The transition from proliferation to differentiation is delayed in satellite cells from mice lacking MyoD

Developmental Biology

Volumn 210, Issue 2, 1999, Pages 440-455

  Yablonka Reuveni, Zipora ^a   Rudnicki, Michael A ^b   Rivera, Anthony J ^a   Primig, Michael ^c   Anderson, Judy E ^a   Natanson, Priscilla ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b MCMASTER UNIVERSITY   (Canada)

^c INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS ANTIGEN; CYCLIN D3; MITOGEN ACTIVATED PROTEIN KINASE; MYOD PROTEIN; MYOGENIC FACTOR; MYOGENIN; REGULATOR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM; FEMALE; MALE; MUSCLE DEVELOPMENT; MUSCLE FIBER CULTURE; MUSCLE REGENERATION; MYOTUBE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT; SATELLITE CELL;

EID: 0033564139     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1999.9284     Document Type: Article

References (63)

1. Allen R. E., Shannon S. M., Taylor R. G., Kendall T. L., Rice G. M. Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro. J. Cell. Physiol. 165:1995;307-312.
2. Anderson J. E. Studies of the dynamics of skeletal muscle regeneration: The mouse came back! Biochem. Cell Biol. 76:1998;13-26.
3. Anderson J. E., McIntosh L. M., Moor A. N., Yablonka-Reuveni Z. Levels of MyoD protein expression following injury of mdx and normal limb muscle are modified by thyroid hormone. J. Histochem. Cytochem. 46:1997;59-67.
4. Aurade F., Pfarr C. M., Lindon C., Garcia A., Primig M., Montarras D., Pinset C. The glucocorticoid receptor and AP-1 are involved in a positive regulation of the muscle regulatory gene myf5 in cultured myoblasts. J. Cell Sci. 110:1997;2771-2779.
5. Bischoff R. Proliferation of muscle satellite cells in intact myofibers in culture. Dev. Biol. 115:1986;129-139.
6. Bischoff R. Analysis of muscle regeneration using single myofibers in culture. Med. Sci. Sports Exerc. 21:1989;S164-S172.
7. Bischoff R. Interaction between satellite cells and skeletal muscle fibers. Development. 109:1990a;943-952.
8. Bischoff R. Cell cycle commitment of rat muscle satellite cells. J. Cell Biol. 111:1990b;201-207.
9. Braun T., Bober E., Rudnicki M. A., Jaenisch R., Arnold H. H. MyoD expression marks the onset of skeletal myogenesis in Myf-5 mutant mice. Development. 120:1994;3083-3092.
10. Braun T., Rudnicki M. A., Arnold H. H., Jaenisch R. Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell. 71:1992;369-382.
11. Buckingham M., Kelly R., Tajbakhsh S., Zammit P. The formation and maturation of skeletal muscle in the mouse: The myosin MLC1F/3F gene as a molecular model. Acta Physiol. Scand. 163:1998;S3-S5.
12. Carnac G., Primig M., Kitzmann M., Chafey P., Tuil D., Lamb N., Fernandez A. RhoA GTPase and serum response factor control selectively the expression of MyoD without affecting Myf5 in mouse myoblasts. Mol. Biol. Cell. 9:1998;1891-1902.
13. Cornelison D. D. W., Wold B. J. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev. Biol. 191:1997;270-283.
14. Danto S. I., Fischman D. A. Immunohistochemical analysis of intermediate filaments in embryonic heart cells with monoclonal antibodies to desmin. J. Cell Biol. 98:1984;2179-2191.
15. Dias P., Parham D. M., Shapiro D. N., Tapscott S. J., Houghton P. J. Monoclonal antibodies to the myogenic regulatory protein MyoD1: Epitope mapping and diagnostic utility. Cancer Res. 52:1992;6431-6439.
16. Füchtbauer E.-M., Westphal H. MyoD and myogenin are coexpressed in regenerating skeletal muscle of the mouse. Dev. Dyn. 193:1992;34-39.
17. Gause K. C., Homma M. K., Licciardi K. A., Seger R., Ahn N. G., Peterson M. J., Krebs E. G., Meier K. E. Effects of phorbol ester on mitogen-activated protein kinase kinase activity in wild-type and phorbol ester-resistant EL4 thymoma cells. J. Biol. Chem. 268:1993;16124-16129.
18. Grounds M. D., Yablonka-Reuveni Z. Molecular and cellular biology of muscle regeneration. Partridge T. Molecular and Cell Biology of Muscular Dystrophy. 1993;210-256 Chapman & Hall, London.
19. Grounds M. D., Garrett K. L., Lai M. C., Wright W. E., Beilharz M. W. Identification of skeletal muscle precursor cells in vivo by use of MyoD1 and myogenin probes. Cell Tissue Res. 267:1992;99-104.
20. Halevy O., Novitch B. G., Spicer D. B., Skapek S. X., Rhee J., Hannon G. J., Beach D., Lassar A. B. Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science. 267:1995;1018-1021.
21. Hinterberger T. J., Sassoon D. A., Rhodes S. J., Konieczny S. F. Expression of the muscle regulatory MRF4 during somite and skeletal myofiber development. Dev. Biol. 147:1991;144-156.
22. Kablar B., Krastel K., Ying C., Asakura A., Tapscott S. J., Rudnicki M. A. MyoD and Myf-5 differentially regulate the development of limb versus trunk skeletal muscle. Development. 124:1997;4729-4738.
23. Kami K., Noguchi K., Senba E. Localization of myogenin, c-fos, c-jun, and muscle-specific gene mRNA in regenerating rat skeletal muscle. Cell Tissue Res. 280:1995;11-19.
24. Kaufman S. J., Foster R. F. Replicating myoblasts express a muscle-specific phenotype. Proc. Natl. Acad. Sci. USA. 185:1988;9606-9610.
25. Kimes B. W., Brandt B. L. Properties of a clonal muscle cell line from rat heart. Exp. Cell Res. 98:1976;367-381.
26. Kiess M., Gill R. M., Hamel P. A. Expression and activity of the retinoblastoma protein (pRB)-family proteins, p107 and p130, during L6 myoblast differentiation. Cell Growth Differ. 6:1995a;1287-1298.
27. Kiess M., Gill R. M., Hamel P. A. Expression of the positive regulator of cell cycle progression, cyclin D3, is induced during differentiation of myoblasts into quiescent myotubes. Oncogene. 10:1995b;159-166.
28. Kitzmann M., Carnac G., Vandromme M., Primig M., Lamb N. J. C., Ferandez A. The muscle regulatory factors MyoD and Myf-5 undergo distinct cell cycle-specific expression in muscle cells. J. Cell Biol. 142:1998;1447-1459.
29. Koishi K., Zhang M., McLennan I. S., Harris A. J. MyoD protein accumulates in satellite cells and is neurally regulated in regenerating myotubes and skeletal muscle fibers. Dev. Dyn. 202:1995;244-254.
30. Lewis T. S., Shapiro P. S., Ahn N. G. Signal transduction through MAP kinases cascades. Adv. Cancer Res. 74:1998;49-139.
31. Lindon C., Montarras D., Pinset C. Cell cycle-regulated expression of the muscle determination factor Myf5 in proliferating myoblasts. J. Cell Biol. 140:1998;111-118.
32. Maley M. A. L., Fan Y., Beilharz M. W., Grounds M. D. Intrinsic differences in MyoD and myogenin expression between primary cultures of SLJ/J and BALB/C skeletal muscle. Exp. Cell Res. 211:1994;99-107.
33. Mauro A. Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 9:1961;493-495.
34. McIntosh L. M., Garrett K. L., Megeney L., Rudnicki M. A., Anderson J. E. Regeneration and myogenic cell proliferation correlate with taurine levels in dystrophin- and MyoD-deficient muscles. Anat. Rec. 252:1998;311-324.
35. Megeney L. A., Kablar B., Garrett K., Anderson J. E., Rudnicki M. A. MyoD is required for myogenic stem cell function in adult skeletal muscle. Genes Dev. 10:1996;1173-1183.
36. Megeney L. A., Rudnicki M. A. Determination versus differentiation and the MyoD family of transcription factors. Biochem. Cell Biol. 73:1995;723-732.
37. Molkentin J. D., Olson E. N. Defining the regulatory networks for muscle development. Curr. Opin. Genet. Dev. 6:1996;445-453.
38. Moss F. P., Leblond C. P. Satellite cells as a source of nuclei in muscles of growing rats. Anat. Rec. 170:1971;421-436.
39. Olson E. N. Interplay between proliferation and differentiation within the myogenic lineage. Dev. Biol. 154:1992;216-272.
40. Olson E. N. Signal transduction pathways that regulate skeletal muscle gene expression. Mol. Endocrinol. 7:1993;1369-1378.
41. Rao S. S., Kohtz D. S. Positive and negative regulation of D-type cyclin expression in skeletal myoblasts by basic fibroblast growth factor and transforming growth factor beta. A role for cyclin D1 in control of myoblast differentiation. J. Biol. Chem. 270:1995;4093-4100.
42. Robinson M. J., Cobb M. H. Mitogen-activated protein kinase pathways. Curr. Opin. Cell Biol. 9:1997;180-186.
43. Sabourin L. A., Girgis-Gabardo A., Seale P., Asakura A., Rudnicki M. A. Reduced differentiation potential of primary MyoD-/- myogenic cells derived from adult skeletal muscle. J. Cell Biol. 144:1999;631-643.
44. Schultz E., Gibson M. C., Champion T. Satellite cells are mitotically quiescent in mature mouse muscle: An EM and radioautographic study. J. Exp. Zool. 206:1978;451-456.
45. Schultz E., McCormick K. M. Skeletal muscle satellite cells. Rev. Physiol. Biochem. Pharmacol. 123:1994;213-257.
46. Seger R., Seger D., Reszka A. A., Munar E. S., Eldar-Finkelman H., Dobrowolska G., Jensen A. M., Campbell J. S., Fischer E. H., Krebs E. G. Overexpression of mitogen-activated protein kinase kinase (MAPKK) and its mutants in NIH 3T3 cells. Evidence that MAPKK involvement in cellular proliferation is regulated by phosphorylation of serine residues in its kinase subdomains VII and VIII. J. Biol. Chem. 269:1994;25699-25709.
47. Smith C. K. II, Janney M. J., Allen R. E. Temporal expression of myogenic regulatory genes during activation, proliferation, and differentiation of rat skeletal muscle satellite cells. J. Cell. Physiol. 159:1994;379-385.
48. Smith T. H., Block N. E., Rhodes S. J., Konieczny S. F., Miller J. B. A unique pattern of expression of the four muscle regulatory factor proteins distinguishes somitic from embryonic, fetal and newborn mouse myogenic cells. Development. 117:1993;1125-1133.
49. Snow M. H. Satellite cell response in rat soleus muscle undergoing hypertrophy due to surgical ablation of synergists. Anat. Rec. 227:1990;437-446.
50. Tajbakhsh S., Borello U., Vivarelli E., Kelly R., Duprez D., Buckingham M., Cossu G. Differential activation of Myf5 and MyoD by different Wnts in explants of mouse paraxial mesoderm and the later activation of myogenesis in the absence of Myf5. Development. 125:1998;4155-4162.
51. Weintraub H. The MyoD family and myogenesis: Redundancy, networks, and thresholds. Cell. 75:1993;1241-1244.
52. Winchester P. K., Davis M. E., Alway S. E., Gonyea W. J. Satellite cell activation in the stretch-enlarged anterior latissimus dorsi muscle of the adult quail. Am J. Physiol. 260:1991;C206-C212.
53. Wright W. E., Sassoon D. A., Lin V. K. Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell. 56:1989;607-617.
54. Yablonka-Reuveni Z. Development and postnatal regulation of adult myoblasts. Microsc. Res. Tech. 30:1995;366-380.
55. Yablonka-Reuveni Z., Nameroff M. Temporal differences in desmin expression between myoblasts from embryonic and adult chicken skeletal muscle. Differentiation. 45:1990;21-28.
56. Yablonka-Reuveni Z., Rivera A. J. Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Dev. Biol. 164:1994;588-603.
57. Yablonka-Reuveni Z., Rivera A. J. Influence of PDGF-BB on proliferation and transition through the MyoD-myogenin-MEF2A expression program during myogenesis in mouse C2 myoblasts. Growth Factors. 15:1997a;1-25.
58. Yablonka-Reuveni Z., Rivera A. J. Proliferative dynamics and the role of FGF2 during myogenesis of rat satellite cells on isolated fibers. Basic Appl. Myol. 7:1997b;189-202.
59. Yablonka-Reuveni Z., Seger R., Rivera A. J. Fibroblast growth factor promotes recruitment of skeletal muscle satellite cells in young and old rats. J. Histochem. Cytochem. 47:1999;23-42.
60. Yaffe D. Retention of differentiation potentialities during prolonged cultivation of myogenic cells. Proc. Natl. Acad. Sci. USA. 61:1968;477-483.
61. Yaffe D., Saxel O. A myogenic cell line with altered serum requirements for differentiation. Differentiation. 7:1977a;159-166.
62. Yaffe D., Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature. 270:1977b;725-727.
63. Yun K., Wold B. Skeletal muscle determination and differentiation: Story of a core regulatory network and its context. Curr. Opin. Cell Biol. 8:1996;877-889.