Bruusgaard, J. C., Liestol, K., Ekmark, M., Kollstad, K. and Gundersen, K. (2003). Number and spatial distribution of nuclei in the muscle fibres of normal mice studied in vivo. J. Physiol. 551, 467-478.
12. Chakravarthy, M. V., Davis, B. S. and Booth, R W. (2000). IGF-I restores satellite cell proliferative potential in immobilized old skeletal muscle. J. Appl. Physiol. 89, 1365-1379.
13. Chargé, S. B., Brack, A. S. and Hughes, S. M. (2002). Aging-related satellite cell differentiation defect occurs prematurely after Ski-induced muscle hypertrophy. Am. J Physiol. Cell Physiol. 283, C1228-C1241.
14. Chen, C. M., Stott, N. S. and Smith, H. K. (2002). Effects of botulinum toxin A injection and exercise on the growth of juvenile rat gastrocnemius muscle. J. Appl. Physiol. 93, 1437-1447.
15. Conboy, I. M., Conboy, M. J., Smythe, G. M. and Rando, T. A. (2003). Notch-mediated restoration of regenerative potential to aged muscle. Science 302, 1575-1577.
16. Cooper, R. N., Tajbakhsh, S., Mouly, V., Cossu, G., Buckingham, M. and Butler-Browne, G. S. (1999). In vivo satellite cell activation via Myf5 and MyoD in regenerating mouse skeletal muscle. J. Cell Sci. 112, 2895-2901.
17. Cornelison, D. D., Olwin, B. B., Rudnicki, M. A. and Wold, B. J. (2000). MyoD(-/-) satellite cells in single-fiber culture are differentiation defective and MRF4 deficient. Dev. Biol. 224, 122-137.
18. Cornelison, D. D., Filla, M. S., Stanley, H. M., Rapraeger, A. C. and Olwin, B. B. (2001). Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev. Biol. 239, 79-94.
19. Darr, K. C. and Schultz, E. (1987). Exercise-induced satellite cell activation in growing and mature skeletal muscle. J. Appl. Physiol. 63, 1816-1821.
20. Dedkov, E. I, Kostrominova, T. Y., Borisov, A. B. and Carlson, B. M. (2003). MyoD and myogenin protein expression in skeletal muscles of senile rats. Cell Tissue Res. 311, 401-416.
21. Dirks, A. and Leeuwenburgh, C. (2002). Apoptosis in skeletal muscle with aging. Am. J. Physiol. Regul. Integr Comp. Physiol. 282, R519-R527.
22. Dupont-Versteegden, E. E., Murphy, R. J., Houle, J. D., Gurley, C. M. and Peterson, C. A. (2000). Mechanisms leading to restoration of muscle size with exercise and transplantation after spinal cord injury. Am. J Physiol. Cell Physiol. 279, C1677-C1684.
23. Gibson, M. C. and Schultz, E. (1983). Age-related differences in absolute numbers of skeletal muscle satellite cells. Muscle Nerve 6, 574-580.
24. Grounds, M. D., Garrett, K. L., Lai, M. C., Wright, W. E. and Beilharz, M. W. (1992). Identification of skeletal muscle precursor cells in vivo by use of MyoD1 and myogenin probes. Cell Tissue Res. 267, 99-104.
25. Hooper, A. C. (1981). Length, diameter and number of ageing skeletal muscle fibres. Gerontology 27, 121-126.
26. Hughes, S. M. and Schiaffino, S. (1999). Control of muscle fibre size: a crucial factor in ageing. Acta Physiol. Scand. 167, 307-312.
27. Hughes, S. M., Koishi, K., Rudnicki, M. and Maggs, A. M. (1997). MyoD protein is differentially accumulated in fast and slow skeletal muscle fibres and required for normal fibre type balance in rodents. Mech. Dev. 61, 151-163.
28. Kasper, C. E. and Xun, L. (1996). Cytoplasm-to-myonucleus ratios in plantaris and soleus muscle fibres following hindlimb suspension. J. Muscle Res. Cell Motil. 17, 603-610.
29. Koishi, K., Zhang, M., McLennan, I. S. and Harris, A. J. (1995). MyoD protein accumulates in satellite cells and is neurally regulated in regenerating myotubes and skeletal muscle fibers. Dev. Dyn. 202, 244-254.
30. Lowe, D. A. and Alway, S. E. (1999). Stretch-induced myogenin, MyoD, and MRF4 expression and acute hypertropby in quail slow-tonic muscle are not dependent upon satellite cell proliferation. Cell Tissue Res. 296, 531-539.
31. Manta, P., Vassilopoulos, D. and Spengos, M. (1987). Nucleo-cytoplasmic ratio in ageing skeletal muscle. Eur Arch. Psychiatry Neurol. Sci. 236, 235-236.
32. Megeney, L. A., Kablar, B., Garrett, K., Anderson, J. E. and Rudnicki, M. A. (1996). MyoD is required for myogenic stem cell function in adult skeletal muscle. Genes Dev. 10, 1173-1183.
33. Mitchell, P. O. and Pavlath, G. K. (2001). A muscle precursor cell-dependent pathway contributes to muscle growth after atrophy. Am. J. Physiol. Cell Physiol. 281, C1706-C1715.
34. Ohira, Y., Yoshinaga, T., Ohara, M., Nonaka, L, Yoshioka, T., Yamashita-Goto, K., Shenkman, B. S., Kozlovskaya, L B., Roy, R. R. and 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.
35. Proctor, D. N., Balagopal, P. and Nair, K. S. (1998). Age-related sarcopenia in humans is associated with reduced synthetic rates of specific muscle proteins. J. Nutr. 128, 351S-355S.
36. Renault, V., Thornell, L. E., Eriksson, P. O., Butler-Browne, G. and Mouly, V. (2002). Regenerative potential of human skeletal muscle during aging. Aging Cell 1, 132-139.
37. Roy, R. R., Monke, S. R., Allen, D. L. and Edgerton, V. R. (1999). Modulation of myonuclear number in functionally overloaded and exercised rat plantaris fibers. J. Appl. Physiol. 87, 634-642.
38. Rudnicki, M. A., Braun, T., Hinuma, S. and Jaenisch, R. (1992). Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 71, 383-390.
39. Sabourin, L. A., Girgis-Gabardo, A., Seale, P., Asakura, A. and Rudnicki, M. A. (1999). Reduced differentiation potential of primary MyoD-/- myogenic cells derived from adult skeletal muscle. J. Cell Biol. 144, 631-643.
40. Sandri, M., Sandri, C., Gilbert, A., Skurk, C., Calabria, E., Picard, A., Walsh, K., Schiaffino, S., Lecker, S. H. and Goldberg, A. L. (2004). Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117, 399-412.
41. Schuierer, M. M., Mann, C. J., Bildsoe, H., Huxley, C. and Hughes, S. M. (2005). Analyses of the differentiation potential of satellite cells from myoD-/-, mdx, and PMP22 C22 mice. BMC Musculoskel. Dis. 6, 15.
42. Sinha-Hikim, L, Roth, S. M., Lee, M. I. and Bhasin, S. (2003). Testosterone-induced muscle hypertrophy is associated with an increase in satellite cell number in healthy, young men. Am. J. Physiol. Endocrinol. Metab. 285, E197-E205.
43. Tamaki, T., Uchiyama, S., Uchiyama, Y., Akatsuka, A., Yoshimura, S., Roy, R. R. and Edgerton, V. R. (2000). Limited myogenic response to a single bout of weight-lifting exercise in old rats. Am. J. Physiol. Cell Physiol. 278, C1143-C1152.
44. Wada, K. I., Takahashi, H., Katsuta, S. and Soya, H. (2002). No decrease in myonuelear number after long-term denervation in mature mice. Am. J. Physiol. Cell Physiol. 283, C484-C488.
45. Webster, C. and Blau, H. M. (1990). Accelerated age-related decline in replicative life-span of Duchenne muscular dystrophy myoblasts: implications for cell and gene therapy. Somatic Cell Mol. Genet. 16, 557-565.
46. Yablonka-Reuveni, Z., Rudnicki, M. A., Rivera, A. J., Primig, M., Anderson, J. E. and Natanson, P. (1999a). The transition from proliferation to differentiation is delayed in satellite cells from mice lacking MyoD. Dev. Biol. 210, 440-455.
47. Yablonka-Reuveni, Z., Seger, R. and Rivera, A. J. (1999b). Fibroblast growth factor promotes recruitment of skeletal muscle satellite cells in young and old rats. J. Histochem. Cytochem. 47, 23-42.
48. Zammit, P. S., Heslop, L., Hudon, V., Rosenblatt, J. D., Tajbakhsh, S., Buckingham, M. E., Beauchamp, J. R. and 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.
49. Zammit, P. S., Golding, J. P., Nagata, Y., Hudon, V., Partridge, T. A. and Beauchamp, J. R. (2004). Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J. Cell Biol. 166, 347-357.