ReviewSWI/SNF complexes, chromatin remodeling and skeletal myogenesis: It's time to exchange!
Introduction
During cellular differentiation, the activation of tissue- and lineage-specific genes coincides with the disruption of the repressive conformation imposed by nucleosomes at previously silent loci. This task is achieved by the combinatorial activities of tissue-specific transcription factors and multi-sub-unit machineries that decompose the chromatin by disassembling and reassembling the nucleosomes [1]. For instance, during skeletal muscle differentiation the myogenic bHLH proteins MyoD and Myf5, which are expressed in myoblasts prior to the differentiation, face the challenge of gaining access to their binding sites (the so-called Eboxes-CANNTG) on muscle genes, by overcoming the unfavorable conformation of repressive chromatin [2]. Physical and functional interactions between muscle bHLH proteins and ATP-dependent SWI/SNF chromatin-remodeling complexes [3], [4] promote the displacement of nucleosomes and generate the landscape conducive for the activation of transcription, by favoring the access of muscle bHLH proteins and MEF2 factors, and the assembly of the myogenic transcriptosome. The alternative presence of two catalytic sub-units, either Brg1 or Brm, confers on the SWI/SNF complex the ATPase activity necessary to remodel the chromatin [5]; moreover, different combinations of non-enzymatic, structural sub-units, such as the Brg1/Brm-associated factors (BAFs), can generate different sub-complexes, thereby providing the molecular variability by which SWI/SNF complexes select the interactions with different tissue-specific transcription factors and with other chromatin-modifying enzymes [6], [7]. Thus, the specific composition of SWI/SNF sub-complexes determines their activity and specificity for particular subsets of genes. An exchange of SW/SNF variant sub-units at key transitions of the myogenic program might generate sub-complexes dedicated to specific tasks, such as facilitating the access of pioneer transcriptional activators and “reading” the combinations of histone marks generated by the activity of muscle-specific transcription factors and components of the epigenetic machinery.
Section snippets
Transcriptional control by chromatin remodelers during skeletal muscle differentiation
The muscle regulatory factors (MRFs) belonging to the bHLH family — MyoD, Myf5, MRF4 and myogenin — activates and perpetuates the skeletal myogenic program by promoting the gradual expression of muscle-specific genes in myoblasts [8]. This task is achieved with the contribution of other transcription factors, such as the MEF2 family members, which are expressed ubiquitously and cooperate with muscle bHLH proteins to activate muscle-gene transcription in myoblasts [9]. Recent evidence supports
SWI/SNF sub-complexes and cellular differentiation: a tissue-specific regulation of sub-unit exchange
The multitude of interaction between SWI/SNF and other chromatin-associated proteins, as well as the temporal and gene-specific SWI/SNF distribution during skeletal myogenesis, suggest that distinct SWI/SNF sub-complexes can perform specific tasks and are subjected to different types of regulation. Indeed, increasing evidence is supporting the concept that SWI/SNF composition can vary depending on the cell type and in response to specific cues.
Conclusions and perspectives
The fundamental contribution of chromatin remodelers to the re-configuration of the chromatin architecture during skeletal myogenesis suggests the involvement of SWI/SNF complexes in many transcriptional events, including repression and activation of gene expression, but also regulation of control long-distance genome interactions and the non-coding (nc) epigenome. Indeed, the essential role of Brg1 in the activation of muscle-specific micro-RNAs activated by MyoD has recently been reported by
Acknowledgments
PLP is an Associate Scientist of Telethon Dulbecco Institute (DTI) and of the Sanford Children' Health Center at Sanford/Burnham Medical Institute, and was partially supported by AIRC and NIAMS (RO1AR052779).
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Histone Modifications
2019, Epigenetics and RegenerationMolecular and cellular regulation of skeletal myogenesis
2014, Current Topics in Developmental BiologyCitation Excerpt :Subsequently, Myod recruits SWI/SNF proteins that use ATP hydrolysis to disrupt the interaction between DNA and histone octamers (de la Serna et al., 2005). These events would then render the canonical E-box-binding sites more accessible to Myod to promote transcription (de la Serna et al., 2005; Dilworth, Seaver, Fishburn, Htet, & Tapscott, 2004; Puri et al., 1997), reviewed in Guasconi & Puri, 2009; Albini and Puri, 2010). The SWI/SNF complexes act in virtually all cell processes, and they are essential for establishing and maintaining pluripotent and multipotent cell states (Lessard & Crabtree, 2010).
Functional studies of the Ciona intestinalis myogenic regulatory factor reveal conserved features of chordate myogenesis
2013, Developmental BiologyCitation Excerpt :Individually, however, their importance varies depending on the target gene thus indicating that vertebrate MRFs regulate different muscle genes by distinct mechanisms (Brennan et al., 1991; Davis and Weintraub, 1992; Schwarz et al., 1992; Rawls et al., 1995; Gerber et al., 1997; Kablar et al., 1997; Wang and Jaenisch, 1997; Bergstrom and Tapscott, 2001; de la Serna et al., 2001; Myer et al., 2001; Berkes et al., 2004; Cao et al., 2006; Heidt et al., 2007). Consistent with this idea, vertebrate MRFs have been shown to bind to consensus E-box motifs of some genes and non-consensus E-boxes of others (Blackwell and Weintraub, 1990; Heidt et al., 2007), to bind non-E-box motifs (Shklover et al., 2007), and to interact directly or even indirectly with different muscle genes via associations with a variety of transcription factors (Molkentin et al., 1995; Groisman et al., 1996; Berkes et al., 2004; Ohkawa et al., 2006; Albini and Puri, 2010; Liu et al., 2010; Delgado-Olguín et al., 2011). Structure/function studies with vertebrates have provided important insights into the mechanisms by which muscle gene activity is regulated by MRFs, but invertebrate systems such as C. intestinalis have much to offer as well.
Non-viral expression of mouse Oct4, Sox2, and Klf4 transcription factors efficiently reprograms tadpole muscle fibers in vivo
2012, Journal of Biological ChemistryCitation Excerpt :Both factors were detectable in uninjected (WT) muscle but were specifically up-regulated in OSK-injected muscles (Fig. 3J). Reactivation of brg1 expression was observed from 14 dpi in GFP-controls and might be involved in MyoD-mediated differentiation during muscle repair (44). Telomerase activity induction is another important feature of iPSCs (45).