Transforming Growth Factor Beta Represses the Actions of Myogenin Through a Mechanism Independent of DNA Binding

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1991 May 1

PMID 1850837

Citations 48

Authors

T J Brennan

D G Edmondson

L Li

E N Olson

Affiliations

Soon will be listed here.

Abstract

Myogenin belongs to a family of regulatory factors that can activate myogenesis when transfected into nonmyogenic cells. A conserved DNA sequence, known as an E box, serves as the target for binding and trans-activation by myogenin. Using 10T1/2 fibroblasts that constitutively express a transfected myogenin cDNA, we show that myogenin accumulates in the nucleus but is unable to initiate myogenesis when cells are maintained with transforming growth factor beta (TGF-beta) or high serum. Although the final effect of TGF-beta and high serum--inhibition of myogenesis--was the same, their effects on the DNA-binding properties of myogenin in vitro differed. TGF-beta did not affect the ability of myogenin to bind DNA, whereas serum diminished the in vitro DNA-binding activity of myogenin. The helix-loop-helix (HLH) protein Id, postulated to inhibit DNA binding of other HLH proteins, was induced by high serum but not by TGF-beta. The presence of Id correlated with the failure of myogenin to bind the muscle creatine kinase enhancer in vitro. These findings suggest that serum can inhibit myogenesis by attenuating the DNA-binding activity of myogenin, possibly as a consequence of Id protein expression, whereas TGF-beta acts through a mechanism distal to DNA sequence recognition by myogenin and independent of Id.

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References

Olson E, STERNBERG E, Hu J, Spizz G, Wilcox C . Regulation of myogenic differentiation by type beta transforming growth factor. J Cell Biol. 1986; 103(5):1799-805. PMC: 2114366. DOI: 10.1083/jcb.103.5.1799. View

Schubert D, Harris A, Devine C, Heinemann S . Characterization of a unique muscle cell line. J Cell Biol. 1974; 61(2):398-413. PMC: 2109296. DOI: 10.1083/jcb.61.2.398. View

Davis R, Weintraub H, Lassar A . Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell. 1987; 51(6):987-1000. DOI: 10.1016/0092-8674(87)90585-x. View

Clegg C, Linkhart T, Olwin B, Hauschka S . 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; 105(2):949-56. PMC: 2114757. DOI: 10.1083/jcb.105.2.949. View

Li L, Hu J, Olson E . Different members of the jun proto-oncogene family exhibit distinct patterns of expression in response to type beta transforming growth factor. J Biol Chem. 1990; 265(3):1556-62. View

Piette J, Bessereau J, Huchet M, Changeux J . Two adjacent MyoD1-binding sites regulate expression of the acetylcholine receptor alpha-subunit gene. Nature. 1990; 345(6273):353-5. DOI: 10.1038/345353a0. View

Miner J, Wold B . Herculin, a fourth member of the MyoD family of myogenic regulatory genes. Proc Natl Acad Sci U S A. 1990; 87(3):1089-93. PMC: 53416. DOI: 10.1073/pnas.87.3.1089. View

Roman D, Billadello J, Gordon J, Grace A, Sobel B, Strauss A . Complete nucleotide sequence of dog heart creatine kinase mRNA: conservation of amino acid sequence within and among species. Proc Natl Acad Sci U S A. 1985; 82(24):8394-8. PMC: 390922. DOI: 10.1073/pnas.82.24.8394. View

Braun T, Winter B, Bober E, Arnold H . Transcriptional activation domain of the muscle-specific gene-regulatory protein myf5. Nature. 1990; 346(6285):663-5. DOI: 10.1038/346663a0. View

10.

Scales J, Olson E, Perry M . Two distinct Xenopus genes with homology to MyoD1 are expressed before somite formation in early embryogenesis. Mol Cell Biol. 1990; 10(4):1516-24. PMC: 362255. DOI: 10.1128/mcb.10.4.1516-1524.1990. View

11.

Braun T, Bober E, Winter B, Rosenthal N, Arnold H . Myf-6, a new member of the human gene family of myogenic determination factors: evidence for a gene cluster on chromosome 12. EMBO J. 1990; 9(3):821-31. PMC: 551742. DOI: 10.1002/j.1460-2075.1990.tb08179.x. View

12.

Yutzey K, Rhodes S, Konieczny S . Differential trans activation associated with the muscle regulatory factors MyoD1, myogenin, and MRF4. Mol Cell Biol. 1990; 10(8):3934-44. PMC: 360904. DOI: 10.1128/mcb.10.8.3934-3944.1990. View

13.

Brennan T, Edmondson D, Olson E . Aberrant regulation of MyoD1 contributes to the partially defective myogenic phenotype of BC3H1 cells. J Cell Biol. 1990; 110(4):929-37. PMC: 2116110. DOI: 10.1083/jcb.110.4.929. View

14.

Heino J, Massague J . Cell adhesion to collagen and decreased myogenic gene expression implicated in the control of myogenesis by transforming growth factor beta. J Biol Chem. 1990; 265(18):10181-4. View

15.

Brennan T, Olson E . Myogenin resides in the nucleus and acquires high affinity for a conserved enhancer element on heterodimerization. Genes Dev. 1990; 4(4):582-95. DOI: 10.1101/gad.4.4.582. View

16.

Benezra R, Davis R, Lockshon D, Turner D, Weintraub H . The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell. 1990; 61(1):49-59. DOI: 10.1016/0092-8674(90)90214-y. View

17.

Davis R, Cheng P, Lassar A, Weintraub H . The MyoD DNA binding domain contains a recognition code for muscle-specific gene activation. Cell. 1990; 60(5):733-46. DOI: 10.1016/0092-8674(90)90088-v. View

18.

Wentworth B, Donoghue M, Engert J, BERGLUND E, Rosenthal N . Paired MyoD-binding sites regulate myosin light chain gene expression. Proc Natl Acad Sci U S A. 1991; 88(4):1242-6. PMC: 50993. DOI: 10.1073/pnas.88.4.1242. View

19.

Olson E . MyoD family: a paradigm for development?. Genes Dev. 1990; 4(9):1454-61. DOI: 10.1101/gad.4.9.1454. View

20.

Chakraborty T, Brennan T, Olson E . Differential trans-activation of a muscle-specific enhancer by myogenic helix-loop-helix proteins is separable from DNA binding. J Biol Chem. 1991; 266(5):2878-82. View