Maturation of the myogenic program is induced by postmitotic expression of insulin-like growth factor I

Molecular and Cellular Biology

Volumn 19, Issue 4, 1999, Pages 3115-3124

  Musarò, Antonio ^a   Rosenthal, Nadia ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CREATINE KINASE; MUSCLE ENZYME; MYOGENIN; MYOSIN HEAVY CHAIN; MYOSIN LIGHT CHAIN; PHOSPHATIDYLINOSITOL 3 KINASE; SOMATOMEDIN BINDING PROTEIN 5; SOMATOMEDIN C;

ANIMAL CELL; ARTICLE; CELL HYPERPLASIA; CELL PROLIFERATION; CONTROLLED STUDY; MITOSIS; MUSCLE DEVELOPMENT; MUSCLE REGENERATION; MYOBLAST; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RAT; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0032949353     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.4.3115     Document Type: Article

References (50)

1. Azzarello, G., S. Sartore, L. Saggin, L. Gorza, E. D'Andrea, L., Chieco-Bianchi, and S. Schiaffino. 1987. Myosin isoform expression in rat rhabdomyosarcoma induced by moloney murine sarcoma virus. J. Cancer Res. Clin. Oncol. 113:417-429.
2. Barbieri, G., L. De Angelis, S. Feo, G. Cossu, and A. Giallongo. 1990. Differential expression of muscle-specific enolase in embryonic and fetal myogenic cells during mouse development. Differentiation 45:179-184.
3. Barton-Davis, E. R., D. I. Shoturma, A. Musarò, N. Rosenthal, and L. H. Sweeney. 1998. Viral mediated expression of insulin-like growth factor I blocks the aging related loss of skeletal muscle function. Proc. Natl. Acad. Sci. USA 91:15603-15607.
4. Belkin, A. M., N. I. Zhidkova, F. Balzac, F. Altruda, D. Tomatis, A. Maier, G. Tarone, V. E. Koteliansky, and K. Burridge. 1996. β1D integrin displaces the β1A isoform in striated muscle: localization at junctional structures and signaling potential in nonmuscle cells. J. Cell Biol. 132:211-226.
5. Benezra, R., R. L. Davis, D. Lockshon, D. L. Turner, and H. Weintraub. 1990. The protein Id: a negative regulator of helix-loop-helix DNA binding protein. Cell 61:49-59.
6. Braun, T., E. Bober, G. Buschhausen-Denker, S. Kohtz, K. H. Grzeschik, and H. H. Arnold. 1989. Differential expression of myogenic determination genes in muscle cells: possible autoactivation by the Myf gene products. EMBO J. 8:3617-3625. (Erratum 13:358.)
7. Braun, T., G. Buschhausen-Denker, E. Bober, and H. H. Arnold. 1989. A novel human muscle factor related to but distinct from MyoD1 induces myogenic conversation in 10T1/2 fibroblasts. EMBO J. 8:701-708.
8. Buonanno, A., and N. Rosenthal. 1996. Molecular control of muscle diversity and plasticity. Dev. Gen. 19:95-107.
9. Chamberlain, J. F., J. B. Jaynes, and S. D. Hauschka. 1985. Regulation of creatine kinase induction in differentiating mouse myoblasts. Mol. Cell. Biol. 5:487-492.
10. Coleman, M. E., F. DeMayo, K. C. Yin, H. M. Lee, R. Geske, C. Montgomery, and R. J. Schwartz. 1995. Myogenic vector expression of insulin-like growth factor I stimulates muscle cell differentiation and myofiber hypertrophy in transgenic mice. J. Biol. Chem. 270:12109-12116.
11. Coolican, S. A., D. S. Samuel, D. Z. Ewton, F. J. McWade, and J. R. Florini. 1997. The mitogenic and myogenic actions of insulin-like growth factors utilize distinct signaling pathways. J. Biol. Chem. 272:6653-6662.
12. Cossu, G., and M. Molinaro. 1987. Cell heterogeneity in the myogenic lineage. Curr. Top. Dev. Biol. 23:185-208.
13. Csejesi, P., B. Lilly, C. Hinkley, M. Perry, and E. N. Olson. 1994. Homeodomain protein Mhox and MADS protein myocyte enhancer-binding factor-2 converge on a common element in the muscle creatine kinase enhancer. J. Biol. Chem. 269:16740-16745.
14. Donoghue, M., H. Ernst, B. Wentworth, B. Nadal-Ginard, and N. Rosenthal. 1988. A muscle-specific enhancer is located at the 3′ end of the myosin light-chain 1/3 gene locus. Genes Dev. 2:1779-1790.
15. Engert, J. C., E. B. Berglund, and N. Rosenthal. 1996. Proliferation precedes differentiation in IGF-I-stimulated myogenesis. J. Cell Biol. 135:431-440.
16. Ewton, D. Z., and J. R. Florini. 1995. Insulin-like growth factor binding proteins -4, -5, and -6 may play specialized roles during L6 myoblast proliferation and differentiation. J. Endocrinol. 144:539-553.
17. Feinber, A. P., and B. Volgelstein. 1983. A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132:6-13.
18. Ferrari, S., S. Molinari, R. Melchionna, M. G. Cusella-De Angelis, R. Battini, L. De Angelis, R. Kelly, and G. Cossu. 1997. Absence of MEF2 binding to the A/T-rich element in the muscle creatine kinase (MCK) enhancer correlates with lack of early expression of the MCK gene in embryonic mammalian muscle. Cell Growth Differ. 8:23-34.
19. Florini, J. R., D. Z. Ewton, S. L. Falen, and J. J. Van Wyk. 1986. Biphasic concentration dependency of the stimulation of myoblast differentiation by somatomedins. Am. J. Physiol. 250:771-778.
20. Florini, J. R., and D. Z. Ewton. 1990. Highly specific inhibition of IGF-I stimulated differentiation by an antisense oligodeoxyribonucleotide to myogenin mRNA. No effects on other actions of IGF-T. J. Biol. Chem. 265: 13435-13437.
21. Florini, J. R., D. Z. Ewton, and K. A. Magri. 1991. Hormones, growth factors, and myogenic differentiation. Annu. Rev. Physiol. 53:201-216.
22. Florini, J. R., D. Z. Ewton, K. A. Magri, and F. J. Mangiacapra. 1994. IGFs and muscle differentiation, p. 319. In M. K. Raizada and D. LeRoith (ed.), Current directions in insulin-like growth factor research. Plenum Press, New York, N.Y.
23. Florini, J. R., D. Z. Ewton, and S. A. Coolican. 1996. Growth hormone and the insulin-like growth factor system in myogenesis. Endocr. Rev. 17:481-516.
24. Garfinkel, L. I., M. Periasamy, and B. Nadal-Ginard. 1982. Cloning and characterization of cDNA sequences corresponding to myosin light chains 1, 2, and 3, troponin-C, troponin-T, alpha-tropomyosin, and alpha-actin. J. Biol. Chem. 257:11078-11086.
25. Gosset, L. A., D. J. Kelvin, E. A. Stenberg, and E. N. Olson. 1989. A new myocyte-specific enhancer-binding factor that recognizes a conserved element associated with multiple muscle-specific genes. Mol. Cell. Biol. 9:5022-5033.
26. Jones, J. I., and D. R. Clemmons. 1995. Insulin-like growth factors and their binding proteins: biological actions. Endocr. Rev. 16:3-34.
27. Kaliman, P., F. Vin̄als, X. Tester, M. Palacín, and A. Zorzano. 1996. Phosphatidylinositol 3-kinase inhibitors block differentiation of skeletal muscle cells. J. Biol. Chem. 271:19146-19151.
28. Keller, A., M. O. Ott, N. Lamande, M. Lucas, F. Gros, M. Buckingham, and M. Lazar. 1992. Activation of the gene encoding the glycolytic enzyme beta-enolase during early myogenesis precedes an increased expression during fetal muscle development. Mech. Dev. 38:41-54.
29. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
30. Liu, J.-L., J. Baker, A. S., Perkins, E. J. Robertson, and A. Efstratiadis. 1993. Mice carrying null mutations of the genes encoding insulin-like growth factors 1 (IGF-I) and type 1 IGF receptor (IGF1r). Cell 75:59-72.
31. Martin, J. F., J. J. Schwarz, and E. N. Olson. 1993. Myocyte enhancer factor (MEF) 2C: a tissue-restricted member of the MEF-2 family of transcription factors. Proc. Natl. Acad. Sci. USA 90:5282-5286.
32. McCusker, R. H., and D. R. Clemmons. 1988. Insulin-like growth factor binding protein secretion by muscle cells: effects of cellular differentiation and proliferation. J. Cell. Physiol. 137:505-512.
33. McCusker, R. H., C. Camacho-Hubner, and D. R. Clemmons. 1989. Identification of the types of insulin-like growth factor-binding proteins that are secreted by muscle cells in vitro. J. Biol. Chem. 264:7795-7800.
34. a. Musarò, A., and N. Rosenthal. Unpublished data.
35. Nadal-Ginard, B. 1978. Commitment, fusion and biochemical differentiation of a myogenic cell line in the absence of DNA synthesis. Cell 15:855-864.
36. Pajak, L., M. Mariappan, and D. F. Wieczorek. 1991. Reprogramming of myosin light chain 1/3 expression in muscle heterokaryons. Dev. Biol. 145: 28-39.
37. Passantino, R., V. Antona, G. Barbieri, P. Rubino, R. Melchionna, G. Cossu, S. Feo, and A. Giallongo. 1998. Negative regulation of β enolase gene transcription in embryonic muscle is dependent upon a zinc finger factor that binds to the G-rich box within the muscle-specific enhancer. J. Biol. Chem. 273:484-494.
38. Powell-Braxton, L., P. Hollingshead, C. Warburton, M. Dowd, S. Pitts-Meek, D. Dalton, N. Gillet, and T. A. Stewart. 1993. IGF-I is required for normal embryonic growth in mice. Genes Dev. 7:2609-2617.
39. Quinn, L. S., B. Steinmetz, A. Maas, L. Ong, and M. Kaleko. 1994. Type-1 insulin-like growth factor receptor overexpression produces dual effects on myoblast proliferation and differentiation. J. Cell. Physiol. 159:387-398.
40. Rhodes, S. J., and S. F. Konieczny. 1989. Identification of MRF4: a new member of the muscle regulatory factor gene family. Genes Dev. 3:2050-2061.
41. Rosen, K. M., B. M. Wentworth, N. Rosenthal, and L. Villa-Komaroff. 1993. Specific, temporally regulated expression of the insulin-like growth factor II gene during muscle cell differentiation. Endocrinology 133:474-481.
42. Rosenthal, N., E. B. Berglund, B. M. Wentworth, M. Donoghue, B. Winter, E. Bober, T. Braun, and H. H. Arnold. 1990. A highly conserved enhancer downstream of the human MLC1/3 locus is a target for multiple myogenic determination factors. Nucleic Acids Res. 18:6239-6246.
43. Rosenthal, S. M., and Z.-Q. Cheng. 1995. Opposing early and late effects of insulin-like growth factor I on differentiation and the cell cycle regulatory retinoblastoma protein in skeletal myoblasts. Proc. Natl. Acad. Sci. USA 92:10307-10311.
44. Stockdale, F. E., and J. B. Miller. 1987. The cellular basis of myosin heavy chain heterogeneity during development of avian skeletal muscle. Dev. Biol. 123:1-9.
45. Stewart, C. E., and P. Rotwein. 1996. Growth, differentiation, and survival: multiple physiological functions for insulin-like growth factors. Physiol. Rev. 76:1005-1026.
46. a. Sweeney, L. Personal communication.
47. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of protein from polyacrylamide gels to nitrocellulose sheets. Proc. Natl. Acad. Sci. USA 76:4350-4354.
48. Vandenburg, H. H., P. Karlish, J. Shansky, and R. Feldstein. 1991. Insulin and IGF-I induce pronounced hypertrophy of skeletal myofibers in tissue culture. Am. J. Physiol. 260:C475-C484.
49. Weintraub, H. 1993. The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell 75:1241-1244.
50. Yaffe, D. 1968. Retention of differentiation potentialities during prolonged cultivation of myogenic cells. Proc. Natl. Acad. Sci. USA 61:477-483.