Cell Cycle Withdrawal Promotes Myogenic Induction of Akt, a Positive Modulator of Myocyte Survival

REFERENCES

• Alessi, D. R., M. Andjelkovic, B. Caudwell, P. Cron, N. Morrice, P. Cohen, and J. Hemmings 1996. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15:6541–6551.
   PubMed Web of Science ®Google Scholar
• Altomare, D. A., K. Guo, J. Q. Cheng, G. Sonoda, K. Walsh, and J. Testa 1995. Cloning, chromosomal localization and expression analysis of the mouse Akt2 oncogene. Oncogene 11:1055–1060.
   PubMed Web of Science ®Google Scholar
• Altomare, D. A., G. E. Lyons, Y. Mitsuuchi, J. Q. Cheng, and J. Testa 1998. Akt2 mRNA is highly expressed in embryonic brown fat and AKT2 kinase is activated by insulin. Oncogene 16:2407–2411.
   PubMedGoogle Scholar
• Andrés, V., and J. Walsh 1996. Myogenin expression, cell cycle withdrawal and phenotypic differentiation are temporally separable events that precede cell fusion upon myogenesis. J. Cell Biol. 132:657–666.
   PubMedGoogle Scholar
• Bellacosa, A., T. F. Franke, M. E. Gonzalez-Portal, K. Datta, T. Taguchi, J. Gardner, J. Q. Cheng, J. R. Testa, and J. Tsichlis 1993. Structure, expression and chromosomal mapping of c-akt: relationship to v-akt and its implications. Oncogene 8:745–754.
   PubMed Web of Science ®Google Scholar
• Bennett, A. M., and J. Tonks 1997. Regulation of distinct stages of skeletal muscle differentiation by mitogen-activated protein kinases. Science 278:1288–1291.
   PubMed Web of Science ®Google Scholar
• Bett, A. J., W. Haddara, L. Prevec, and J. Graham 1994. An efficient and flexible system for construction of adenovirus vectors with insertions or deletions in early regions 1 and 3. Proc. Natl. Acad. Sci. USA 91:8802–8806.
   PubMed Web of Science ®Google Scholar
• Cardone, M. H., N. Roy, H. R. Stennicke, G. S. Salvesen, T. F. Franke, E. Stanbridge, S. Frisch, and J. Reed 1998. Regulation of cell death protease caspase-9 by phosphorylation. Science 282:1318–1321.
   PubMed Web of Science ®Google Scholar
• Chen, D., K. Krasinski, D. Chen, A. Sylvester, J. Chen, P. D. Nisen, and J. Andrés 1997. Down-regulation of cyclin-dependent kinase activity and cyclin A promoter activity in vascular smooth muscle cells by p27 (KIP-1), an inhibitor of neointima formation in the rat carotid artery. J. Clin. Investig. 99:2334–2341.
   PubMed Web of Science ®Google Scholar
• Chomczynski, P., and J. Sacchi 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156–159.
   PubMed Web of Science ®Google Scholar
• Coffer, P. J., J. Jin, and J. Woodgett 1998. Protein kinase B (c-Akt): a multifunctional mediator of phosphatidylinositol 3-kinase activation. Biochem. J. 335:1–13.
   PubMed Web of Science ®Google Scholar
• Datta, K., A. Bellacosa, T. O. Chan, and J. Tsichlis 1996. Akt is a direct target of the phosphatidylinositol 3-kinase. J. Biol. Chem. 271:30835–30839.
   PubMed Web of Science ®Google Scholar
• Datta, S. R., H. Dudek, X. Tao, S. Masters, H. Fu, Y. Gotoh, and J. Greenberg 1997. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231–241.
   PubMed Web of Science ®Google Scholar
• Dominov, J. A., J. J. Dunn, and J. Miller 1998. Bcl-2 expression identifies an early stage of myogenesis and promotes clonal expansion of muscle cells. J. Cell Biol. 142:537–544.
   PubMedGoogle Scholar
• Dudek, H., S. R. Datta, T. F. Franke, M. J. Birnbaum, R. Yao, G. M. Cooper, R. A. Segal, D. R. Kaplan, and J. Greenberg 1997. Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275:661–665.
   PubMed Web of Science ®Google Scholar
• Florini, J. R., E. Z. Ewton, and J. Magri 1991. Hormones, growth factors and myogenic differentiation. Annu. Rev. Physiol. 53:201–216.
   PubMed Web of Science ®Google Scholar
• Florini, J. R., K. A. Magri, D. Z. Ewton, P. L. James, K. Grindstaff, and J. Rotwein 1991. “Spontaneous” differentiation of skeletal myoblasts is dependent upon autocrine secretion of insulin-like growth factor-II. J. Biol. Chem. 266:15917–15923.
   PubMed Web of Science ®Google Scholar
• Franke, T. F., D. R. Kaplan, and J. Cantley 1997. PI3K: downstream AKTion blocks apoptosis. Cell 88:435–437.
   PubMed Web of Science ®Google Scholar
• Franke, T. F., D. R. Kaplan, L. C. Cantley, and J. Toker 1997. Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-biphosphate. Science 275:665–668.
   PubMed Web of Science ®Google Scholar
• Franke, T. F., S.-I. Yang, T. O. Chan, K. Datta, A. Kazlauskas, D. K. Morrison, D. R. Kaplan, and J. Tsichlis 1995. The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phophatidylinositol 3-kinase. Cell 81:727–736.
   PubMed Web of Science ®Google Scholar
• Glücksmann, A. 1951. Cell deaths in normal vertebrate ontogeny. Biol. Rev. Cambridge Philos. Soc. 26:59–86.
   PubMed Web of Science ®Google Scholar
• Guo, K., and J. Walsh 1997. Inhibition of myogenesis by multiple cyclin/cdk complexes: coordinate regulation of myogenesis and cell cycle activity at the level of E2F. J. Biol. Chem. 272:791–797.
   PubMedGoogle Scholar
• Guo, K., J. Wang, V. Andrés, R. C. Smith, and J. Walsh 1995. MyoD-induced expression of p21 inhibits cyclin-dependent kinase activity upon myocyte terminal differentiation. Mol. Cell. Biol. 15:3823–3829.
   PubMed Web of Science ®Google Scholar
• Halevy, O., B. G. Novitch, D. B. Spicer, S. X. Skapek, J. Rhee, G. J. Hannon, D. Beach, and J. Lassar 1995. Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science 267:1018–1021.
   PubMed Web of Science ®Google Scholar
• Hemmings, B. A. 1997. Akt signaling: linking membrane events to life and death decisions. Science 275:628–630.
   PubMed Web of Science ®Google Scholar
• Hiromura, K., J. W. Pippin, M. L. Fero, J. M. Roberts, and J. Shankland 1999. Modulation of apoptosis by the cyclin-dependent kinase inhibitor p27Kip1. J. Clin. Investig. 103:597–604.
   PubMedGoogle Scholar
• Hsieh, J.-K., F. S. G. Chan, D. J. O’Connor, S. Mittnacht, S. Zhong, and J. Lu 1999. RB regulates the stability and the apoptotic function of p53 via MDM2. Mol. Cell 3:181–193.
   PubMed Web of Science ®Google Scholar
• Jiang, B.-H., M. Aoki, J. Z. Zheng, J. Li, and J. Vogt 1999. Myogenic signaling of phosphatidylinositol 3-kinase requires the serine-threonine kinase Akt/protein kinase B. Proc. Natl. Acad. Sci. USA 96:2077–2081.
   PubMed Web of Science ®Google Scholar
• King, K. L., and J. Cidlowski 1998. Cell cycle regulation and apoptosis. Annu. Rev. Physiol. 60:601–617.
   PubMed Web of Science ®Google Scholar
• King, W. G., M. D. Mattaliano, T. O. Chan, P. N. Tsichlis, and J. Brugge 1997. Phosphatidylinositol 3-kinase is required for integrin-stimulated AKT and Raf-1/mitogen-activated protein kinase pathway activation. Mol. Cell. Biol. 17:4406–4418.
   PubMed Web of Science ®Google Scholar
• Kirshenbaum, L. A., M. Abdellatif, S. Chakraborty, and J. Schneider 1996. Human E2F-1 reactivates cell cycle progression in ventricular myocytes and represses cardiac gene transcription. Dev. Biol. 179:402–411.
   PubMed Web of Science ®Google Scholar
• Kitzmann, M., M. Vandromme, V. Schaeffer, G. Carnac, J.-C. Labbé, N. Lamb, and J. Fernandez 1999. cdk1- and cdk2-mediated phosphorylation of MyoD Ser200 in growing C2 myoblasts: role in modulating MyoD half-life and myogenic activity. Mol. Cell. Biol. 19:3167–3176.
   PubMedGoogle Scholar
• Klippel, A., W. M. Kavanaugh, D. Pot, and J. Williams 1997. A specific product of phosphatidylinositol 3-kinase directly activates the protein kinase Akt through its pleckstrin homology domain. Mol. Cell. Biol. 17:338–344.
   PubMed Web of Science ®Google Scholar
• Kohn, A. D., F. Takeuchi, and J. Roth 1996. Akt, a pleckstrin homology domain containing kinase, is activated primarily by phosphorylation. J. Biol. Chem. 271:21920–21926.
   PubMed Web of Science ®Google Scholar
• Kou, K., and J. Rotwein 1993. Transcriptional activation of the insulin-like growth factor-II gene during myoblast differentiation. Mol. Endocrinol. 7:291–302.
   PubMedGoogle Scholar
• Kranenburg, O., A. J. van der Eb, and J. Zantema 1996. Cyclin D1 is an essential mediator of apoptotic neuronal cell death. EMBO J. 15:46–54.
   PubMed Web of Science ®Google Scholar
• Kulik, G., and J. Weber 1998. Akt-dependent and -independent survival signaling pathways utilized by insulin-like growth factor I. Mol. Cell. Biol. 18:6711–6718.
   PubMed Web of Science ®Google Scholar
• Lindon, C., D. Montarras, and J. Pinset 1998. Cell cycle-regulated expression of the muscle determination factor Myf5 in proliferating myoblasts. J. Cell Biol. 140:111–118.
   PubMedGoogle Scholar
• Liu, Y., and J. Kitsis 1996. Induction of DNA synthesis and apoptosis in cardiac myocytes by E1A oncoprotein. J. Cell Biol. 133:325–334.
   PubMedGoogle Scholar
• Missero, C., E. Calautti, R. Eckner, J. Chin, L. H. Tsai, D. M. Livingston, and J. Dotto 1995. Involvement of the cell-cycle inhibitor Cip1/WAF1 and the E1A-associated p300 chain protein in terminal differentiation. Proc. Natl. Acad. Sci. USA 92:5451–5455.
   PubMed Web of Science ®Google Scholar
• Novitch, B. G., G. J. Mulligan, T. Jacks, and J. Lassar 1996. Skeletal muscle cells lacking the retinoblastoma protein display defects in muscle gene expression and accumulate in S and G2 phases of the cell cycle. J. Cell Biol. 135:441–456.
   PubMed Web of Science ®Google Scholar
• Parker, S. B., G. Eichele, P. Zhang, A. Rawls, A. T. Sands, A. Bradley, E. N. Olson, J. W. Harper, and J. Elledge 1995. p53-independent expression of p21cip1 in muscle and other terminally differentiating cells. Science 267:1024–1027.
   PubMed Web of Science ®Google Scholar
• Peso, L., M. Gonzalez-Garcia, C. Page, R. Herrera, and J. Nunez 1997. Interleukin3-induced phosphorylation of BAD through the protein kinase Akt. Science 278:687–689.
   PubMedGoogle Scholar
• Poluha, W., D. K. Poluha, B. Chang, N. E. Crosbie, C. M. Schonhoff, D. L. Kilpatrick, and J. Ross 1996. The cyclin-dependent kinase inhibitor p21WAF1 is required for survival of differentiating neuroblastoma cells. Mol. Cell. Biol. 16:1335–1341.
   PubMed Web of Science ®Google Scholar
• Rosen, K. M., B. M. Wentworth, N. Rosenthal, and J. Villa-Komaroff 1993. Specific, temporally regulated expression of the insulin-like growth factor II gene during muscle cell differentiation. Endocrinology 133:474–481.
   PubMedGoogle Scholar
• Schneider, J. W., W. Gu, L. Zhu, V. Mahdavi, and J. Nadal-Ginard 1994. Reversal of terminal differentiation mediated by p107 in Rb−/− muscle cells. Science 264:1467–1471.
   PubMed Web of Science ®Google Scholar
• Seemüller, E., A. Lupas, D. Stock, J. Löwe, R. Huber, and J. Baumeister 1995. Proteasome from Thermoplasma acidophilum: a threonine protease. Science 268:579–582.
   PubMed Web of Science ®Google Scholar
• Sellers, W. R., B. G. Novitch, S. Miyake, A. Heith, G. A. Otterson, F. J. Kaye, A. B. Lassar, W. G. Kaelin Jr.. 1998. Stable binding to E2F is not required for the retinoblastoma protein to activate transcription, promote differentiation, and suppress tumor cell growth. Genes Dev. 12:95–106.
   PubMed Web of Science ®Google Scholar
• Smith, R. C., D. Branellec, D. H. Gorski, K. Guo, H. Perlman, J.-F. Dedieu, C. Pastore, A. Mahfoudi, P. Denèfle, J. M. Isner, and J. Walsh 1997. p21CIP1-mediated inhibition of cell proliferation by overexpression of the gax homeodomain gene. Genes Dev. 11:1674–1689.
   PubMed Web of Science ®Google Scholar
• Song, A., Q. Wang, M. G. Goeble, and J. Harrington 1998. Phosphorylation of nuclear MyoD is required for its rapid degradation. Mol. Cell. Biol. 18:4994–4999.
   PubMed Web of Science ®Google Scholar
• Stewart, C. E. H., and J. Rotwein 1996. Insulin-like growth factor-II is an autocrine survival factor for differentiating myoblasts. J. Biol. Chem. 271:11330–11338.
   PubMed Web of Science ®Google Scholar
• Stokoe, D., L. R. Stephens, T. Copeland, P. R. J. Gaffney, C. B. Reese, G. F. Painter, A. B. Holmes, F. McCormick, and J. Hawkins 1997. Dual role of phosphatidylinositol-3,4,5-trisphosphate in the activation of protein kinase B. Science 277:567–570.
   PubMed Web of Science ®Google Scholar
• Testa, J. R., and J. Bellacosa 1997. Membrane translocation and activation of the Akt kinase in growth factor-stimulated hematopoietic cells. Leuk. Res. 21:1027–1031.
   PubMed Web of Science ®Google Scholar
• Tollefsen, S. E., J. L. Sadow, and J. Rotwein 1989. Coordinate expression of insulin-like growth factor II and its receptor during muscle differentiation. Proc. Natl. Acad. Sci. USA 86:1543–1547.
   PubMedGoogle Scholar
• Walsh, K., and J. Perlman 1997. Cell cycle exit upon myogenic differentiation. Curr. Opin. Genet. Dev. 7:597–602.
   PubMed Web of Science ®Google Scholar
• Wang, J., K. Guo, K. N. Wills, and J. Walsh 1997. Rb functions to inhibit apoptosis during myocyte differentiation. Cancer Res. 57:351–354.
   PubMed Web of Science ®Google Scholar
• Wang, J., and J. Walsh 1996. Resistance to apoptosis conferred by Cdk inhibitors during myocyte differentiation. Science 273:359–361.
   PubMedGoogle Scholar
• Yoshida, S., A. Fujisawa-Sehara, T. Taki, K. Arai, and J. Nabeshima 1996. Lysophosphatidic acid and bFGF control different modes in proliferating myoblasts. J. Cell Biol. 132:181–193.
   PubMedGoogle Scholar
• Zacksenhaus, E., Z. Jiang, D. Chung, J. D. Marth, R. A. Phillips, and J. Gallie 1996. pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis. Genes Dev. 10:3051–3064.
   PubMed Web of Science ®Google Scholar
• Zhang, P., C. Wong, D. Liu, M. Finegold, J. W. Harper, and J. Elledge 1999. p21CIP1 and p57KIP2 control muscle differentiation at the myogenin step. Genes Dev. 13:213–224.
   PubMed Web of Science ®Google Scholar