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PMID: 1594628 Published · ppublish English Journal Article

Transforming growth factor beta induces myoblast differentiation in the presence of mitogens.

Zentella A, Massagué J

Abstract

Transforming growth factor beta 1 (TGF-beta 1) added to L6E9 rat skeletal myoblasts in mitogen-rich medium induces a rapid decrease in c-myc expression and delays progression through the G1 phase of the cell cycle. This growth inhibitory response is followed by cell commitment to terminal differentiation with elevated expression of myogenin muscle determination genes, induction of muscle-specific proteins, and formation of multinucleated myotubes. These results suggest that TGF-beta 1 may act as a physiological inducer of myogenic differentiation in mitogen-rich environments, and its otherwise reversible growth inhibitory effect may become permanent if coupled to induction of terminal differentiation.

MeSH Terms
Animals Base Sequence Cell Cycle/drug effects Cell Differentiation/drug effects Cells, Cultured Creatine Kinase/metabolism Gene Expression/drug effects Genes, myc In Vitro Techniques Mitogens/pharmacology Molecular Sequence Data Muscles/cytology RNA, Messenger/genetics Rats Transforming Growth Factor beta/pharmacology
Chemicals
Mitogens RNA, Messenger Transforming Growth Factor beta Creatine Kinase
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Zentella A
Cell Biology and Genetics Program, Memorial Sloan-Kettering Cancer Center, New York, NY 10021.
Massagué J
References (51)
51 references, click to expand
  1. Transforming growth factor-beta. A very potent inhibitor of myoblast differentiation, identical to the differentiation inhibitor secreted by Buffalo rat liver cells.
    J Biol Chem. 1986 Dec 15;261(35):16509-13 PMID: 3465726
  2. Developmental changes preceding cell fusion during muscle differentiation in vitro.
    Exp Cell Res. 1971 May;66(1):33-48 PMID: 5104198
  3. Type beta transforming growth factor/growth inhibitor stimulates entry of monolayer cultures of AKR-2B cells into S phase after a prolonged prereplicative interval.
    Proc Natl Acad Sci U S A. 1985 Jun;82(12):4147-51 PMID: 3858871
  4. Density-dependent arrest of DNA replication is accompanied by decreased levels of c-myc mRNA in myogenic but not in differentiation-defective myoblasts.
    J Cell Physiol. 1985 Dec;125(3):465-70 PMID: 4066768
  5. Transforming growth factor beta 1 suppression of c-myc gene transcription: role in inhibition of keratinocyte proliferation.
    Proc Natl Acad Sci U S A. 1990 May;87(10):3758-62 PMID: 2187192
  6. TGF beta in murine morphogenetic processes: the early embryo and cardiogenesis.
    Development. 1990 Apr;108(4):645-56 PMID: 1696875
  7. Early gene responses to transforming growth factor-beta in cells lacking growth-suppressive RB function.
    Mol Cell Biol. 1991 Oct;11(10):4952-8 PMID: 1922028
  8. Cloning of cDNAs for cellular proteins that bind to the retinoblastoma gene product.
    Nature. 1991 Jul 18;352(6332):251-4 PMID: 1857421
  9. Hormones, growth factors, and myogenic differentiation.
    Annu Rev Physiol. 1991;53:201-16 PMID: 2042960
  10. Cytokines in context.
    J Cell Biol. 1991 Jun;113(5):981-6 PMID: 2040651
  11. Epithelial-mesenchymal transformation of embryonic cardiac endothelial cells is inhibited by a modified antisense oligodeoxynucleotide to transforming growth factor beta 3.
    Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1516-20 PMID: 1996351
  12. Negative autoregulation of c-myc gene expression is inactivated in transformed cells.
    EMBO J. 1990 Dec;9(12):3913-22 PMID: 2249657
  13. Translation of c-myc mRNA is required for its post-transcriptional regulation during myogenesis.
    J Biol Chem. 1990 Nov 5;265(31):19015-21 PMID: 2229059
  14. TGF-beta stimulation and inhibition of cell proliferation: new mechanistic insights.
    Cell. 1990 Oct 19;63(2):245-7 PMID: 2208284
  15. Transcriptional regulation of osteopontin production in rat osteosarcoma cells by type beta transforming growth factor.
    J Biol Chem. 1988 Sep 25;263(27):13916-21 PMID: 3166460
  16. Transforming growth factor-beta modulates the expression of osteoblast and chondroblast phenotypes in vitro.
    J Cell Physiol. 1988 Mar;134(3):337-46 PMID: 3162457
  17. Type beta transforming growth factor controls the adipogenic differentiation of 3T3 fibroblasts.
    Proc Natl Acad Sci U S A. 1985 Dec;82(24):8530-4 PMID: 3001708
  18. Various rat adult tissues express only one major mRNA species from the glyceraldehyde-3-phosphate-dehydrogenase multigenic family.
    Nucleic Acids Res. 1985 Mar 11;13(5):1431-42 PMID: 2987824
  19. 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. 1989 May;3(5):628-40 PMID: 2473006
  20. Fibroblast growth factor and transforming growth factor beta repress transcription of the myogenic regulatory gene MyoD1.
    Mol Cell Biol. 1989 Aug;9(8):3576-9 PMID: 2797000
  21. Type beta transforming growth factor is an inhibitor of myogenic differentiation.
    Proc Natl Acad Sci U S A. 1986 Nov;83(21):8206-10 PMID: 3022285
  22. Transforming growth factor beta-1 in acute myocardial infarction in rats.
    Growth Factors. 1988;1(1):91-9 PMID: 3078566
  23. c-myc antisense transcripts accelerate differentiation and inhibit G1 progression in murine erythroleukemia cells.
    Mol Cell Biol. 1988 Sep;8(9):3683-95 PMID: 2464742
  24. c-myc oncogene expression inhibits the initiation of myogenic differentiation.
    Exp Cell Res. 1987 Sep;172(1):212-7 PMID: 2443373
  25. The T/E1A-binding domain of the retinoblastoma product can interact selectively with a sequence-specific DNA-binding protein.
    Cell. 1991 Jun 14;65(6):1073-82 PMID: 1828394
  26. Identification of cellular proteins that can interact specifically with the T/E1A-binding region of the retinoblastoma gene product.
    Cell. 1991 Feb 8;64(3):521-32 PMID: 1825028
  27. The transforming growth factor-beta family.
    Annu Rev Cell Biol. 1990;6:597-641 PMID: 2177343
  28. MyoD family: a paradigm for development?
    Genes Dev. 1990 Sep;4(9):1454-61 PMID: 2253873
  29. Cardiac fibroblasts are predisposed to convert into myocyte phenotype: specific effect of transforming growth factor beta.
    Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):795-9 PMID: 1704132
  30. Functional activity of myogenic HLH proteins requires hetero-oligomerization with E12/E47-like proteins in vivo.
    Cell. 1991 Jul 26;66(2):305-15 PMID: 1649701
  31. Transforming growth factor beta represses the actions of myogenin through a mechanism independent of DNA binding.
    Proc Natl Acad Sci U S A. 1991 May 1;88(9):3822-6 PMID: 1850837
  32. MyoD and the regulation of myogenesis by helix-loop-helix proteins.
    J Clin Invest. 1991 Apr;87(4):1133-8 PMID: 1849142
  33. c-myc inhibition of MyoD and myogenin-initiated myogenic differentiation.
    Mol Cell Biol. 1991 May;11(5):2842-51 PMID: 1850105
  34. The retinoblastoma protein copurifies with E2F-I, an E1A-regulated inhibitor of the transcription factor E2F.
    Cell. 1991 Jun 14;65(6):1063-72 PMID: 1828393
  35. The E2F transcription factor is a cellular target for the RB protein.
    Cell. 1991 Jun 14;65(6):1053-61 PMID: 1828392
  36. Expression of the fibroblast growth factor-5 gene in the mouse embryo.
    Development. 1991 Jun;112(2):397-406 PMID: 1794310
  37. Immunohistochemical localization of TGF beta 1, TGF beta 2, and TGF beta 3 in the mouse embryo: expression patterns suggest multiple roles during embryonic development.
    J Cell Biol. 1991 Nov;115(4):1091-105 PMID: 1955457
  38. MyoD is a sequence-specific DNA binding protein requiring a region of myc homology to bind to the muscle creatine kinase enhancer.
    Cell. 1989 Sep 8;58(5):823-31 PMID: 2550138
  39. Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD.
    Cell. 1989 Feb 24;56(4):607-17 PMID: 2537150
  40. Identification of a myocyte nuclear factor that binds to the muscle-specific enhancer of the mouse muscle creatine kinase gene.
    Mol Cell Biol. 1989 Jun;9(6):2627-40 PMID: 2761542
  41. Basic fibroblast growth factor in the chick embryo: immunolocalization to striated muscle cells and their precursors.
    J Cell Biol. 1989 Jun;108(6):2459-66 PMID: 2738095
  42. Growth inhibitor from BSC-1 cells closely related to platelet type beta transforming growth factor.
    Science. 1984 Nov 9;226(4675):705-7 PMID: 6093254
  43. Role of transforming growth factor-beta in the development of the mouse embryo.
    J Cell Biol. 1987 Dec;105(6 Pt 2):2861-76 PMID: 3320058
  44. Growth inhibition by TGF-beta linked to suppression of retinoblastoma protein phosphorylation.
    Cell. 1990 Jul 13;62(1):175-85 PMID: 2163767
  45. Cell adhesion to collagen and decreased myogenic gene expression implicated in the control of myogenesis by transforming growth factor beta.
    J Biol Chem. 1990 Jun 25;265(18):10181-4 PMID: 2162338
  46. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins.
    Cell. 1990 Apr 6;61(1):49-59 PMID: 2156629
  47. Effect of transforming growth factor beta on proliferation of L6 and embryonic porcine myogenic cells.
    J Cell Physiol. 1990 Jun;143(3):524-8 PMID: 2358471
  48. Functional role for c-myc in mitogenic response to platelet-derived growth factor.
    Nature. 1984 Aug 23-29;310(5979):655-60 PMID: 6088986
  49. Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro.
    J Cell Biol. 1982 Dec;95(3):763-70 PMID: 6185504
  50. Commitment, fusion and biochemical differentiation of a myogenic cell line in the absence of DNA synthesis.
    Cell. 1978 Nov;15(3):855-64 PMID: 728992
  51. Growth factor control of skeletal muscle differentiation: commitment to terminal differentiation occurs in G1 phase and is repressed by fibroblast growth factor.
    J Cell Biol. 1987 Aug;105(2):949-56 PMID: 3624313
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1992-06-01
Pages
5176-80
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC49252
Subset
IM
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