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(Received for publication, November 8, 1996, and in revised form, December 23, 1996)
From the Biology Department, Syracuse University,
Syracuse, New York 13244
It is well established that mitogens inhibit
differentiation of skeletal muscle cells, but the insulin-like growth
factors (IGFs), acting through a single receptor, stimulate both
proliferation and differentiation of myoblasts. Although the IGF-I
mitogenic signaling pathway has been extensively studied in other cell
types, little is known about the signaling pathway leading to
differentiation in skeletal muscle. By using specific inhibitors of the
IGF signal transduction pathway, we have begun to define the signaling
intermediates mediating the two responses to IGFs. We found that
PD098059, an inhibitor of mitogen-activated protein (MAP) kinase kinase
activation, inhibited IGF-stimulated proliferation of L6A1 myoblasts
and the events associated with it, such as phosphorylation of the MAP kinases and elevation of c-fos mRNA and cyclin D protein.
Surprisingly, PD098059 caused a dramatic enhancement of
differentiation, evident both at a morphological (fusion of myoblasts
into myotubes) and biochemical level (elevation of myogenin and p21
cyclin-dependent kinase inhibitor expression, as well as
creatine kinase activity). In sharp contrast, LY294002, an inhibitor of
phosphatidylinositol 3-kinase, and rapamycin, an inhibitor of the
activation of p70 S6 kinase (p70S6k), completely abolished
IGF stimulation of L6A1 differentiation. We found that
p70S6k activity increased substantially during
differentiation, and this increase was further enhanced by PD098059.
Our results demonstrate that the MAP kinase pathway plays a primary
role in the mitogenic response and is inhibitory to the myogenic
response in L6A1 myoblasts, while activation of the
phosphatidylinositol 3-kinase/p70S6k pathway is essential
for IGF-stimulated differentiation. Thus, it appears that signaling
from the IGF-I receptor utilizes two distinct pathways leading either
to proliferation or differentiation.
Volume 272, Number 10,
Issue of March 7, 1997
pp. 6653-6662
©1997 by The American Society for Biochemistry and Molecular Biology, Inc.
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E. M. Wilson, J. Tureckova, and P. Rotwein Permissive Roles of Phosphatidyl Inositol 3-Kinase and Akt in Skeletal Myocyte Maturation Mol. Biol. Cell, February 1, 2004; 15(2): 497 - 505. [Abstract] [Full Text] [PDF]
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X. Wang, S. R. Thomson, J. D. Starkey, J. L. Page, A. D. Ealy, and S. E. Johnson Transforming Growth Factor {beta}1 Is Up-regulated by Activated Raf in Skeletal Myoblasts but Does Not Contribute to the Differentiation-defective Phenotype J. Biol. Chem., January 23, 2004; 279(4): 2528 - 2534. [Abstract] [Full Text] [PDF]
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F. Haddad and G. R. Adams Inhibition of MAP/ERK kinase prevents IGF-I-induced hypertrophy in rat muscles J Appl Physiol, January 1, 2004; 96(1): 203 - 210. [Abstract] [Full Text] [PDF]
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E. Erbay, I.-H. Park, P. D. Nuzzi, C. J. Schoenherr, and J. Chen IGF-II transcription in skeletal myogenesis is controlled by mTOR and nutrients J. Cell Biol., December 8, 2003; 163(5): 931 - 936. [Abstract] [Full Text] [PDF]
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 S. P. Kirk, J. M. Oldham, F. Jeanplong, and J. J. Bass Insulin-like Growth Factor-II Delays Early but Enhances Late Regeneration of Skeletal Muscle J. Histochem. Cytochem., December 1, 2003; 51(12): 1611 - 1620. [Abstract] [Full Text] [PDF]
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 N. C. Sundgren, G. D. Giraud, J. M. Schultz, M. R. Lasarev, P. J. S. Stork, and K. L. Thornburg Extracellular signal-regulated kinase and phosphoinositol-3 kinase mediate IGF-1 induced proliferation of fetal sheep cardiomyocytes Am J Physiol Regulatory Integrative Comp Physiol, December 1, 2003; 285(6): R1481 - R1489. [Abstract] [Full Text] [PDF]
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Y. Kataoka, I. Matsumura, S. Ezoe, S. Nakata, E. Takigawa, Y. Sato, A. Kawasaki, T. Yokota, K. Nakajima, A. Felsani, et al. Reciprocal Inhibition between MyoD and STAT3 in the Regulation of Growth and Differentiation of Myoblasts J. Biol. Chem., November 7, 2003; 278(45): 44178 - 44187. [Abstract] [Full Text] [PDF]
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 I Sermet-Gaudelus, J C Souberbielle, I Azhar, J C Ruiz, P Magnine, V Colomb, C Le Bihan, D Folio, and G Lenoir Insulin-like growth factor I correlates with lean body mass in cystic fibrosis patients Arch. Dis. Child., November 1, 2003; 88(11): 956 - 961. [Abstract] [Full Text] [PDF]
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M. L. Hribal, J. Nakae, T. Kitamura, J. R. Shutter, and D. Accili Regulation of insulin-like growth factor-dependent myoblast differentiation by Foxo forkhead transcription factors J. Cell Biol., August 18, 2003; 162(4): 535 - 541. [Abstract] [Full Text] [PDF]
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S. R. Broussard, R. H. MCCusker, J. E. Novakofski, K. Strle, W. Hong Shen, R. W. Johnson, G. G. Freund, R. Dantzer, and K. W. Kelley Cytokine-Hormone Interactions: Tumor Necrosis Factor {alpha} Impairs Biologic Activity and Downstream Activation Signals of the Insulin-Like Growth Factor I Receptor in Myoblasts Endocrinology, July 1, 2003; 144(7): 2988 - 2996. [Abstract] [Full Text] [PDF]
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O. Ostrovsky and E. Bengal The Mitogen-activated Protein Kinase Cascade Promotes Myoblast Cell Survival by Stabilizing the Cyclin-dependent Kinase Inhibitor, p21WAF1 Protein J. Biol. Chem., May 30, 2003; 278(23): 21221 - 21231. [Abstract] [Full Text] [PDF]
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D. M. Cox, M. Du, M. Marback, E. C. C. Yang, J. Chan, K. W. M. Siu, and J. C. McDermott Phosphorylation Motifs Regulating the Stability and Function of Myocyte Enhancer Factor 2A J. Biol. Chem., April 18, 2003; 278(17): 15297 - 15303. [Abstract] [Full Text] [PDF]
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V. De Arcangelis, D. Coletti, M. Conti, M. Lagarde, M. Molinaro, S. Adamo, G. Nemoz, and F. Naro IGF-I-induced Differentiation of L6 Myogenic Cells Requires the Activity of cAMP-Phosphodiesterase Mol. Biol. Cell, April 1, 2003; 14(4): 1392 - 1404. [Abstract] [Full Text] [PDF]
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J. F. Kuemmerle IGF-I elicits growth of human intestinal smooth muscle cells by activation of PI3K, PDK-1, and p70S6 kinase Am J Physiol Gastrointest Liver Physiol, March 1, 2003; 284(3): G411 - G422. [Abstract] [Full Text] [PDF]
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 M. M. Bamman, V. J. Hill, G. R. Adams, F. Haddad, C. J. Wetzstein, B. A. Gower, A. Ahmed, and G. R. Hunter Gender Differences in Resistance-Training-Induced Myofiber Hypertrophy Among Older Adults J. Gerontol. A Biol. Sci. Med. Sci., February 1, 2003; 58(2): B108 - 116. [Abstract] [Full Text] [PDF]
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E. E. Spangenburg, T. Abraha, T. E. Childs, J. S. Pattison, and F. W. Booth Skeletal muscle IGF-binding protein-3 and -5 expressions are age, muscle, and load dependent Am J Physiol Endocrinol Metab, February 1, 2003; 284(2): E340 - E350. [Abstract] [Full Text] [PDF]
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 E. Cellier, M. Mage, J. Duchene, C. Pecher, R. Couture, J.-L. Bascands, and J.-P. Girolami Bradykinin reduces growth factor-induced glomerular ERK1/2 phosphorylation Am J Physiol Renal Physiol, February 1, 2003; 284(2): F282 - F292. [Abstract] [Full Text] [PDF]
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 E. Chaum and H. Yang Transgenic Expression of IGF-1 Modifies the Proliferative Potential of Human Retinal Pigment Epithelial Cells Invest. Ophthalmol. Vis. Sci., December 1, 2002; 43(12): 3758 - 3764. [Abstract] [Full Text] [PDF]
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Y. Yoshiko, K. Hirao, and N. Maeda Differentiation in C2C12 myoblasts depends on the expression of endogenous IGFs and not serum depletion Am J Physiol Cell Physiol, October 1, 2002; 283(4): C1278 - C1286. [Abstract] [Full Text] [PDF]
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A. Mauro, C. Ciccarelli, P. De Cesaris, A. Scoglio, M. Bouche, M. Molinaro, A. Aquino, and B. M. Zani PKC{alpha}-mediated ERK, JNK and p38 activation regulates the myogenic program in human rhabdomyosarcoma cells J. Cell Sci., September 15, 2002; 115(18): 3587 - 3599. [Abstract] [Full Text] [PDF]
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G. R. Adams Exercise Effects on Muscle Insulin Signaling and Action: Invited Review: Autocrine/paracrine IGF-I and skeletal muscle adaptation J Appl Physiol, September 1, 2002; 93(3): 1159 - 1167. [Abstract] [Full Text] [PDF]
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M. Carrasco, J. Canicio, M. Palacin, A. Zorzano, and P. Kaliman Identification of Intracellular Signaling Pathways that Induce Myotonic Dystrophy Protein Kinase Expression during Myogenesis Endocrinology, August 1, 2002; 143(8): 3017 - 3025. [Abstract] [Full Text] [PDF]
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X. Zhang, L. Shu, H. Hosoi, K. G. Murti, and P. J. Houghton Predominant Nuclear Localization of Mammalian Target of Rapamycin in Normal and Malignant Cells in Culture J. Biol. Chem., July 26, 2002; 277(31): 28127 - 28134. [Abstract] [Full Text] [PDF]
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 G. Pallafacchina, E. Calabria, A. L. Serrano, J. M. Kalhovde, and S. Schiaffino A protein kinase B-dependent and rapamycin-sensitive pathway controls skeletal muscle growth but not fiber type specification PNAS, July 9, 2002; 99(14): 9213 - 9218. [Abstract] [Full Text] [PDF]
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F. Haddad and G. R. Adams Exercise Effects on Muscle Insulin Signaling and Action: Selected Contribution: Acute cellular and molecular responses to resistance exercise J Appl Physiol, July 1, 2002; 93(1): 394 - 403. [Abstract] [Full Text] [PDF]
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E. E. Spangenburg and F. W. Booth Multiple signaling pathways mediate LIF-induced skeletal muscle satellite cell proliferation Am J Physiol Cell Physiol, July 1, 2002; 283(1): C204 - C211. [Abstract] [Full Text] [PDF]
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M. I. Kontaridis, X. Liu, L. Zhang, and A. M. Bennett Role of SHP-2 in Fibroblast Growth Factor Receptor-Mediated Suppression of Myogenesis in C2C12 Myoblasts Mol. Cell. Biol., June 1, 2002; 22(11): 3875 - 3891. [Abstract] [Full Text] [PDF]
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B. M. Scicchitano, L. Spath, A. Musaro, M. Molinaro, S. Adamo, and C. Nervi AVP Induces Myogenesis through the Transcriptional Activation of the Myocyte Enhancer Factor 2 Mol. Endocrinol., June 1, 2002; 16(6): 1407 - 1416. [Abstract] [Full Text] [PDF]
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Q. Xu, L. Yu, L. Liu, C. F. Cheung, X. Li, S.-P. Yee, X.-J. Yang, and Z. Wu p38 Mitogen-activated Protein Kinase-, Calcium-Calmodulin-dependent Protein Kinase-, and Calcineurin-mediated Signaling Pathways Transcriptionally Regulate Myogenin Expression Mol. Biol. Cell, June 1, 2002; 13(6): 1940 - 1952. [Abstract] [Full Text] [PDF]
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L. Shu, X. Zhang, and P. J. Houghton Myogenic Differentiation Is Dependent on Both the Kinase Function and the N-terminal Sequence of Mammalian Target of Rapamycin J. Biol. Chem., May 3, 2002; 277(19): 16726 - 16732. [Abstract] [Full Text] [PDF]
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E. R. Barton, L. Morris, A. Musaro, N. Rosenthal, and H. L. Sweeney Muscle-specific expression of insulin-like growth factor I counters muscle decline in mdx mice J. Cell Biol., April 1, 2002; 157(1): 137 - 148. [Abstract] [Full Text] [PDF]
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