DOI: 10.1101/gad.1234304. A MyoD-generated feed-forward circuit temporally patterns gene expression during skeletal muscle differentiation

A MyoD-generated feed-forward circuit temporally patterns gene expression during skeletal muscle differentiation

10.1101/gad.1234304

Crossref journal-article

Cold Spring Harbor Laboratory

Genes & Development (246)

Abstract

The development and differentiation of distinct cell types is achieved through the sequential expression of subsets of genes; yet, the molecular mechanisms that temporally pattern gene expression remain largely unknown. In skeletal myogenesis, gene expression is initiated by MyoD and includes the expression of specific Mef2 isoforms and activation of the p38 mitogen-activated protein kinase (MAPK) pathway. Here, we show that p38 activity facilitates MyoD and Mef2 binding at a subset of late-activated promoters, and the binding of Mef2D recruits Pol II. Most importantly, expression of late-activated genes can be shifted to the early stages of differentiation by precocious activation of p38 and expression of Mef2D, demonstrating that a MyoD-mediated feed-forward circuit temporally patterns gene expression.

Bibliography

Penn, B. H., Bergstrom, D. A., Dilworth, F. J., Bengal, E., & Tapscott, S. J. (2004). A MyoD-generated feed-forward circuit temporally patterns gene expression during skeletal muscle differentiation. Genes & Development, 18(19), 2348â2353.

Authors 5

Bennett H. Penn (first)
Donald A. Bergstrom (additional)
F. Jeffrey Dilworth (additional)
Eyal Bengal (additional)
Stephen J. Tapscott (additional)

References 30 Referenced 158

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10.1016/S1097-2765(02)00481-1
10.1126/science.2174572
10.1073/pnas.87.20.7988
10.1016/S1097-2765(02)00604-4
10.1074/jbc.M211312200
10.1074/jbc.274.7.4341
10.1016/S0888-7543(03)00104-6
10.1074/jbc.271.6.2886
10.1038/386296a0
10.1073/pnas.90.17.8028
10.1126/science.1075090
10.1016/S0898-6568(00)00120-0
10.1002/cm.970290102
10.1073/pnas.2133841100
10.1126/science.298.5594.824
10.1128/jvi.70.8.5701-5705.1996 / J. Virol. (1996)
10.1093/nar/27.13.2646
10.1101/gad.14.5.574 / Genes & Dev. (2000)
10.1038/ni748
10.1038/ng881
10.1038/ng1378
10.1073/pnas.1530509100
10.1074/jbc.M005815200
{'key': '2021111620092286000_18.19.2348.25', 'first-page': '403', 'volume': '18', 'year': '2003', 'journal-title': 'FASEB J.'} / FASEB J. (2003)
10.1073/pnas.86.14.5434
10.1128/MCB.20.11.3951-3964.2000
10.1074/jbc.274.8.5193
10.1128/MCB.19.1.21 / Mol. Cell. Biol. (1999)
10.1074/jbc.M202668200

Dates

Type	When
Created	20 years, 11 months ago (Oct. 4, 2004, 2:22 p.m.)
Deposited	3 years, 9 months ago (Nov. 16, 2021, 11:15 p.m.)
Indexed	1 month, 3 weeks ago (July 11, 2025, 6:16 a.m.)
Issued	20 years, 11 months ago (Oct. 1, 2004)
Published	20 years, 11 months ago (Oct. 1, 2004)
Published Online	20 years, 11 months ago (Oct. 1, 2004)
Published Print	20 years, 11 months ago (Oct. 1, 2004)

Funders 0

None

BibTeX

@article{Penn_2004, title={A MyoD-generated feed-forward circuit temporally patterns gene expression during skeletal muscle differentiation}, volume={18}, ISSN={1549-5477}, url={http://dx.doi.org/10.1101/gad.1234304}, DOI={10.1101/gad.1234304}, number={19}, journal={Genes & Development}, publisher={Cold Spring Harbor Laboratory}, author={Penn, Bennett H. and Bergstrom, Donald A. and Dilworth, F. Jeffrey and Bengal, Eyal and Tapscott, Stephen J.}, year={2004}, month=oct, pages={2348–2353} }

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