Growth factor control of skeletal muscle differentiation: commitment to terminal differentiation occurs in G1 phase and is repressed by fibroblast growth factor

doi:10.1083/jcb.105.2.949

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Growth factor control of skeletal muscle differentiation: commitment to terminal differentiation occurs in G1 phase and is repressed by fibroblast growth factor

CH Clegg, TA Linkhart, BB Olwin and SD Hauschka

Analysis of MM14 mouse myoblasts demonstrates that terminal differentiation is repressed by pure preparations of both acidic and basic fibroblast growth factor (FGF). Basic FGF is approximately 30- fold more potent than acidic FGF and it exhibits half maximal activity in clonal assays at 0.03 ng/ml (2 pM). FGF repression occurs only during the G1 phase of the cell cycle by a mechanism that appears to be independent of ongoing cell proliferation. When exponentially growing myoblasts are deprived of FGF, cells become postmitotic within 2-3 h, express muscle-specific proteins within 6-7 h, and commence fusion within 12-14 h. Although expression of these three terminal differentiation phenotypes occurs at different times, all are initiated by a single regulatory "commitment" event in G1. The entire population commits to terminal differentiation within 12.5 h of FGF removal as all cells complete the cell cycle and move into G1. Differentiation does not require a new round of DNA synthesis. Comparison of MM14 behavior with other myoblast types suggests a general model for skeletal muscle development in which specific growth factors serve the dual role of stimulating myoblast proliferation and directly repressing terminal differentiation.
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Shi, X., Garry, D. J. (2006). Muscle stem cells in development, regeneration, and disease.. Genes Dev. 20: 1692-1708 [Abstract] [Full Text]
Melcon, G., Kozlov, S., Cutler, D. A., Sullivan, T., Hernandez, L., Zhao, P., Mitchell, S., Nader, G., Bakay, M., Rottman, J. N., Hoffman, E. P., Stewart, C. L. (2006). Loss of emerin at the nuclear envelope disrupts the Rb1/E2F and MyoD pathways during muscle regeneration. Hum Mol Genet 15: 637-651 [Abstract] [Full Text]
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Scicchitano, B. M., Spath, L., Musaro, A., Molinaro, M., Rosenthal, N., Nervi, C., Adamo, S. (2005). Vasopressin-dependent Myogenic Cell Differentiation Is Mediated by Both Ca2+/Calmodulin-dependent Kinase and Calcineurin Pathways. Mol. Biol. Cell 16: 3632-3641 [Abstract] [Full Text]
Jones, N. C., Tyner, K. J., Nibarger, L., Stanley, H. M., Cornelison, D. D.W., Fedorov, Y. V., Olwin, B. B. (2005). The p38{alpha}/{beta} MAPK functions as a molecular switch to activate the quiescent satellite cell. JCB 169: 105-116 [Abstract] [Full Text]
Sasson, I. E., Stern, M. J. (2004). FGF and PI3 kinase signaling pathways antagonistically modulate sex muscle differentiation in C. elegans. Development 131: 5381-5392 [Abstract] [Full Text]
Dhawan, J., Helfman, D. M. (2004). Modulation of acto-myosin contractility in skeletal muscle myoblasts uncouples growth arrest from differentiation. J. Cell Sci. 117: 3735-3748 [Abstract] [Full Text]
Himeda, C. L., Ranish, J. A., Angello, J. C., Maire, P., Aebersold, R., Hauschka, S. D. (2004). Quantitative Proteomic Identification of Six4 as the Trex-Binding Factor in the Muscle Creatine Kinase Enhancer. Mol. Cell. Biol. 24: 2132-2143 [Abstract] [Full Text]
Favreau, C., Higuet, D., Courvalin, J.-C., Buendia, B. (2004). Expression of a Mutant Lamin A That Causes Emery-Dreifuss Muscular Dystrophy Inhibits In Vitro Differentiation of C2C12 Myoblasts. Mol. Cell. Biol. 24: 1481-1492 [Abstract] [Full Text]
Suzuki, M., Angata, K., Nakayama, J., Fukuda, M. (2003). Polysialic Acid and Mucin Type O-Glycans on the Neural Cell Adhesion Molecule Differentially Regulate Myoblast Fusion. J. Biol. Chem. 278: 49459-49468 [Abstract] [Full Text]
Nguyen, Q.-G. V., Buskin, J. N., Himeda, C. L., Shield, M. A., Hauschka, S. D. (2003). Differences in the Function of Three Conserved E-boxes of the Muscle Creatine Kinase Gene in Cultured Myocytes and in Transgenic Mouse Skeletal and Cardiac Muscle. J. Biol. Chem. 278: 46494-46505 [Abstract] [Full Text]
Neuhaus, P., Oustanina, S., Loch, T., Kruger, M., Bober, E., Dono, R., Zeller, R., Braun, T. (2003). Reduced Mobility of Fibroblast Growth Factor (FGF)-Deficient Myoblasts Might Contribute to Dystrophic Changes in the Musculature of FGF2/FGF6/mdx Triple-Mutant Mice. Mol. Cell. Biol. 23: 6037-6048 [Abstract] [Full Text]
Langley, B., Thomas, M., Bishop, A., Sharma, M., Gilmour, S., Kambadur, R. (2002). Myostatin Inhibits Myoblast Differentiation by Down-regulating MyoD Expression. J. Biol. Chem. 277: 49831-49840 [Abstract] [Full Text]
Buehler, A., Martire, A., Strohm, C., Wolfram, S., Fernandez, B., Palmen, M., Wehrens, X. H.T, Doevendans, P. A, Franz, W. M, Schaper, W., Zimmermann, R. (2002). Angiogenesis-independent cardioprotection in FGF-1 transgenic mice. Cardiovasc Res 55: 768-777 [Abstract] [Full Text]
Kontaridis, M. I., Liu, X., Zhang, L., Bennett, A. M. (2002). Role of SHP-2 in Fibroblast Growth Factor Receptor-Mediated Suppression of Myogenesis in C2C12 Myoblasts. Mol. Cell. Biol. 22: 3875-3891 [Abstract] [Full Text]
Scicchitano, B. M., Spath, L., Musaro, A., Molinaro, M., Adamo, S., Nervi, C. (2002). AVP Induces Myogenesis through the Transcriptional Activation of the Myocyte Enhancer Factor 2. Mol. Endocrinol. 16: 1407-1416 [Abstract] [Full Text]
Fedorov, Y. V., Jones, N. C., Olwin, B. B. (2002). Atypical Protein Kinase Cs Are the Ras Effectors That Mediate Repression of Myogenic Satellite Cell Differentiation. Mol. Cell. Biol. 22: 1140-1149 [Abstract] [Full Text]
Marics, I., Padilla, F., Guillemot, J.-F., Scaal, M., Marcelle, C. (2002). FGFR4 signaling is a necessary step in limb muscle differentiation. Development 129: 4559-4569 [Abstract] [Full Text]
Sachidanandan, C., Sambasivan, R., Dhawan, J. (2002). Tristetraprolin and LPS-inducible CXC chemokine are rapidly induced in presumptive satellite cells in response to skeletal muscle injury. J. Cell Sci. 115: 2701-2712 [Abstract] [Full Text]
Hawke, T. J., Garry, D. J. (2001). Myogenic satellite cells: physiology to molecular biology. J. Appl. Physiol. 91: 534-551 [Abstract] [Full Text]
Fedorov, Y. V., Rosenthal, R. S., Olwin, B. B. (2001). Oncogenic Ras-induced Proliferation Requires Autocrine Fibroblast Growth Factor 2 Signaling in Skeletal Muscle Cells. JCB 152: 1301-1306 [Abstract] [Full Text]
Kästner, S., Elias, M. C., Rivera, A. J., Yablonka–Reuveni, Z. (2000). Gene Expression Patterns of the Fibroblast Growth Factors and Their Receptors During Myogenesis of Rat Satellite Cells. J. Histochem. Cytochem. 48: 1079-1096 [Abstract] [Full Text]
Naro, F., Sette, C., Vicini, E., De Arcangelis, V., Grange, M., Conti, M., Lagarde, M., Molinaro, M., Adamo, S., Némoz, G. (1999). Involvement of Type 4 cAMP-Phosphodiesterase in the Myogenic Differentiation of L6 Cells. Mol. Biol. Cell 10: 4355-4367 [Abstract] [Full Text]
Luo, Z. D., Wang, Y., Werlen, G., Camp, S., Chien, K. R., Taylor, P. (1999). Calcineurin Enhances Acetylcholinesterase mRNA Stability during C2-C12 Muscle Cell Differentiation. Mol. Pharmacol. 56: 886-894 [Abstract] [Full Text]
Zhang, P., Wong, C., Liu, D., Finegold, M., Harper, J. W., Elledge, S. J. (1999). p21CIP1 and p57KIP2 control muscle differentiation at the myogenin step. Genes Dev. 13: 213-224 [Abstract] [Full Text]
Yablonka–Reuveni, Z., Seger, R., Rivera, A. J. (1999). Fibroblast Growth Factor Promotes Recruitment of Skeletal Muscle Satellite Cells in Young and Old Rats. J. Histochem. Cytochem. 47: 23-42 [Abstract] [Full Text]
Fedorov, Y. V., Jones, N. C., Olwin, B. B. (1998). Regulation of Myogenesis by Fibroblast Growth Factors Requires Beta-Gamma Subunits of Pertussis Toxin-Sensitive G Proteins. Mol. Cell. Biol. 18: 5780-5787 [Abstract] [Full Text]
Kitzmann, M., Carnac, G., Vandromme, M., Primig, M., Lamb, N. J.C., Fernandez, A. (1998). The Muscle Regulatory Factors MyoD and Myf-5 Undergo Distinct Cell Cycle-specific Expression in Muscle Cells. JCB 142: 1447-1459 [Abstract] [Full Text]
Kudla, A. J., Jones, N. C., Scott Rosenthal, R., Arthur, K., Clase, K. L., Olwin, B. B. (1998). The FGF Receptor-1 Tyrosine Kinase Domain Regulates Myogenesis but Is Not Sufficient to Stimulate Proliferation. JCB 142: 241-250 [Abstract] [Full Text]
Weyman, C. M., Wolfman, A. (1998). Mitogen-Activated Protein Kinase Kinase (MEK) Activity Is Required for Inhibition of Skeletal Muscle Differentiation by Insulin-Like Growth Factor 1 or Fibroblast Growth Factor 2. Endocrinology 139: 1794-1800 [Abstract] [Full Text]
Miralles, F., Ron, D., Baiget, M., Felez, J., Munoz-Canoves, P. (1998). Differential Regulation of Urokinase-type Plasminogen Activator Expression by Basic Fibroblast Growth Factor and Serum in Myogenesis. REQUIREMENT OF A COMMON MITOGEN-ACTIVATED PROTEIN KINASE PATHWAY. J. Biol. Chem. 273: 2052-2058 [Abstract] [Full Text]
Sarbassov, D. D., Jones, L. G., Peterson, C. A. (1997). Extracellular Signal-Regulated Kinase-1 and -2 Respond Differently to Mitogenic and Differentiative Signaling Pathways in Myoblasts. Mol. Endocrinol. 11: 2038-2047 [Abstract] [Full Text]
Coolican, S. A., Samuel, D. S., Ewton, D. Z., McWade, F. J., Florini, J. R. (1997). The Mitogenic and Myogenic Actions of Insulin-like Growth Factors Utilize Distinct Signaling Pathways. J. Biol. Chem. 272: 6653-6662 [Abstract] [Full Text]
Chu, C., Cogswell, J., Kohtz, D. S. (1997). MyoD Functions as a Transcriptional Repressor in Proliferating Myoblasts. J. Biol. Chem. 272: 3145-3148 [Abstract] [Full Text]
Stolen, C., Jackson, M., Griep, A. (1997). Overexpression of FGF-2 modulates fiber cell differentiation and survival in the mouse lens. Development 124: 4009-4017 [Abstract]
Stern, H., Lin-Jones, J, Hauschka, S. (1997). Synergistic interactions between bFGF and a TGF-beta family member may mediate myogenic signals from the neural tube. Development 124: 3511-3523 [Abstract]
Suidan, H. S., Niclou, S. P., Dreessen, J., Beltraminelli, N., Monard, D. (1996). The Thrombin Receptor Is Present in Myoblasts and Its Expression Is Repressed upon Fusion. J. Biol. Chem. 271: 29162-29169 [Abstract] [Full Text]
Fabre-Suver, C., Hauschka, S. D. (1996). A Novel Site in the Muscle Creatine Kinase Enhancer Is Required for Expression in Skeletal but Not Cardiac Muscle. J. Biol. Chem. 271: 4646-4652 [Abstract] [Full Text]
Mannion, J. D., Blood, V., Bailey, W., Bauer, T. L., Magno, M. G., DiMeo, F., Epple, A., Spinale, F. G. (1996). THE EFFECT OF BASIC FIBROBLAST GROWTH FACTOR ON THE BLOOD FLOW AND MORPHOLOGIC FEATURES OF A LATISSIMUS DORSI CARDIOMYOPLASTY. J. Thorac. Cardiovasc. Surg. 111: 19-28 [Abstract] [Full Text]
Itoh, N, Mima, T, Mikawa, T (1996). Loss of fibroblast growth factor receptors is necessary for terminal differentiation of embryonic limb muscle. Development 122: 291-300 [Abstract]
Patrie, K. M., Kudla, A. J., Olwin, B. B., Chiu, I.-M. (1995). Conservation of Ligand Specificity between the Mammalian and Amphibian Fibroblast Growth Factor Receptors. J. Biol. Chem. 270: 29018-29024 [Abstract] [Full Text]
Apone, S., Hauschka, S. D. (1995). Muscle Gene E-box Control Elements. J. Biol. Chem. 270: 21420-21427 [Abstract] [Full Text]
Chen, X., Raab, G., Deutsch, U., Zhang, J., Ezzell, R. M., Klagsbrun, M. (1995). Induction of Heparin-binding EGF-like Growth Factor Expression during Myogenesis. J. Biol. Chem. 270: 18285-18294 [Abstract] [Full Text]
Rao, S. S., Kohtz, D. S. (1995). Positive and Negative Regulation of D-type Cyclin Expression in Skeletal Myoblasts by Basic Fibroblast Growth Factor and Transforming Growth Factor beta. J. Biol. Chem. 270: 4093-4100 [Abstract] [Full Text]
Stern, H., Brown, A., Hauschka, S. (1995). Myogenesis in paraxial mesoderm: preferential induction by dorsal neural tube and by cells expressing Wnt-1. Development 121: 3675-3686 [Abstract]
Quarto, N, Amalric, F (1994). Heparan sulfate proteoglycans as transducers of FGF-2 signalling. J. Cell Sci. 107: 3201-3212 [Abstract]
Cusella-De Angelis, M., Molinari, S, Le Donne, A, Coletta, M, Vivarelli, E, Bouche, M, Molinaro, M, Ferrari, S, Cossu, G (1994). Differential response of embryonic and fetal myoblasts to TGF beta: a possible regulatory mechanism of skeletal muscle histogenesis. Development 120: 925-933 [Abstract]
Marcelle, C, Eichmann, A, Halevy, O, Breant, C, Le Douarin, N. (1994). Distinct developmental expression of a new avian fibroblast growth factor receptor. Development 120: 683-694 [Abstract]
deLapeyriere, O, Ollendorff, V, Planche, J, Ott, M., Pizette, S, Coulier, F, Birnbaum, D (1993). Expression of the Fgf6 gene is restricted to developing skeletal muscle in the mouse embryo. Development 118: 601-611 [Abstract]
Blauer, M, Kohonen, J, Leivonen, I, Vilja, P, Tuohimaa, P (1992). Inhibin alpha- and beta A-subunit immunoreactivity in the chicken embryo during morphogenesis. Development 115: 1079-1086 [Abstract]
Rapraeger, A., Krufka, A, Olwin, B. (1991). Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 252: 1705-1708 [Abstract]
de la Brousse, F C, Emerson, C P (1990). Localized expression of a myogenic regulatory gene, qmf1, in the somite dermatome of avian embryos.. Genes Dev. 4: 567-581 [Abstract]
Edmondson, D G, Olson, E N (1989). A gene with homology to the myc similarity region of MyoD1 is expressed during myogenesis and is sufficient to activate the muscle differentiation program.. Genes Dev. 3: 628-640 [Abstract]
Tortorella, L. L., Milasincic, D. J., Pilch, P. F. (2001). Critical Proliferation-independent Window for Basic Fibroblast Growth Factor Repression of Myogenesis via the p42/p44 MAPK Signaling Pathway. J. Biol. Chem. 276: 13709-13717 [Abstract] [Full Text]
Whitney, M. L., Otto, K. G., Blau, C. A., Reinecke, H., Murry, C. E. (2001). Control of Myoblast Proliferation with a Synthetic Ligand. J. Biol. Chem. 276: 41191-41196 [Abstract] [Full Text]