The muscle regulators MyoD and Myf-5 control cell cycle withdrawal and induction of differentiation in skeletal muscle cells. By immunofluorescence analysis, we show that MyoD and Myf-5 expression patterns become mutually exclusive when C2 cells are induced to differentiate with Myf-5 staining present in cells which fail to differentiate. Isolation of these undifferentiated cells reveals that upon serum stimulation they reenter the cell cycle, express MyoD and downregulate Myf-5. Similar regulations of MyoD and Myf-5 were observed using cultured primary myoblasts derived from satellite cells. To further analyze these regulations of MyoD and Myf-5 expression, we synchronized proliferating myoblasts. Analysis of MyoD and Myf-5 expression during cell cycle progression revealed distinct and contrasting profiles of expression. MyoD is absent in G0, peaks in mid-G1, falls to its minimum level at G1/S and reaugments from S to M. In contrast, Myf-5 protein is high in G0, decreases during G1 and reappears at the end of G1 to remain stable until mitosis. These data demonstrate that the two myogenic factors MyoD and Myf-5 undergo specific and distinct cell cycle–dependent regulation, thus establishing a correlation between the cell cycle–specific ratios of MyoD and Myf-5 and the capacity of cells to differentiate: (a) in G1, when cells express high levels of MyoD and enter differentiation; (b) in G0, when cells express high levels of Myf-5 and fail to differentiate.
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21 September 1998
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September 21 1998
The Muscle Regulatory Factors MyoD and Myf-5 Undergo Distinct Cell Cycle–specific Expression in Muscle Cells
Magali Kitzmann,
Magali Kitzmann
*Cell Biology Unit, Institut de Génétique Humaine, Unité Propre de Recherche 1142, Centre National de la Recherche Scientifique, 34396 Montpellier Cedex 5, France; and ‡Institut Pasteur, Department de Biologie Moleculaire, 75724 Paris Cedex 15, France
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Gilles Carnac,
Gilles Carnac
*Cell Biology Unit, Institut de Génétique Humaine, Unité Propre de Recherche 1142, Centre National de la Recherche Scientifique, 34396 Montpellier Cedex 5, France; and ‡Institut Pasteur, Department de Biologie Moleculaire, 75724 Paris Cedex 15, France
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Marie Vandromme,
Marie Vandromme
*Cell Biology Unit, Institut de Génétique Humaine, Unité Propre de Recherche 1142, Centre National de la Recherche Scientifique, 34396 Montpellier Cedex 5, France; and ‡Institut Pasteur, Department de Biologie Moleculaire, 75724 Paris Cedex 15, France
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Michael Primig,
Michael Primig
*Cell Biology Unit, Institut de Génétique Humaine, Unité Propre de Recherche 1142, Centre National de la Recherche Scientifique, 34396 Montpellier Cedex 5, France; and ‡Institut Pasteur, Department de Biologie Moleculaire, 75724 Paris Cedex 15, France
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Ned J.C. Lamb,
Ned J.C. Lamb
*Cell Biology Unit, Institut de Génétique Humaine, Unité Propre de Recherche 1142, Centre National de la Recherche Scientifique, 34396 Montpellier Cedex 5, France; and ‡Institut Pasteur, Department de Biologie Moleculaire, 75724 Paris Cedex 15, France
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Anne Fernandez
Anne Fernandez
*Cell Biology Unit, Institut de Génétique Humaine, Unité Propre de Recherche 1142, Centre National de la Recherche Scientifique, 34396 Montpellier Cedex 5, France; and ‡Institut Pasteur, Department de Biologie Moleculaire, 75724 Paris Cedex 15, France
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Magali Kitzmann
*Cell Biology Unit, Institut de Génétique Humaine, Unité Propre de Recherche 1142, Centre National de la Recherche Scientifique, 34396 Montpellier Cedex 5, France; and ‡Institut Pasteur, Department de Biologie Moleculaire, 75724 Paris Cedex 15, France
Gilles Carnac
*Cell Biology Unit, Institut de Génétique Humaine, Unité Propre de Recherche 1142, Centre National de la Recherche Scientifique, 34396 Montpellier Cedex 5, France; and ‡Institut Pasteur, Department de Biologie Moleculaire, 75724 Paris Cedex 15, France
Marie Vandromme
*Cell Biology Unit, Institut de Génétique Humaine, Unité Propre de Recherche 1142, Centre National de la Recherche Scientifique, 34396 Montpellier Cedex 5, France; and ‡Institut Pasteur, Department de Biologie Moleculaire, 75724 Paris Cedex 15, France
Michael Primig
*Cell Biology Unit, Institut de Génétique Humaine, Unité Propre de Recherche 1142, Centre National de la Recherche Scientifique, 34396 Montpellier Cedex 5, France; and ‡Institut Pasteur, Department de Biologie Moleculaire, 75724 Paris Cedex 15, France
Ned J.C. Lamb
*Cell Biology Unit, Institut de Génétique Humaine, Unité Propre de Recherche 1142, Centre National de la Recherche Scientifique, 34396 Montpellier Cedex 5, France; and ‡Institut Pasteur, Department de Biologie Moleculaire, 75724 Paris Cedex 15, France
Anne Fernandez
*Cell Biology Unit, Institut de Génétique Humaine, Unité Propre de Recherche 1142, Centre National de la Recherche Scientifique, 34396 Montpellier Cedex 5, France; and ‡Institut Pasteur, Department de Biologie Moleculaire, 75724 Paris Cedex 15, France
Address correspondence to Anne Fernandez, Cell Biology Unit, IGH UPR 1142, 141 rue de la Cardonille, 34396 Montpellier Cedex 5, France. Tel.: 33 4 99 61 99 14. Fax: 33 4 99 61 99 01. E-mail: [email protected]
The first two authors contributed equally to this work.
Received:
April 16 1998
Revision Received:
August 14 1998
Online ISSN: 1540-8140
Print ISSN: 0021-9525
1998
J Cell Biol (1998) 142 (6): 1447–1459.
Article history
Received:
April 16 1998
Revision Received:
August 14 1998
Citation
Magali Kitzmann, Gilles Carnac, Marie Vandromme, Michael Primig, Ned J.C. Lamb, Anne Fernandez; The Muscle Regulatory Factors MyoD and Myf-5 Undergo Distinct Cell Cycle–specific Expression in Muscle Cells . J Cell Biol 21 September 1998; 142 (6): 1447–1459. doi: https://doi.org/10.1083/jcb.142.6.1447
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