Published online 26 July 2004. doi:10.1083/jcb.200312007
The Rockefeller University Press, 0021-9525 $8.00
JCB, Volume 166, Number 3, 347-357
Muscle satellite cells adopt divergent fates
:
a mechanism for self-renewal?
Peter S. Zammit,
Jon P. Golding,
Yosuke Nagata,
Valérie Hudon,
Terence A. Partridge, and
Jonathan R. Beauchamp
Muscle Cell Biology Group, Medical Research Council Clinical Sciences Centre, Faculty of Medicine, Imperial College, Hammersmith Hospital Campus, London W12 0NN, UK
Address correspondence to P.S. Zammit, Muscle Cell Biology Group, Medical Research Council Clinical Sciences Centre, Faculty of Medicine, Imperial College, Hammersmith Hospital Campus, Du Cane Rd., London W12 0NN, UK. Fax: 44 208 383 8264. email: peter.zammit{at}csc.mrc.ac.uk; or T.A. Partridge, email: terence.partridge{at}csc.mrc.ac.uk
Growth, repair, and regeneration of adult skeletal muscle depends on the persistence of satellite cells: muscle stem cells resident beneath the basal lamina that surrounds each myofiber. However, how the satellite cell compartment is maintained is unclear. Here, we use cultured myofibers to model muscle regeneration and show that satellite cells adopt divergent fates. Quiescent satellite cells are synchronously activated to coexpress the transcription factors Pax7 and MyoD. Most then proliferate, down-regulate Pax7, and differentiate. In contrast, other proliferating cells maintain Pax7 but lose MyoD and withdraw from immediate differentiation. These cells are typically located in clusters, together with Pax7ve progeny destined for differentiation. Some of the Pax7+ve/MyoDve cells then leave the cell cycle, thus regaining the quiescent satellite cell phenotype. Significantly, noncycling cells contained within a cluster can be stimulated to proliferate again. These observations suggest that satellite cells either differentiate or switch from terminal myogenesis to maintain the satellite cell pool.
Key Words: stem; skeletal muscle regeneration; Pax7; MyoD; myogenin
Y. Nagata's present address is Dept. of Life Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro-ku, Tokyo 153-8902, Japan.
V. Hudon's present address is McGill Cancer Center, 3655 Promenade Sir William Osler, Montreal, Quebec, H3G 1Y6, Canada.
Abbreviations used in this paper: EDL, extensor digitorum longus; MLC, myosin light chain; MRF, myogenic regulatory factor.

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-
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-
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[Full Text]
-
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174: 245-253
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-
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[Abstract]
[Full Text]
-
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-
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[Abstract]
[Full Text]
-
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[Full Text]
-
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290: R1062-R1070
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[Full Text]
-
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[Full Text]
-
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(2006). Salamander limb regeneration involves the activation of a multipotent skeletal muscle satellite cell population. J. Cell Biol.
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[Abstract]
[Full Text]
-
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[Abstract]
[Full Text]
-
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[Abstract]
[Full Text]
-
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[Full Text]
-
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118: 4813-4821
[Abstract]
[Full Text]
-
Montarras, D., Morgan, J., Collins, C., Relaix, F., Zaffran, S., Cumano, A., Partridge, T., Buckingham, M.
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[Abstract]
[Full Text]
-
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(2005). Ubiquitin-Proteasome-mediated Degradation, Intracellular Localization, and Protein Synthesis of MyoD and Id1 during Muscle Differentiation. J. Biol. Chem.
280: 26448-26456
[Abstract]
[Full Text]
-
Chen, Y., Zajac, J. D, MacLean, H. E
(2005). Androgen regulation of satellite cell function. J Endocrinol
186: 21-31
[Abstract]
[Full Text]
-
Yi, H., Gruszczynska-Biegala, J., Wood, D., Zhao, Z., Zolkiewska, A.
(2005). Cooperation of the Metalloprotease, Disintegrin, and Cysteine-rich Domains of ADAM12 during Inhibition of Myogenic Differentiation. J. Biol. Chem.
280: 23475-23483
[Abstract]
[Full Text]
-
Jarvinen, T. A. H., Jarvinen, T. L. N., Kaariainen, M., Kalimo, H., Jarvinen, M.
(2005). Muscle Injuries: Biology and Treatment. Am J Sports Med
33: 745-764
[Abstract]
[Full Text]
-
Yoshimoto, M., Chang, H., Shiota, M., Kobayashi, H., Umeda, K., Kawakami, A., Heike, T., Nakahata, T.
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[Abstract]
[Full Text]