Cooperation between myogenic regulatory factors and SIX family transcription factors is important for myoblast differentiation

Liu, Yubing; Chu, Alphonse; Chakroun, Imane; Islam, Uzma; Blais, Alexandre

doi:10.1093/nar/gkq585

Cited by 100 publications

(159 citation statements)

References 70 publications

(81 reference statements)

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“…Consequently, an important question in muscle development is how specificity is achieved. A combinatorial action between MRF and other transcription factors has been suggested, and a few examples have been identified 10,41 . In B-cell development, Ebf1 acts synergistically with the transcription factor E47, a product of the E2A gene, which also binds to E-boxes 35 .…”

Section: Discussionmentioning

confidence: 99%

Ebf factors and MyoD cooperate to regulate muscle relaxation via Atp2a1

et al. 2014

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Myogenic regulatory factors such as MyoD and Myf5 lie at the core of vertebrate muscle differentiation. However, E-boxes, the cognate binding sites for these transcription factors, are not restricted to the promoters/enhancers of muscle cell-specific genes. Thus, the specificity in myogenic transcription is poorly defined. Here we describe the transcription factor Ebf3 as a new determinant of muscle cell-specific transcription. In the absence of Ebf3 the lung does not unfold at birth, resulting in respiratory failure and perinatal death. This is due to a hypercontractile diaphragm with impaired Ca 2 þ efflux-related muscle functions. Expression of the Ca 2 þ pump Serca1 (Atp2a1) is downregulated in the absence of Ebf3, and its transgenic expression rescues this phenotype. Ebf3 binds directly to the promoter of Atp2a1 and synergises with MyoD in the induction of Atp2a1. In skeletal muscle, the homologous family member Ebf1 is strongly expressed and together with MyoD induces Atp2a1. Thus, Ebf3 is a new regulator of terminal muscle differentiation in the diaphragm, and Ebf factors cooperate with MyoD in the induction of muscle-specific genes.

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Section: Discussionmentioning

confidence: 99%

Ebf factors and MyoD cooperate to regulate muscle relaxation via Atp2a1

et al. 2014

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“…A role for MRFs in the maintenance of premyogenic mesoderm expression is supported by the activation of Six1 by (69). It was originally thought that satellite cells were derived from cells that mark the fetal myoblasts in the chick and mouse (85,86).…”

Section: Discussionmentioning

confidence: 99%

MyoD Directly Up-regulates Premyogenic Mesoderm Factors during Induction of Skeletal Myogenesis in Stem Cells

Gianakopoulos

Mehta

Voronova

et al. 2011

Journal of Biological Chemistry

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Gain-and loss-of-function experiments have illustrated that the family of myogenic regulatory factors is necessary and sufficient for the formation of skeletal muscle. Furthermore, MyoD required cellular aggregation to induce myogenesis in P19 embryonal carcinoma stem cells. To determine the mechanism by which stem cells can be directed into skeletal muscle, a time course of P19 cell differentiation was examined in the presence and absence of exogenous MyoD. By quantitative PCR, the first MyoD up-regulated transcripts were the premyogenic mesoderm factors Meox1, Pax7, Six1, and Eya2 on day 4 of differentiation. Subsequently, the myoblast markers myogenin, MEF2C, and Myf5 were up-regulated, leading to skeletal myogenesis. These results were corroborated by Western blot analysis, showing up-regulation of Pax3, Six1, and MEF2C proteins, prior to myogenin protein expression. To determine at what stage a dominant-negative MyoD/EnR mutant could inhibit myogenesis, stable cell lines were created and examined. Interestingly, the premyogenic mesoderm factors, Meox1, Pax3/7, Six1, Eya2, and Foxc1, were down-regulated, and as expected, skeletal myogenesis was abolished. Finally, to identify direct targets of MyoD in this system, chromatin immunoprecipitation experiments were performed. MyoD was observed associated with regulatory regions of Meox1, Pax3/7, Six1, Eya2, and myogenin genes. Taken together, MyoD directs stem cells into the skeletal muscle lineage by binding and activating the expression of premyogenic mesoderm genes, prior to activating myoblast genes.

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“…The immunopurified and input DNA (pre-IP) samples were amplified by LM-PCR, fluorescently labeled and co-hybridized on a DNA microarray custom made by Agilent Technologies (Mississauga, ON, Canada), essentially as described previously. 55 Experimental details and data analysis methods are provided in Supplementary Text S1. The data have been deposited on the NCBI Gene Expression Omnibus under the accession number GSE54941.…”

Section: Methodsmentioning

confidence: 99%

“…Gene expression data for all E2f3 target genes in NPCs were obtained from the mouse Gene Atlas V3, 61 and was analyzed and normalized as previously described. 55 K-means clustering was performed on the gene expression data using the Cluster 3 program, 62 and was visualized using Java Treeview 63 to identify tissues and cell types that demonstrate similar gene expression profiles.…”

Section: Methodsmentioning

confidence: 99%

Tissue-specific targeting of cell fate regulatory genes by E2f factors

et al. 2015

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Cell cycle proteins are important regulators of diverse cell fate decisions, and in this capacity have pivotal roles in neurogenesis and brain development. The mechanisms by which cell cycle regulation is integrated with cell fate control in the brain and other tissues are poorly understood, and an outstanding question is whether the cell cycle machinery regulates fate decisions directly or instead as a secondary consequence of proliferative control. Identification of the genes targeted by E2 promoter binding factor (E2f) transcription factors, effectors of the pRb/E2f cell cycle pathway, will provide essential insights into these mechanisms. We identified the promoter regions bound by three neurogenic E2f factors in neural precursor cells in a genome-wide manner. Through bioinformatic analyses and integration of published genomic data sets we uncovered hundreds of transcriptionally active E2f-bound promoters corresponding to genes that control cell fate processes, including key transcriptional regulators and members of the Notch, fibroblast growth factor, Wnt and Tgf-β signaling pathways. We also demonstrate a striking enrichment of the CCCTC binding factor transcription factor (Ctcf) at E2f3-bound nervous system-related genes, suggesting a potential regulatory co-factor for E2f3 in controlling differentiation. Finally, we provide the first demonstration of extensive tissue specificity among E2f target genes in mammalian cells, whereby E2f3 promoter binding is well conserved between neural and muscle precursors at genes associated with cell cycle processes, but is tissue-specific at differentiation-associated genes. Our findings implicate the cell cycle pathway as a widespread regulator of cell fate genes, and suggest that E2f3 proteins control cell typespecific differentiation programs by regulating unique sets of target genes. This work significantly enhances our understanding of how the cell cycle machinery impacts cell fate and differentiation, and will importantly drive further discovery regarding the mechanisms of cell fate control and transcriptional regulation in the brain, as well as in other tissues.

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Cooperation between myogenic regulatory factors and SIX family transcription factors is important for myoblast differentiation

Cited by 100 publications

References 70 publications

Ebf factors and MyoD cooperate to regulate muscle relaxation via Atp2a1

Ebf factors and MyoD cooperate to regulate muscle relaxation via Atp2a1

MyoD Directly Up-regulates Premyogenic Mesoderm Factors during Induction of Skeletal Myogenesis in Stem Cells

Tissue-specific targeting of cell fate regulatory genes by E2f factors

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