Chromatin signaling in muscle stem cells: Interpreting the regenerative microenvironment

Frontiers in Aging Neuroscience

Volumn 7, Issue MAR, 2015, Pages

  Brancaccio, Arianna ^a   Palacios, Daniela ^a  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT STEM CELL; CELL DIFFERENTIATION; CELL FUNCTION; CHROMATIN; CHROMATIN STRUCTURE; DNA METHYLATION; DNA SEQUENCE; EPIGENETICS; GENE EXPRESSION; HISTONE MODIFICATION; HUMAN; MICROENVIRONMENT; MUSCLE DEVELOPMENT; MUSCLE REGENERATION; MUSCLE STEM CELL; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUTRIENT AVAILABILITY; REGENERATIVE MEDICINE; REVIEW; SATELLITE CELL; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

EID: 84926288297     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2015.00036     Document Type: Review

References (246)

1. Abdel Khalek, W., Cortade, F., Ollendorff, V., Lapasset, L., Tintignac, L., Chabi, B., et al. (2014). SIRT3, a Mitochondrial NAD+-Dependent Deacetylase, Is Involved in the Regulation of Myoblast Differentiation. PLoS ONE 9, e114388.
2. Acharyya, S., Sharma, S.M., Cheng, A.S., Ladner, K.J., He, W., Kline, W., et al (2010). TNF inhibits Notch-1 in skeletal muscle cells by Ezh2 and DNA methylation mediated repression: implications in duchenne muscular dystrophy. PLoS ONE 5, e12479.
3. Al-Sawaf, O., Fragoulis, A., Rosen, C., Keimes, N., Liehn, E.A., Holzle, F., et al (2014). Nrf2 augments skeletal muscle regeneration after ischaemia-reperfusion injury. J Pathol 234, 538-547.
4. Ardite, E., Barbera, J.A., Roca, J., and Fernandez-Checa, J.C. (2004). Glutathione depletion impairs myogenic differentiation of murine skeletal muscle C2C12 cells through sustained NF-kappaB activation. Am J Pathol 165, 719-728.
5. Armand, A.S., Bourajjaj, M., Martinez-Martinez, S., el Azzouzi, H., da Costa Martins, P.A., et al (2008). Cooperative synergy between NFAT and MyoD regulates myogenin expression and myogenesis. J Biol Chem 283, 29004-29010.
6. Asp, P., Blum, R., Vethantham, V., Parisi, F., Micsinai, M., Cheng, J., et al (2011). Genome-wide remodeling of the epigenetic landscape during myogenic differentiation. Proc Natl Acad Sci U S A 108, E149-158.
7. Azuara, V., Perry, P., Sauer, S., Spivakov, M., Jorgensen, H.F., John, R.M., et al. (2006). Chromatin signatures of pluripotent cell lines. Nat Cell Biol 8, 532-538.
8. Bannister, A.J., and Kouzarides, T. (2011). Regulation of chromatin by histone modifications. Cell Res 21, 381-395.
9. Barja, G. (1999). Mitochondrial oxygen radical generation and leak: sites of production in states 4 and 3, organ specificity, and relation to aging and longevity. J Bioenerg Biomembr 31, 347-366.
10. Basu, S., Totty, N.F., Irwin, M.S., Sudol, M., and Downward, J. (2003). Akt phosphorylates the Yes-associated protein, YAP, to induce interaction with 14-3-3 and attenuation of p73-mediated apoptosis. Mol Cell 11, 11-23.
11. Bergman, Y., and Cedar, H. (2013). DNA methylation dynamics in health and disease. Nat Struct Mol Biol 20, 274-281.
12. Bernet, J.D., Doles, J.D., Hall, J.K., Kelly Tanaka, K., Carter, T.A., and Olwin, B.B. (2014). p38 MAPK signaling underlies a cell-autonomous loss of stem cell selfrenewal in skeletal muscle of aged mice. Nat Med 20, 265-271.
13. Bernstein, B.E., Meissner, A., and Lander, E.S. (2007). The mammalian epigenome. Cell 128, 669-681.
14. Bird, A., Taggart, M., Frommer, M., Miller, O.J., and Macleod, D. (1985). A fraction of the mouse genome that is derived from islands of nonmethylated, CpG-rich DNA. Cell 40, 91-99.
15. Bjornson, C.R., Cheung, T.H., Liu, L., Tripathi, P.V., Steeper, K.M., and Rando, T.A. (2012). Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells 30, 232-242.
16. Blackledge, N.P., Farcas, A.M., Kondo, T., King, H.W., McGouran, J.F., Hanssen, L.L., et al. (2014). Variant PRC1 complex-dependent H2A ubiquitylation drives PRC2 recruitment and polycomb domain formation. Cell 157, 1445-1459.
17. Blattler, S.M., Cunningham, J.T., Verdeguer, F., Chim, H., Haas, W., Liu, H., et al. (2012). Yin Yang 1 deficiency in skeletal muscle protects against rapamycin-induced diabetic-like symptoms through activation of insulin/IGF signaling. Cell Metab 15, 505-517.
18. Blum, R., and Dynlacht, B.D. (2013). The role of MyoD1 and histone modifications in the activation of muscle enhancers. Epigenetics 8, 778-784.
19. Blum, R., Vethantham, V., Bowman, C., Rudnicki, M., and Dynlacht, B.D. (2012). Genome-wide identification of enhancers in skeletal muscle: the role of MyoD1. Genes Dev 26, 2763-2779.
20. Brack, A.S., Conboy, I.M., Conboy, M.J., Shen, J., and Rando, T.A. (2008). A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell 2, 50-59.
21. Brack, A.S., Conboy, M.J., Roy, S., Lee, M., Kuo, C.J., Keller, C., et al. (2007). Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317, 807-810.
22. Brack, A.S., Murphy-Seiler, F., Hanifi, J., Deka, J., Eyckerman, S., Keller, C., et al. (2009). BCL9 is an essential component of canonical Wnt signaling that mediates the differentiation of myogenic progenitors during muscle regeneration. Dev Biol 335, 93-105.
23. Brack, A.S., and Rando, T.A. (2007). Intrinsic changes and extrinsic influences of myogenic stem cell function during aging. Stem Cell Rev 3, 226-237.
24. Brenman, J.E., Chao, D.S., Xia, H., Aldape, K., and Bredt, D.S. (1995). Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell 82, 743-752.
25. Buck, M., and Chojkier, M. (1996). Muscle wasting and dedifferentiation induced by oxidative stress in a murine model of cachexia is prevented by inhibitors of nitric oxide synthesis and antioxidants. Embo J 15, 1753-1765.
26. Buckingham, M., and Rigby, P.W. (2014). Gene regulatory networks and transcriptional mechanisms that control myogenesis. Dev Cell 28, 225-238.
27. Burks, T.N., and Cohn, R.D. (2011). Role of TGF-beta signaling in inherited and acquired myopathies. Skelet Muscle 1, 19.
28. Cacchiarelli, D., Martone, J., Girardi, E., Cesana, M., Incitti, T., Morlando, M., et al. (2010). MicroRNAs involved in molecular circuitries relevant for the Duchenne muscular dystrophy pathogenesis are controlled by the dystrophin/nNOS pathway. Cell Metab 12, 341-351.
29. Calabria, E., Ciciliot, S., Moretti, I., Garcia, M., Picard, A., Dyar, K.A., et al. (2009). NFAT isoforms control activity-dependent muscle fiber type specification. Proc Natl Acad Sci U S A 106, 13335-13340.
30. Canalis, E., Economides, A.N., and Gazzerro, E. (2003). Bone morphogenetic proteins, their antagonists, and the skeleton. Endocr Rev 24, 218-235.
31. Cao, Y., Yao, Z., Sarkar, D., Lawrence, M., Sanchez, G.J., Parker, M.H., et al. (2010). Genome-wide MyoD binding in skeletal muscle cells: a potential for broad cellular reprogramming. Dev Cell 18, 662-674.
32. Castel, D., Mourikis, P., Bartels, S.J., Brinkman, A.B., Tajbakhsh, S., and Stunnenberg, H.G. (2013). Dynamic binding of RBPJ is determined by Notch signaling status. Genes Dev 27, 1059-1071.
33. Cazzella, V., Martone, J., Pinnaro, C., Santini, T., Twayana, S.S., Sthandier, O., et al. (2012). Exon 45 skipping through U1-snRNA antisense molecules recovers the DysnNOS pathway and muscle differentiation in human DMD myoblasts. Mol Ther 20, 2134-2142.
34. Cha, T.L., Zhou, B.P., Xia, W., Wu, Y., Yang, C.C., Chen, C.T., et al. (2005). Aktmediated phosphorylation of EZH2 suppresses methylation of lysine 27 in histone H3. Science 310, 306-310.
35. Charge, S.B., and Rudnicki, M.A. (2004). Cellular and molecular regulation of muscle regeneration. Physiol Rev 84, 209-238.
36. Chen, A.E., Ginty, D.D., and Fan, C.M. (2005). Protein kinase A signalling via CREB controls myogenesis induced by Wnt proteins. Nature 433, 317-322.
37. Chen, S.L., Loffler, K.A., Chen, D., Stallcup, M.R., and Muscat, G.E. (2002). The coactivator-associated arginine methyltransferase is necessary for muscle differentiation: CARM1 coactivates myocyte enhancer factor-2. J Biol Chem 277, 4324-4333.
38. Chiarugi, P., and Cirri, P. (2003). Redox regulation of protein tyrosine phosphatases during receptor tyrosine kinase signal transduction. Trends Biochem Sci 28, 509-514.
39. Choi, J., Jang, H., Kim, H., Lee, J.H., Kim, S.T., Cho, E.J., et al. (2014a). Modulation of lysine methylation in myocyte enhancer factor 2 during skeletal muscle cell differentiation. Nucleic Acids Res 42, 224-234.
40. Choi, J.K. (2010). Contrasting chromatin organization of CpG islands and exons in the human genome. Genome Biol 11, R70.
41. Choi, M.C., Ryu, S., Hao, R., Wang, B., Kapur, M., Fan, C.M., et al. (2014b). HDAC4 promotes Pax7-dependent satellite cell activation and muscle regeneration. EMBO Rep 15, 1175-1183.
42. Chow, C.W., and Davis, R.J. (2006). Proteins kinases: chromatin-associated enzymes? Cell 127, 887-890.
43. Colussi, C., Gurtner, A., Rosati, J., Illi, B., Ragone, G., Piaggio, G., et al. (2009). Nitric oxide deficiency determines global chromatin changes in Duchenne muscular dystrophy. Faseb J 23, 2131-2141.
44. Colussi, C., Mozzetta, C., Gurtner, A., Illi, B., Rosati, J., Straino, S., et al. (2008). HDAC2 blockade by nitric oxide and histone deacetylase inhibitors reveals a common target in Duchenne muscular dystrophy treatment. Proc Natl Acad Sci U S A 105, 19183-19187.
45. Conboy, I.M., Conboy, M.J., Wagers, A.J., Girma, E.R., Weissman, I.L., and Rando, T.A. (2005). Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433, 760-764.
46. Conboy, I.M., and Rando, T.A. (2002). The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell 3, 397-409.
47. Consalvi, S., Mozzetta, C., Bettica, P., Germani, M., Fiorentini, F., Del Bene, F., et al. (2013). Preclinical studies in the mdx mouse model of duchenne muscular dystrophy with the histone deacetylase inhibitor givinostat. Mol Med 19, 79-87.
48. Cooper, S., Dienstbier, M., Hassan, R., Schermelleh, L., Sharif, J., Blackledge, N.P., et al. (2014). Targeting polycomb to pericentric heterochromatin in embryonic stem cells reveals a role for H2AK119u1 in PRC2 recruitment. Cell Rep 7, 1456-1470.
49. Cornelison, D.D., and Wold, B.J. (1997). Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191, 270-283.
50. Cosgrove, B.D., Gilbert, P.M., Porpiglia, E., Mourkioti, F., Lee, S.P., Corbel, S.Y., et al. (2014). Rejuvenation of the muscle stem cell population restores strength to injured aged muscles. Nat Med 20, 255-264.
51. Cuenda, A., and Cohen, P. (1999). Stress-activated protein kinase-2/p38 and a rapamycin-sensitive pathway are required for C2C12 myogenesis. J Biol Chem 274, 4341-4346.
52. Cunningham, J.T., Rodgers, J.T., Arlow, D.H., Vazquez, F., Mootha, V.K., and Puigserver, P. (2007). mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Nature 450, 736-740.
53. Cuschieri, J., and Maier, R.V. (2005). Mitogen-activated protein kinase (MAPK). Crit Care Med 33, S417-419.
54. Dacwag, C.S., Bedford, M.T., Sif, S., and Imbalzano, A.N. (2009). Distinct protein arginine methyltransferases promote ATP-dependent chromatin remodeling function at different stages of skeletal muscle differentiation. Mol Cell Biol 29, 1909-1921.
55. Dahlqvist, C., Blokzijl, A., Chapman, G., Falk, A., Dannaeus, K., Ibanez, C.F., et al. (2003). Functional Notch signaling is required for BMP4-induced inhibition of myogenic differentiation. Development 130, 6089-6099.
56. Day, K., Waite, L.L., Thalacker-Mercer, A., West, A., Bamman, M.M., Brooks, J.D., Myers, R.M., and Absher, D. (2013). Differential DNA methylation with age displays both common and dynamic features across human tissues that are influenced by CpG landscape. Genome Biol 14, R102.
57. de Nadal, E., and Posas, F. (2010). Multilayered control of gene expression by stressactivated protein kinases. Embo J 29, 4-13.
58. Delling, U., Tureckova, J., Lim, H.W., De Windt, L.J., Rotwein, P., and Molkentin, J.D. (2000). A calcineurin-NFATc3-dependent pathway regulates skeletal muscle differentiation and slow myosin heavy-chain expression. Mol Cell Biol 20, 6600-6611.
59. Deuring, R., Fanti, L., Armstrong, J.A., Sarte, M., Papoulas, O., Prestel, M., et al. (2000). The ISWI chromatin-remodeling protein is required for gene expression and the maintenance of higher order chromatin structure in vivo. Mol Cell 5, 355-365.
60. Di Padova, M., Caretti, G., Zhao, P., Hoffman, E.P., and Sartorelli, V. (2007). MyoD acetylation influences temporal patterns of skeletal muscle gene expression. J Biol Chem 282, 37650-37659.
61. Dilworth, F.J., Seaver, K.J., Fishburn, A.L., Htet, S.L., and Tapscott, S.J. (2004). In vitro transcription system delineates the distinct roles of the coactivators pCAF and p300 during MyoD/E47-dependent transactivation. Proc Natl Acad Sci U S A 101, 11593-11598.
62. Dirks, A.J., and Leeuwenburgh, C. (2006). Tumor necrosis factor alpha signaling in skeletal muscle: effects of age and caloric restriction. J Nutr Biochem 17, 501-508.
63. Doi, R., Endo, M., Yamakoshi, K., Yamanashi, Y., Nishita, M., Fukada, S., et al. (2014). Critical role of Frizzled1 in age-related alterations of Wnt/beta-catenin signal in myogenic cells during differentiation. Genes Cells 19, 287-296.
64. Dupont, S., Morsut, L., Aragona, M., Enzo, E., Giulitti, S., Cordenonsi, M., et al. (2011). Role of YAP/TAZ in mechanotransduction. Nature 474, 179-183.
65. Duquet, A., Polesskaya, A., Cuvellier, S., Ait-Si-Ali, S., Hery, P., Pritchard, L.L., et al. (2006). Acetylation is important for MyoD function in adult mice. EMBO Rep 7, 1140-1146.
66. Eckhardt, F., Lewin, J., Cortese, R., Rakyan, V.K., Attwood, J., Burger, M., et al. (2006). DNA methylation profiling of human chromosomes 6, 20 and 22. Nat Genet 38, 1378-1385.
67. Elia, D., Madhala, D., Ardon, E., Reshef, R., and Halevy, O. (2007). Sonic hedgehog promotes proliferation and differentiation of adult muscle cells: Involvement of MAPK/ERK and PI3K/Akt pathways. Biochim Biophys Acta 1773, 1438-1446.
68. Ervasti, J.M., and Sonnemann, K.J. (2008). Biology of the striated muscle dystrophinglycoprotein complex. Int Rev Cytol 265, 191-225.
69. Feinberg, A.P., and Tycko, B. (2004). The history of cancer epigenetics. Nat Rev Cancer 4, 143-153.
70. Fong, A.P., Yao, Z., Zhong, J.W., Cao, Y., Ruzzo, W.L., Gentleman, R.C., et al. (2012). Genetic and epigenetic determinants of neurogenesis and myogenesis. Dev Cell 22, 721-735.
71. Forcales, S.V., Albini, S., Giordani, L., Malecova, B., Cignolo, L., Chernov, A., et al. (2012). Signal-dependent incorporation of MyoD-BAF60c into Brg1-based SWI/SNF chromatin-remodelling complex. Embo J 31, 301-316.
72. Formicola, L., Marazzi, G., and Sassoon, D.A. (2014). The extraocular muscle stem cell niche is resistant to ageing and disease. Front Aging Neurosci 6, 328.
73. Friday, B.B., Horsley, V., and Pavlath, G.K. (2000). Calcineurin activity is required for the initiation of skeletal muscle differentiation. J Cell Biol 149, 657-666.
74. Friday, B.B., and Pavlath, G.K. (2001). A calcineurin- and NFAT-dependent pathway regulates Myf5 gene expression in skeletal muscle reserve cells. J Cell Sci 114, 303-310.
75. Friedrichs, M., Wirsdoerfer, F., Flohe, S.B., Schneider, S., Wuelling, M., and Vortkamp, A. (2011). BMP signaling balances proliferation and differentiation of muscle satellite cell descendants. BMC Cell Biol 12, 26.
76. Fu, W., Asp, P., Canter, B., and Dynlacht, B.D. (2014). Primary cilia control hedgehog signaling during muscle differentiation and are deregulated in rhabdomyosarcoma. Proc Natl Acad Sci U S A 111, 9151-9156.
77. Fulco, M., Schiltz, R.L., Iezzi, S., King, M.T., Zhao, P., Kashiwaya, Y., et al. (2003). Sir2 regulates skeletal muscle differentiation as a potential sensor of the redox state. Mol Cell 12, 51-62.
78. Garcia-Prat, L., Sousa-Victor, P., and Munoz-Canoves, P. (2013). Functional dysregulation of stem cells during aging: a focus on skeletal muscle stem cells. FEBS J 280, 4051-4062.
79. Gardiner-Garden, M., and Frommer, M. (1987). CpG islands in vertebrate genomes. J Mol Biol. 196(2):261-82.
80. George, R.M., Biressi, S., Beres, B.J., Rogers, E., Mulia, A.K., Allen, R.E., et al. (2013). Numb-deficient satellite cells have regeneration and proliferation defects. Proc Natl Acad Sci U S A 110, 18549-18554.
81. Gilbert, P.M., Havenstrite, K.L., Magnusson, K.E., Sacco, A., Leonardi, N.A., Kraft, P., et al. (2011). Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 329, 1078-1081.
82. Gillespie, M.A., Le Grand, F., Scime, A., Kuang, S., von Maltzahn, J., Seale, V., et al. (2009). p38-{gamma}-dependent gene silencing restricts entry into the myogenic differentiation program. J Cell Biol 187, 991-1005.
83. Goll, M.G., and Bestor, T.H. (2005). Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74, 481-514.
84. Grune, T., Brzeski, J., Eberharter, A., Clapier, C.R., Corona, D.F., Becker, P.B., et al. (2003). Crystal structure and functional analysis of a nucleosome recognition module of the remodeling factor ISWI. Mol Cell 12, 449-460.
85. Guardiola, O., Lafuste, P., Brunelli, S., Iaconis, S., Touvier, T., Mourikis, P., et al. (2012). Cripto regulates skeletal muscle regeneration and modulates satellite cell determination by antagonizing myostatin. Proc Natl Acad Sci U S A 109, E3231-3240.
86. Guasconi, V., and Puri, P.L. (2009). Chromatin: the interface between extrinsic cues and the epigenetic regulation of muscle regeneration. Trends Cell Biol 19, 286-294.
87. Guttridge, D.C., Albanese, C., Reuther, J.Y., Pestell, R.G., and Baldwin, A.S., Jr. (1999). NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol Cell Biol 19, 5785-5799.
88. He, Y.F., Li, B.Z., Li, Z., Liu, P., Wang, Y., Tang, Q., et al. (2011). Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333, 1303-1307.
89. Hendrich, B., and Bird, A. (1998). Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol Cell Biol 18, 6538-6547.
90. Hendrich, B., Guy, J., Ramsahoye, B., Wilson, V.A., and Bird, A. (2001). Closely related proteins MBD2 and MBD3 play distinctive but interacting roles in mouse development. Genes Dev 15, 710-723.
91. Himeda, C.L., Barro, M.V., and Emerson, C.P., Jr. (2013). Pax3 synergizes with Gli2 and Zic1 in transactivating the Myf5 epaxial somite enhancer. Dev Biol 383, 7-14.
92. Hoey, T., Sun, Y.L., Williamson, K., and Xu, X. (1995). Isolation of two new members of the NF-AT gene family and functional characterization of the NF-AT proteins. Immunity 2, 461-472.
93. Hogan, P.G., Chen, L., Nardone, J., and Rao, A. (2003). Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev 17, 2205-2232.
94. Hong, W., and Guan, K.L. (2012). The YAP and TAZ transcription co-activators: key downstream effectors of the mammalian Hippo pathway. Semin Cell Dev Biol 23, 785-793.
95. Horsley, V., Friday, B.B., Matteson, S., Kegley, K.M., Gephart, J., and Pavlath, G.K. (2001). Regulation of the growth of multinucleated muscle cells by an NFATC2-dependent pathway. J Cell Biol 153, 329-338.
96. Horsley, V., and Pavlath, G.K. (2002). NFAT: ubiquitous regulator of cell differentiation and adaptation. J Cell Biol 156, 771-774.
97. Huang, J., Wu, S., Barrera, J., Matthews, K., and Pan, D. (2005). The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell 122, 421-434.
98. Huang, P., Zhao, X.S., Fields, M., Ransohoff, R.M., and Zhou, L. (2009). Imatinib attenuates skeletal muscle dystrophy in mdx mice. Faseb J 23, 2539-2548.
99. Iezzi, S., Di Padova, M., Serra, C., Caretti, G., Simone, C., Maklan, E., et al. (2004). Deacetylase inhibitors increase muscle cell size by promoting myoblast recruitment and fusion through induction of follistatin. Dev Cell 6, 673-684.
100. Jeon, Y.H., Park, Y.H., Lee, J.H., Hong, J.H., and Kim, I.Y. (2014). Selenoprotein W enhances skeletal muscle differentiation by inhibiting TAZ binding to 14-3-3 protein. Biochim Biophys Acta 1843, 1356-1364.
101. Jeong, H., Bae, S., An, S.Y., Byun, M.R., Hwang, J.H., Yaffe, M.B., et al. (2010). TAZ as a novel enhancer of MyoD-mediated myogenic differentiation. Faseb J 24, 3310-3320.
102. Jiang, J., and Hui, C.C. (2008). Hedgehog signaling in development and cancer. Dev Cell 15, 801-812.
103. Jin, L., Jiang, Z., Xia, Y., Lou, P., Chen, L., Wang, H., et al. (2014). Genome-wide DNA methylation changes in skeletal muscle between young and middle-aged pigs. BMC Genomics 15, 653.
104. Joe, A.W., Yi, L., Natarajan, A., Le Grand, F., So, L., Wang, J., Rudnicki, M.A., et al. (2010). Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat Cell Biol 12, 153-163.
105. Judson, R.N., Tremblay, A.M., Knopp, P., White, R.B., Urcia, R., De Bari, C., et al. (2012). The Hippo pathway member Yap plays a key role in influencing fate decisions in muscle satellite cells. J Cell Sci 125, 6009-6019.
106. Kaliman, P., Canicio, J., Testar, X., Palacin, M., and Zorzano, A. (1999). Insulin-like growth factor-II, phosphatidylinositol 3-kinase, nuclear factor-kappaB and inducible nitric-oxide synthase define a common myogenic signaling pathway. J Biol Chem 274, 17437-17444.
107. Kasten, M., Szerlong, H., Erdjument-Bromage, H., Tempst, P., Werner, M., and Cairns, B.R. (2004). Tandem bromodomains in the chromatin remodeler RSC recognize acetylated histone H3 Lys14. Embo J 23, 1348-1359.
108. Katoh, M. (2007). WNT signaling pathway and stem cell signaling network. Clin Cancer Res 13, 4042-4045.
109. Kawabe, Y., Wang, Y.X., McKinnell, I.W., Bedford, M.T., and Rudnicki, M.A. (2012). Carm1 regulates Pax7 transcriptional activity through MLL1/2 recruitment during asymmetric satellite stem cell divisions. Cell Stem Cell 11, 333-345.
110. Kegley, K.M., Gephart, J., Warren, G.L., and Pavlath, G.K. (2001). Altered primary myogenesis in NFATC3(-/-) mice leads to decreased muscle size in the adult. Dev Biol 232, 115-126.
111. Klose, R.J., and Zhang, Y. (2007). Regulation of histone methylation by demethylimination and demethylation. Nat Rev Mol Cell Biol 8, 307-318.
112. Kohli, R.M., and Zhang, Y. (2013). TET enzymes, TDG and the dynamics of DNA demethylation. Nature 502, 472-479.
113. Koleva, M., Kappler, R., Vogler, M., Herwig, A., Fulda, S., and Hahn, H. (2005). Pleiotropic effects of sonic hedgehog on muscle satellite cells. Cell Mol Life Sci 62, 1863-1870.
114. Kollias, H.D., Perry, R.L., Miyake, T., Aziz, A., and McDermott, J.C. (2006). Smad7 promotes and enhances skeletal muscle differentiation. Mol Cell Biol 26, 6248-6260.
115. Kopan, R., and Ilagan, M.X. (2009). The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137, 216-233.
116. Kouzarides, T. (1999). Histone acetylases and deacetylases in cell proliferation. Curr Opin Genet Dev 9, 40-48.
117. Kuhl, M. (2004). The WNT/calcium pathway: biochemical mediators, tools and future requirements. Front Biosci 9, 967-974.
118. Lachner, M., O'Carroll, D., Rea, S., Mechtler, K., and Jenuwein, T. (2001). Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410, 116-120.
119. Langen, R.C., Schols, A.M., Kelders, M.C., Wouters, E.F., and Janssen-Heininger, Y.M. (2001). Inflammatory cytokines inhibit myogenic differentiation through activation of nuclear factor-kappaB. Faseb J 15, 1169-1180.
120. Langley, B., Thomas, M., Bishop, A., Sharma, M., Gilmour, S., and Kambadur, R. (2002). Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. J Biol Chem 277, 49831-49840.
121. Laplante, M., and Sabatini, D.M. (2012). mTOR signaling in growth control and disease. Cell 149, 274-293.
122. Lassar, A.B. (2009). The p38 MAPK family, a pushmi-pullyu of skeletal muscle differentiation. J Cell Biol 187, 941-943.
123. Le Grand, F., Jones, A.E., Seale, V., Scime, A., and Rudnicki, M.A. (2009). Wnt7a activates the planar cell polarity pathway to drive the symmetric expansion of satellite stem cells. Cell Stem Cell 4, 535-547.
124. Ling, B.M., Bharathy, N., Chung, T.K., Kok, W.K., Li, S., Tan, Y.H., et al. (2012a). Lysine methyltransferase G9a methylates the transcription factor MyoD and regulates skeletal muscle differentiation. Proc Natl Acad Sci U S A 109, 841-846.
125. Ling, B.M., Gopinadhan, S., Kok, W.K., Shankar, S.R., Gopal, P., Bharathy, N., et al. (2012b). G9a mediates Sharp-1-dependent inhibition of skeletal muscle differentiation. Mol Biol Cell 23, 4778-4785.
126. Liu, D., Kang, J.S., and Derynck, R. (2004). TGF-beta-activated Smad3 represses MEF2-dependent transcription in myogenic differentiation. Embo J 23, 1557-1566.
127. Liu, L., Cheung, T.H., Charville, G.W., Hurgo, B.M., Leavitt, T., Shih, J., et al. (2013). Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging. Cell Rep 4, 189-204.
128. Liu, L., and Rando, T.A. (2011). Manifestations and mechanisms of stem cell aging. J Cell Biol 193, 257-266.
129. Lluis, F., Ballestar, E., Suelves, M., Esteller, M., and Munoz-Canoves, P. (2005). E47 phosphorylation by p38 MAPK promotes MyoD/E47 association and muscle-specific gene transcription. Embo J 24, 974-984.
130. Lluis, F., Perdiguero, E., Nebreda, A.R., and Munoz-Canoves, P. (2006). Regulation of skeletal muscle gene expression by p38 MAP kinases. Trends Cell Biol 16, 36-44.
131. Lu, J., McKinsey, T.A., Zhang, C.L., and Olson, E.N. (2000). Regulation of skeletal myogenesis by association of the MEF2 transcription factor with class II histone deacetylases. Mol Cell 6, 233-244.
132. Luger, K., Mader, A.W., Richmond, R.K., Sargent, D.F., and Richmond, T.J. (1997). Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389, 251-260.
133. Ma, K., Chan, J.K., Zhu, G., and Wu, Z. (2005). Myocyte enhancer factor 2 acetylation by p300 enhances its DNA binding activity, transcriptional activity, and myogenic differentiation. Mol Cell Biol 25, 3575-3582.
134. MacDonald, M.J., and Marshall, L.K. (2000). Mouse lacking NAD+-linked glycerol phosphate dehydrogenase has normal pancreatic beta cell function but abnormal metabolite pattern in skeletal muscle. Arch Biochem Biophys 384, 143-153.
135. Mal, A., Sturniolo, M., Schiltz, R.L., Ghosh, M.K., and Harter, M.L. (2001). A role for histone deacetylase HDAC1 in modulating the transcriptional activity of MyoD: inhibition of the myogenic program. Embo J 20, 1739-1753.
136. Mallappa, C., Hu, Y.J., Shamulailatpam, P., Tae, S., Sif, S., and Imbalzano, A.N. (2011). The expression of myogenic microRNAs indirectly requires protein arginine methyltransferase (Prmt)5 but directly requires Prmt4. Nucleic Acids Res 39, 1243-1255.
137. Margueron, R., and Reinberg, D. (2011). The Polycomb complex PRC2 and its mark in life. Nature 469, 343-349.
138. Martens, J.A., and Winston, F. (2002). Evidence that Swi/Snf directly represses transcription in S. cerevisiae. Genes Dev 16, 2231-2236.
139. Matsumura, K., Tome, F.M., Collin, H., Leturcq, F., Jeanpierre, M., Kaplan, J.C., et al. (1994). Expression of dystrophin-associated proteins in dystrophin-positive muscle fibers (revertants) in Duchenne muscular dystrophy. Neuromuscul Disord 4, 115-120.
140. Mauro, A. (1961). Satellite cell of skeletal muscle fibers. J. Biophys Biochem Cytol Feb9; 493-5.
141. McGill, M.A., and McGlade, C.J. (2003). Mammalian numb proteins promote Notch1 receptor ubiquitination and degradation of the Notch1 intracellular domain. J Biol Chem 278, 23196-23203.
142. McKinnell, I.W., Ishibashi, J., Le Grand, F., Punch, V.G., Addicks, G.C., Greenblatt, J.F., et al. (2008). Pax7 activates myogenic genes by recruitment of a histone methyltransferase complex. Nat Cell Biol 10, 77-84.
143. McKinsey, T.A., Zhang, C.L., Lu, J., and Olson, E.N. (2000). Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature 408, 106-111.
144. McKinsey, T.A., Zhang, C.L., and Olson, E.N. (2001). Identification of a signalresponsive nuclear export sequence in class II histone deacetylases. Mol Cell Biol 21, 6312-6321.
145. Minetti, G.C., Colussi, C., Adami, R., Serra, C., Mozzetta, C., Parente, V., et al. (2006). Functional and morphological recovery of dystrophic muscles in mice treated with deacetylase inhibitors. Nat Med.
146. Mitchell, K.J., Pannerec, A., Cadot, B., Parlakian, A., Besson, V., Gomes, E.R., et al. (2010). Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development. Nat Cell Biol 12, 257-266.
147. Miyazawa, K. (2010). Hepatocyte growth factor activator (HGFA): a serine protease that links tissue injury to activation of hepatocyte growth factor. FEBS J 277, 2208-2214.
148. Montcouquiol, M., Rachel, R.A., Lanford, P.J., Copeland, N.G., Jenkins, N.A., and Kelley, M.W. (2003). Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 423, 173-177.
149. Mourikis, P., Gopalakrishnan, S., Sambasivan, R., and Tajbakhsh, S. (2012a). Cellautonomous Notch activity maintains the temporal specification potential of skeletal muscle stem cells. Development 139, 4536-4548.
150. Mourikis, P., Sambasivan, R., Castel, D., Rocheteau, P., Bizzarro, V., and Tajbakhsh, S. (2012b). A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells 30, 243-252.
151. Mousavi, K., Zare, H., Dell'orso, S., Grontved, L., Gutierrez-Cruz, G., Derfoul, A., et al. (2013). eRNAs promote transcription by establishing chromatin accessibility at defined genomic loci. Mol Cell 51, 606-617.
152. Mousavi, K., Zare, H., Wang, A.H., and Sartorelli, V. (2012). Polycomb protein Ezh1 promotes RNA polymerase II elongation. Mol Cell 45, 255-262.
153. Moustakas, A. (2002). Smad signalling network. J Cell Sci 115, 3355-3356.
154. Mozzetta, C., Consalvi, S., Saccone, V., Forcales, S.V., Puri, P.L., and Palacios, D. (2011). Selective control of Pax7 expression by TNF-activated p38alpha/polycomb repressive complex 2 (PRC2) signaling during muscle satellite cell differentiation. Cell Cycle 10, 191-198.
155. Mozzetta, C., Consalvi, S., Saccone, V., Tierney, M., Diamantini, A., Mitchell, K.J., et al. (2013). Fibroadipogenic progenitors mediate the ability of HDAC inhibitors to promote regeneration in dystrophic muscles of young, but not old Mdx mice. EMBO Mol Med 5, 626-639.
156. Munoz-Canoves, P., Scheele, C., Pedersen, B.K., and Serrano, A.L. (2013). Interleukin-6 myokine signaling in skeletal muscle: a double-edged sword? FEBS J 280, 4131-4148.
157. Murakami, M., Tominaga, J., Makita, R., Uchijima, Y., Kurihara, Y., Nakagawa, O., et al (2006). Transcriptional activity of Pax3 is co-activated by TAZ. Biochem Biophys Res Commun 339, 533-539.
158. Murphy, M.M., Keefe, A.C., Lawson, J.A., Flygare, S.D., Yandell, M., and Kardon, G. (2014). Transiently active Wnt/beta-catenin signaling is not required but must be silenced for stem cell function during muscle regeneration. Stem Cell Reports 3, 475-488.
159. Nakane, M., Schmidt, H.H., Pollock, J.S., Forstermann, U., and Murad, F. (1993). Cloned human brain nitric oxide synthase is highly expressed in skeletal muscle. FEBS Lett 316, 175-180.
160. Nan, X., Meehan, R.R., and Bird, A. (1993). Dissection of the methyl-CpG binding domain from the chromosomal protein MeCP2. Nucleic Acids Res 21, 4886-4892.
161. Nan, X., Ng, H.H., Johnson, C.A., Laherty, C.D., Turner, B.M., Eisenman, R.N., et al. (1998). Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393, 386-389.
162. Nathan, C., and Xie, Q.W. (1994). Nitric oxide synthases: roles, tolls, and controls. Cell 78, 915-918.
163. Ng, H.H., Zhang, Y., Hendrich, B., Johnson, C.A., Turner, B.M., Erdjument- Bromage, H., et al. (1999). MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat Genet 23, 58-61.
164. Ng, S.S., Yue, W.W., Oppermann, U., and Klose, R.J. (2009). Dynamic protein methylation in chromatin biology. Cell Mol Life Sci 66, 407-422.
165. Nott, A., Watson, P.M., Robinson, J.D., Crepaldi, L., and Riccio, A. (2008). SNitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature 455, 411-415.
166. Nusse, R. (2008). Wnt signaling and stem cell control. Cell Res 18, 523-527.
167. Ong, M.L., and Holbrook, J.D. (2014). Novel region discovery method for Infinium 450K DNA methylation data reveals changes associated with aging in muscle and neuronal pathways. Aging Cell 13, 142-155.
168. Ono, Y., Calhabeu, F., Morgan, J.E., Katagiri, T., Amthor, H., and Zammit, P.S (2011). BMP signalling permits population expansion by preventing premature myogenic differentiation in muscle satellite cells. Cell Death Differ 18, 222-234.
169. Palacios, D., Mozzetta, C., Consalvi, S., Caretti, G., Saccone, V., Proserpio, V., et al. (2010). TNF/p38alpha/polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration. Cell Stem Cell 7, 455-469.
170. Palacios, D., and Puri, P.L. (2006). The epigenetic network regulating muscle development and regeneration. J Cell Physiol 207, 1-11.
171. Pan, D. (2010). The hippo signaling pathway in development and cancer. Dev Cell 19, 491-505.
172. Pannerec, A., Formicola, L., Besson, V., Marazzi, G., and Sassoon, D.A. (2013). Defining skeletal muscle resident progenitors and their cell fate potentials. Development 140, 2879-2891.
173. Park, G.H., Jeong, H., Jeong, M.G., Jang, E.J., Bae, M.A., Lee, Y.L., et al. (2014). Novel TAZ modulators enhance myogenic differentiation and muscle regeneration. Br J Pharmacol 171, 4051-4061.
174. Parsons, S.A., Wilkins, B.J., Bueno, O.F., and Molkentin, J.D. (2003). Altered skeletal muscle phenotypes in calcineurin Aalpha and Abeta gene-targeted mice. Mol Cell Biol 23, 4331-4343.
175. Phillips, T., and Leeuwenburgh, C. (2005). Muscle fiber specific apoptosis and TNFalpha signaling in sarcopenia are attenuated by life-long calorie restriction. Faseb J 19, 668-670.
176. Piao, Y.J., Seo, Y.H., Hong, F., Kim, J.H., Kim, Y.J., Kang, M.H., et al. (2005). Nox 2 stimulates muscle differentiation via NF-kappaB/iNOS pathway. Free Radic Biol Med 38, 989-1001.
177. Piccolo, F.M., and Fisher, A.G. (2014). Getting rid of DNA methylation. Trends Cell Biol 24, 136-143.
178. Pokholok, D.K., Zeitlinger, J., Hannett, N.M., Reynolds, D.B., and Young, R.A. (2006). Activated signal transduction kinases frequently occupy target genes. Science 313, 533-536.
179. Polesskaya, A., Seale, P., and Rudnicki, M.A. (2003). Wnt signaling induces the myogenic specification of resident CD45+ adult stem cells during muscle regeneration. Cell 113, 841-852.
180. Potthoff, M.J., and Olson, E.N. (2007). MEF2: a central regulator of diverse developmental programs. Development 134, 4131-4140.
181. Price, F.D., von Maltzahn, J., Bentzinger, C.F., Dumont, N.A., Yin, H., Chang, N.C., et al. (2014). Inhibition of JAK-STAT signaling stimulates adult satellite cell function. Nat Med 20, 1174-1181.
182. Puri, P.L., Iezzi, S., Stiegler, P., Chen, T.T., Schiltz, R.L., Muscat, G.E., et al. (2001). Class I histone deacetylases sequentially interact with MyoD and pRb during skeletal myogenesis. Mol Cell 8, 885-897.
183. Puri, P.L., and Sartorelli, V. (2000). Regulation of muscle regulatory factors by DNAbinding, interacting proteins, and post-transcriptional modifications. J Cell Physiol 185, 155-173.
184. Radley, H.G., Davies, M.J., and Grounds, M.D. (2008). Reduced muscle necrosis and long-term benefits in dystrophic mdx mice after cV1q (blockade of TNF) treatment. Neuromuscul Disord 18, 227-238.
185. Ramirez-Carrozzi, V.R., Braas, D., Bhatt, D.M., Cheng, C.S., Hong, C., Doty, K.R., et al. (2009). A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling. Cell 138, 114-128.
186. Rampalli, S., Li, L., Mak, E., Ge, K., Brand, M., Tapscott, S.J., a et al. (2007). p38 MAPK signaling regulates recruitment of Ash2L-containing methyltransferase complexes to specific genes during differentiation. Nat Struct Mol Biol 14, 1150-1156.
187. Rebbapragada, A., Benchabane, H., Wrana, J.L., Celeste, A.J., and Attisano, L. (2003). Myostatin signals through a transforming growth factor beta-like signaling pathway to block adipogenesis. Mol Cell Biol 23, 7230-7242.
188. Riising, E.M., Comet, I., Leblanc, B., Wu, X., Johansen, J.V., and Helin, K. (2014). Gene silencing triggers polycomb repressive complex 2 recruitment to CpG islands genome wide. Mol Cell 55, 347-360.
189. Rochat, A., Fernandez, A., Vandromme, M., Moles, J.P., Bouschet, T., Carnac, G., et al. (2004). Insulin and wnt1 pathways cooperate to induce reserve cell activation in differentiation and myotube hypertrophy. Mol Biol Cell 15, 4544-4555.
190. Rodgers, J.T., King, K.Y., Brett, J.O., Cromie, M.J., Charville, G.W., Maguire, K.K., et al. (2014). mTORC1 controls the adaptive transition of quiescent stem cells from G0 to G(Alert). Nature 510, 393-396.
191. Saccone, V., Consalvi, S., Giordani, L., Mozzetta, C., Barozzi, I., Sandona, M., et al. (2014). HDAC-regulated myomiRs control BAF60 variant exchange and direct the functional phenotype of fibro-adipogenic progenitors in dystrophic muscles. Genes Dev 28, 841-857.
192. Saha, A., Wittmeyer, J., and Cairns, B.R. (2006). Chromatin remodelling: the industrial revolution of DNA around histones. Nat Rev Mol Cell Biol 7, 437-447.
193. Sartorelli, V., Puri, P.L., Hamamori, Y., Ogryzko, V., Chung, G., Nakatani, Y., et al. (1999). Acetylation of MyoD directed by PCAF is necessary for the execution of the muscle program. Mol Cell 4, 725-734.
194. Schlesinger, Y., Straussman, R., Keshet, I., Farkash, S., Hecht, M., Zimmerman, J., et al. (2007). Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 39, 232-236.
195. Schneider, R., Bannister, A.J., Myers, F.A., Thorne, A.W., Crane-Robinson, C., and Kouzarides, T. (2004). Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat Cell Biol 6, 73-77.
196. Schroeter, E.H., Kisslinger, J.A., and Kopan, R. (1998). Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature 393, 382-386.
197. Seale, P., Sabourin, L.A., Girgis-Gabardo, A., Mansouri, A., Gruss, P., and Rudnicki, M.A. (2000). Pax7 is required for the specification of myogenic satellite cells. Cell 102, 777-786.
198. Segales, J., Perdiguero, E., and Munoz-Canoves, P. (2014). Epigenetic control of adult skeletal muscle stem cell functions. FEBS J.
199. Serra, C., Palacios, D., Mozzetta, C., Forcales, S.V., Morantte, I., Ripani, M., et al. (2007). Functional interdependence at the chromatin level between the MKK6/p38 and IGF1/PI3K/AKT pathways during muscle differentiation. Mol Cell 28, 200-213.
200. Sethi, J.K., and Vidal-Puig, A. (2010). Wnt signalling and the control of cellular metabolism. Biochem J 427, 1-17.
201. Shen, M.M., and Schier, A.F. (2000). The EGF-CFC gene family in vertebrate development. Trends Genet 16, 303-309.
202. Shi, X., Zhang, Z., Zhan, X., Cao, M., Satoh, T., Akira, S., et al. (2014). An epigenetic switch induced by Shh signalling regulates gene activation during development and medulloblastoma growth. Nat Commun 5, 5425.
203. Shinin, V., Gayraud-Morel, B., Gomes, D., and Tajbakhsh, S. (2006). Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol 8, 677-687.
204. Silvagno, F., Xia, H., and Bredt, D.S. (1996). Neuronal nitric-oxide synthase-mu, an alternatively spliced isoform expressed in differentiated skeletal muscle. J Biol Chem 271, 11204-11208.
205. Simone, C., Forcales, S.V., Hill, D.A., Imbalzano, A.N., Latella, L., and Puri, P.L. (2004). p38 pathway targets SWI-SNF chromatin-remodeling complex to musclespecific loci. Nat Genet 36, 738-743.
206. Sinha, M., Jang, Y.C., Oh, J., Khong, D., Wu, E.Y., Manohar, R., et al. (2014). Restoring systemic GDF11 levels reverses age-related dysfunction in mouse skeletal muscle. Science 344, 649-652.
207. Sousa-Victor, P., Gutarra, S., Garcia-Prat, L., Rodriguez-Ubreva, J., Ortet, L., Ruiz- Bonilla, V., et al. (2014). Geriatric muscle stem cells switch reversible quiescence into senescence. Nature 506, 316-321.
208. Sparmann, A., and van Lohuizen, M. (2006). Polycomb silencers control cell fate, development and cancer. Nat Rev Cancer 6, 846-856.
209. Stark, G.R., and Darnell, J.E., Jr. (2012). The JAK-STAT pathway at twenty. Immunity 36, 503-514.
210. Stoick-Cooper, C.L., Moon, R.T., and Weidinger, G. (2007). Advances in signaling in vertebrate regeneration as a prelude to regenerative medicine. Genes Dev 21, 1292-1315.
211. Stojic, L., Jasencakova, Z., Prezioso, C., Stutzer, A., Bodega, B., Pasini, D., et al. (2011). Chromatin regulated interchange between polycomb repressive complex 2 (PRC2)-Ezh2 and PRC2-Ezh1 complexes controls myogenin activation in skeletal muscle cells. Epigenetics Chromatin 4, 16.
212. Straface, G., Aprahamian, T., Flex, A., Gaetani, E., Biscetti, F., Smith, R.C., et al. (2009). Sonic hedgehog regulates angiogenesis and myogenesis during post-natal skeletal muscle regeneration. J Cell Mol Med 13, 2424-2435.
213. Sun, L., Ma, K., Wang, H., Xiao, F., Gao, Y., Zhang, W., et al. (2007). JAK1-STAT1-STAT3, a key pathway promoting proliferation and preventing premature differentiation of myoblasts. J Cell Biol 179, 129-138.
214. Tatsumi, R., Anderson, J.E., Nevoret, C.J., Halevy, O., and Allen, R.E. (1998). HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev Biol 194, 114-128.
215. Tatsumi, R., Hattori, A., Ikeuchi, Y., Anderson, J.E., and Allen, R.E. (2002). Release of hepatocyte growth factor from mechanically stretched skeletal muscle satellite cells and role of pH and nitric oxide. Mol Biol Cell 13, 2909-2918.
216. Tazi, J., and Bird, A. (1990). Alternative chromatin structure at CpG islands. Cell 60, 909-920.
217. Tessarz, P., and Kouzarides, T. (2014). Histone core modifications regulating nucleosome structure and dynamics. Nat Rev Mol Cell Biol 15, 703-708.
218. Tierney, M.T., Aydogdu, T., Sala, D., Malecova, B., Gatto, S., Puri, P.L., et al. (2014). STAT3 signaling controls satellite cell expansion and skeletal muscle repair. Nat Med 20, 1182-1186.
219. Torres, M., and Forman, H.J. (2003). Redox signaling and the MAP kinase pathways. Biofactors 17, 287-296.
220. Tremblay, A.M., and Camargo, F.D. (2012). Hippo signaling in mammalian stem cells. Semin Cell Dev Biol 23, 818-826.
221. Tremblay, A.M., Missiaglia, E., Galli, G.G., Hettmer, S., Urcia, R., Carrara, M., et al. (2014). The Hippo transducer YAP1 transforms activated satellite cells and is a potent effector of embryonal rhabdomyosarcoma formation. Cancer Cell 26, 273-287.
222. Trendelenburg, A.U., Meyer, A., Jacobi, C., Feige, J.N., and Glass, D.J. (2012). TAK- 1/p38/nNFkappaB signaling inhibits myoblast differentiation by increasing levels of Activin A. Skelet Muscle 2, 3.
223. Uezumi, A., Fukada, S., Yamamoto, N., Takeda, S., and Tsuchida, K. (2010). Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat Cell Biol 12, 143-152.
224. Valinluck, V., Tsai, H.H., Rogstad, D.K., Burdzy, A., Bird, A., and Sowers, L.C. (2004). Oxidative damage to methyl-CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2). Nucleic Acids Res 32, 4100-4108.
225. van der Velden, J.L., Langen, R.C., Kelders, M.C., Wouters, E.F., Janssen-Heininger, Y.M., and Schols, A.M. (2006). Inhibition of glycogen synthase kinase-3beta activity is sufficient to stimulate myogenic differentiation. Am J Physiol Cell Physiol 290, C453-462.
226. Vladar, E.K., Antic, D., and Axelrod, J.D. (2009). Planar cell polarity signaling: the developing cell's compass. Cold Spring Harb Perspect Biol 1, a002964.
227. Voigt, P., Tee, W.W., and Reinberg, D. (2013). A double take on bivalent promoters. Genes Dev 27, 1318-1338.
228. Vokes, S.A., Ji, H., Wong, W.H., and McMahon, A.P. (2008). A genome-scale analysis of the cis-regulatory circuitry underlying sonic hedgehog-mediated patterning of the mammalian limb. Genes Dev 22, 2651-2663.
229. von Maltzahn, J., Bentzinger, C.F., and Rudnicki, M.A. (2012a). Wnt7a-Fzd7 signalling directly activates the Akt/mTOR anabolic growth pathway in skeletal muscle. Nat Cell Biol 14, 186-191.
230. von Maltzahn, J., Chang, N.C., Bentzinger, C.F., and Rudnicki, M.A. (2012b). Wnt signaling in myogenesis. Trends Cell Biol 22, 602-609.
231. Wackerhage, H., Del Re, D.P., Judson, R.N., Sudol, M., and Sadoshima, J. (2014). The Hippo signal transduction network in skeletal and cardiac muscle. Sci Signal 7, re4.
232. Wade, P.A. (2005). SWItching off methylated DNA. Nat Genet 37, 212-213.
233. Wang, K., Wang, C., Xiao, F., Wang, H., and Wu, Z. (2008). JAK2/STAT2/STAT3 are required for myogenic differentiation. J Biol Chem 283, 34029-34036.
234. Wang, Y., Shankar, S.R., Kher, D., Ling, B.M., and Taneja, R. (2013). Sumoylation of the basic helix-loop-helix transcription factor sharp-1 regulates recruitment of the histone methyltransferase G9a and function in myogenesis. J Biol Chem 288, 17654-17662.
235. Wang, Y.X., Dumont, N.A., and Rudnicki, M.A. (2014). Muscle stem cells at a glance. J Cell Sci 127, 4543-4548.
236. Watt, K.I., Judson, R., Medlow, P., Reid, K., Kurth, T.B., Burniston, J.G., et al. (2010). Yap is a novel regulator of C2C12 myogenesis. Biochem Biophys Res Commun 393, 619-624.
237. Wen, Y., Bi, P., Liu, W., Asakura, A., Keller, C., and Kuang, S. (2012). Constitutive Notch activation upregulates Pax7 and promotes the self-renewal of skeletal muscle satellite cells. Mol Cell Biol 32, 2300-2311.
238. Winston, F., and Allis, C.D. (1999). The bromodomain: a chromatin-targeting module? Nat Struct Biol 6, 601-604.
239. Wu, Z., Woodring, P.J., Bhakta, K.S., Tamura, K., Wen, F., Feramisco, J.R., et al. (2000). p38 and extracellular signal-regulated kinases regulate the myogenic program at multiple steps. Mol Cell Biol 20, 3951-3964.
240. Yamada, M., Tatsumi, R., Yamanouchi, K., Hosoyama, T., Shiratsuchi, S., Sato, A., et al. (2010). High concentrations of HGF inhibit skeletal muscle satellite cell proliferation in vitro by inducing expression of myostatin: a possible mechanism for reestablishing satellite cell quiescence in vivo. Am J Physiol Cell Physiol 298, C465-476.
241. Yu, F.X., and Guan, K.L. (2013). The Hippo pathway: regulators and regulations. Genes Dev 27, 355-371.
242. Yu, F.X., Zhao, B., Panupinthu, N., Jewell, J.L., Lian, I., Wang, L.H., et al. (2012). Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 150, 780-791.
243. Zaccagnini, G., Martelli, F., Magenta, A., Cencioni, C., Fasanaro, P., Nicoletti, C., et al. (2007). p66(ShcA) and oxidative stress modulate myogenic differentiation and skeletal muscle regeneration after hind limb ischemia. J Biol Chem 282, 31453-31459.
244. Zetser, A., Gredinger, E., and Bengal, E. (1999). p38 mitogen-activated protein kinase pathway promotes skeletal muscle differentiation. Participation of the Mef2c transcription factor. J Biol Chem 274, 5193-5200.
245. Zhu, S., Goldschmidt-Clermont, P.J., and Dong, C. (2004). Transforming growth factor-beta-induced inhibition of myogenesis is mediated through Smad pathway and is modulated by microtubule dynamic stability. Circ Res 94, 617-625.
246. Zykovich, A., Hubbard, A., Flynn, J.M., Tarnopolsky, M., Fraga, M.F., Kerksick, C., et al. (2014). Genome-wide DNA methylation changes with age in disease-free human skeletal muscle. Aging Cell 13, 360-366.