Epigenetic control of skeletal muscle regeneration: Integrating genetic determinants and environmental changes - PubMed
Review
. 2013 Sep;280(17):4014-25.
doi: 10.1111/febs.12383. Epub 2013 Jul 15.
Affiliations
- PMID: 23745685
- PMCID: PMC3753079
- DOI: 10.1111/febs.12383
Review
Epigenetic control of skeletal muscle regeneration: Integrating genetic determinants and environmental changes
Lorenzo Giordani et al. FEBS J. 2013 Sep.
Abstract
During embryonic development, pluripotent cells are genetically committed to specific lineages by the expression of cell-type-specific transcriptional activators that direct the formation of specialized tissues and organs in response to developmental cues. Chromatin-modifying proteins are emerging as essential components of the epigenetic machinery, which establishes the nuclear landscape that ultimately determines the final identity and functional specialization of adult cells. Recent evidence has revealed that discrete populations of adult cells can retain the ability to adopt alternative cell fates in response to environmental cues. These cells include conventional adult stem cells and a still poorly defined collection of cell types endowed with facultative phenotype and functional plasticity. Under physiological conditions or adaptive states, these cells cooperate to support tissue and organ homeostasis, and to promote growth or compensatory regeneration. However, during chronic diseases and aging these cells can adopt a pathological phenotype and mediate maladaptive responses, such as the formation of fibrotic scars and fat deposition that progressively replaces structural and functional units of tissues and organs. The molecular determinants of these phenotypic transitions are only emerging from recent studies that reveal how dynamic chromatin states can generate flexible epigenetic landscapes, which confer on cells the ability to retain partial pluripotency and adapt to environmental changes. This review summarizes our current knowledge on the role of the epigenetic machinery as a 'filter' between genetic commitment and environmental signals in cell types that can alternatively promote skeletal muscle regeneration or fibro-adipogenic degeneration.
Keywords: Duchenne dystrophy; chromatin; epigenetics; fibro/adipogenic progenitors; muscle; muscle differentiation; muscle interstistial cells; muscle stem cells; regeneration; satellite cells.
© 2013 FEBS.
Figures

Illustration of the different functional states of MuSCs and related regulatory networks that coordinate expression of different subsets of genes at each stage. In quiescent cells the muscle stem cells lineage is maintained through the cooperation of Pax7 and PRC2 that promote the expression of MuSC lineage genes and repressed muscle differentiation genes, respectively, and through miR31 that blocks Myf5 translation. Upon activation by muscle injury, the exposure to regeneration cues promotes asymmetric division, giving rise to differentiation-committed MuSCs in which Pax7 activates the expression of cell cycle genes and, with the collaboration of the Wdr5-Ash2L-MLL2 histone methyltransferase complex (HMT) promotes Myf5 transcription. At the same time HDAC class I and II contribute to repress the activity of MEF2 and MyoD and hold the cells at the stage of proliferating myoblasts. Subsequent exposure to differentiation signals triggers pro-myogenic cascades (e.g. p38) and causes the recruitment of SWI/SNF complex on muscle loci, the deposition of H3K4 marks on Myog and CKM by the HMT complex and the downregulation of the PRC2 enzymatic subunit EzH2. MyoD and SWI/SNF complex also promote the expression of Myomirs. In addition different miR contribute to the repression of Pax7 YY1 and Ezh2. The overall decrease in Ezh2 levels lead to de-repression of muscle genes and formation of limiting amounts of EzH2-based PRC2 complexes that extinguish the expression of Pax7 and cell cycle genes.

Schematic representation of the possible lineages that can be adopted by the different muscle resident cells. List of the reference used in the figure: 1 (Gussoni et al. 1999); 2 (Uezumi et al. 2006); 3 (Qu-Petersen et al. 2002); 4 (Cao et al. 2003); 5 (A. Dellavalle et al. 2007); 6 (Alliot-Licht et al. 2005); 7 (Farrington-Rock et al. 2004); 8 (Schor et al. 1990); 9 (Doherty et al. 1998); 10 (Minasi et al. 2002); 11 (Mitchell et al. 2010); 12 (Joe et al. 2010);13 (Uezumi et al. 2010)
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