Myogenesis in the Genomics Era

Journal of Molecular Biology

Volumn 427, Issue 11, 2015, Pages 2023-2038

  Blais, Alexandre ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

chromatin structure; epigenetics; myogenesis; transcription factors; transcriptional regulatory network

Indexed keywords

TRANSCRIPTION FACTOR;

ANIMAL; EPIGENETICS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MUSCLE DEVELOPMENT; PHYSIOLOGY; PROCEDURES; SKELETAL MUSCLE;

ANIMALS; EPIGENOMICS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOMICS; HUMANS; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; TRANSCRIPTION FACTORS;

EID: 84937511084     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.02.009     Document Type: Review

References (161)

1. M. Buckingham Skeletal muscle formation in vertebrates Curr Opin Genet Dev 11 2001 440 448
2. R.J. Bryson-Richardson, and P.D. Currie The genetics of vertebrate myogenesis Nat Rev Genet 9 2008 632 646 10.1038/nrg2369
3. M. Buckingham, and S.D. Vincent Distinct and dynamic myogenic populations in the vertebrate embryo Curr Opin Genet Dev 19 2009 444 453 10.1016/j.gde.2009.08.001
4. D. Montarras, A. L'honore, and M. Buckingham Lying low but ready for action: the quiescent muscle satellite cell FEBS J 280 2013 4036 4050 10.1111/febs.12372
5. N.C. Chang, and M.A. Rudnicki Satellite cells: the architects of skeletal muscle Curr Top Dev Biol 107 2014 161 181 10.1016/B978-0-12-416022-4.00006-8
6. A. Mauro Satellite cell of skeletal muscle fibers J Biophys Biochem Cytol 9 1961 493 495
7. R.B. White, A.S. Bierinx, V.F. Gnocchi, and P.S. Zammit Dynamics of muscle fibre growth during postnatal mouse development BMC Dev Biol 10 2010 10.1186/1471-213X-10-21
8. X. Shen, J.M. Collier, M. Hlaing, L. Zhang, E.H. Delshad, and J. Bristow Genome-wide examination of myoblast cell cycle withdrawal during differentiation Dev Dyn 226 2003 128 138 10.1002/dvdy.10200
9. F.J. Dilworth, and A. Blais Epigenetic regulation of satellite cell activation during muscle regeneration Stem Cell Res Ther 2 2011 18 10.1186/scrt59
10. S.L. Berger The complex language of chromatin regulation during transcription Nature 447 2007 407 412 10.1038/nature05915
11. C.A. Berkes, and S.J. Tapscott MyoD and the transcriptional control of myogenesis Semin Cell Dev Biol 16 2005 585 595
12. R.L. Davis, H. Weintraub, and A.B. Lassar Expression of a single transfected cDNA converts fibroblasts to myoblasts Cell 51 1987 987 1000
13. S.J. Tapscott, R.L. Davis, M.J. Thayer, P.F. Cheng, H. Weintraub, and A.B. Lassar MyoD1: a nuclear phosphoprotein requiring a Myc homology region to convert fibroblasts to myoblasts Science 242 1988 405 411
14. Y. Liu, A. Chu, I. Chakroun, U. Islam, and A. Blais Cooperation between myogenic regulatory factors and SIX family transcription factors is important for myoblast differentiation Nucleic Acids Res 38 2010 6857 6871 10.1093/nar/gkq585
15. C.A. Berkes, D.A. Bergstrom, B.H. Penn, K.J. Seaver, P.S. Knoepfler, and S.J. Tapscott Pbx marks genes for activation by MyoD indicating a role for a homeodomain protein in establishing myogenic potential Mol Cell 14 2004 465 477
16. D.G. Edmondson, T.C. Cheng, P. Cserjesi, T. Chakraborty, and E.N. Olson Analysis of the myogenin promoter reveals an indirect pathway for positive autoregulation mediated by the muscle-specific enhancer factor MEF-2 Mol Cell Biol 12 1992 3665 3677
17. Y.T. Yu, R.E. Breitbart, L.B. Smoot, Y. Lee, V. Mahdavi, and B. Nadal-Ginard Human myocyte-specific enhancer factor 2 comprises a group of tissue-restricted MADS box transcription factors Genes Dev 6 1992 1783 1798
18. N. Daou, S. Lecolle, S. Lefebvre, B. della Gaspera, F. Charbonnier, and C. Chanoine A new role for the calcineurin/NFAT pathway in neonatal myosin heavy chain expression via the NFATc2/MyoD complex during mouse myogenesis Development 140 2013 4914 4925 10.1242/dev.097428
19. A.S. Armand, M. Bourajjaj, S. Martinez-Martinez, H. el Azzouzi, P.A. da Costa Martins, and P. Hatzis Cooperative synergy between NFAT and MyoD regulates myogenin expression and myogenesis J Biol Chem 283 2008 29004 29010 10.1074/jbc.M801297200
20. M. Buckingham, and P.W. Rigby Gene regulatory networks and transcriptional mechanisms that control myogenesis Dev Cell 28 2014 225 238 10.1016/j.devcel.2013.12.020
21. S. Tajbakhsh, D. Rocancourt, G. Cossu, and M. Buckingham Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD Cell 89 1997 127 138
22. F. Relaix, D. Montarras, S. Zaffran, B. Gayraud-Morel, D. Rocancourt, and S. Tajbakhsh Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells J Cell Biol 172 2006 91 102 10.1083/jcb.200508044
23. A. L'honore, J.F. Ouimette, M. Lavertu-Jolin, and J. Drouin Pitx2 defines alternate pathways acting through MyoD during limb and somitic myogenesis Development 137 2010 3847 3856 10.1242/dev.053421
24. G. Messina, S. Biressi, S. Monteverde, A. Magli, M. Cassano, and L. Perani Nfix regulates fetal-specific transcription in developing skeletal muscle Cell 140 2010 554 566 10.1016/j.cell.2010.01.027
25. P. Seale, L.A. Sabourin, A. Girgis-Gabardo, A. Mansouri, P. Gruss, and M.A. Rudnicki Pax7 is required for the specification of myogenic satellite cells Cell 102 2000 777 786
26. R. Sambasivan, R. Yao, A. Kissenpfennig, L. Van Wittenberghe, A. Paldi, and B. Gayraud-Morel Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration Development 138 2011 3647 3656 10.1242/dev.067587
27. C. Lepper, T.A. Partridge, and C.M. Fan An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration Development 138 2011 3639 3646 10.1242/dev.067595
28. J. von Maltzahn, A.E. Jones, R.J. Parks, and M.A. Rudnicki Pax7 is critical for the normal function of satellite cells in adult skeletal muscle Proc Natl Acad Sci U S A 110 2013 16474 16479 10.1073/pnas.1307680110
29. S. Gunther, J. Kim, S. Kostin, C. Lepper, C.M. Fan, and T. Braun Myf5-positive satellite cells contribute to Pax7-dependent long-term maintenance of adult muscle stem cells Cell Stem Cell 13 2013 590 601 10.1016/j.stem.2013.07.016
30. T. Ryan, J. Liu, A. Chu, L. Wang, A. Blais, and I.S. Skerjanc Retinoic acid enhances skeletal myogenesis in human embryonic stem cells by expanding the premyogenic progenitor population Stem Cell Rev 8 2012 482 493 10.1007/s12015-011-9284-0
31. M. Shelton, J. Metz, J. Liu, R.L. Carpenedo, S.P. Demers, and W.L. Stanford Derivation and expansion of PAX7-positive muscle progenitors from human and mouse embryonic stem cells Stem Cell Rep 3 2014 516 529 10.1016/j.stemcr.2014.07.001
32. A. Voronova, E. Coyne, A. Al Madhoun, J.V. Fair, N. Bosiljcic, and C. St-Louis Hedgehog signaling regulates MyoD expression and activity J Biol Chem 288 2013 4389 4404 10.1074/jbc.M112.400184
33. J. Wong, V. Mehta, A. Voronova, J. Coutu, T. Ryan, and M. Shelton beta-Catenin is essential for efficient in vitro premyogenic mesoderm formation but can be partially compensated by retinoic acid signalling PLoS One 8 2013 e57501 10.1371/journal.pone.0057501
34. R. Darabi, and R.C. Perlingeiro Derivation of skeletal myogenic precursors from human pluripotent stem cells using conditional expression of PAX7 Methods Mol Biol 2014 10.1007/7651-2014-134
35. A. Magli, E. Schnettler, S.A. Swanson, L. Borges, K. Hoffman, and R. Stewart Pax3 and Tbx5 specify whether PDGFRalpha + cells assume skeletal or cardiac muscle fate in differentiating embryonic stem cells Stem Cells 32 2014 2072 2083 10.1002/stem.1713
36. M.S. Hickey, J.O. Carey, J.L. Azevedo, J.A. Houmard, W.J. Pories, and R.G. Israel Skeletal muscle fiber composition is related to adiposity and in vitro glucose transport rate in humans Am J Physiol 268 1995 E453 E457
37. D.E. Kelley, J. He, E.V. Menshikova, and V.B. Ritov Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes Diabetes 51 2002 2944 2950
38. M.F. Gerrits, S. Ghosh, N. Kavaslar, B. Hill, A. Tour, and E.L. Seifert Distinct skeletal muscle fiber characteristics and gene expression in diet-sensitive versus diet-resistant obesity J Lipid Res 51 2010 2394 2404 10.1194/jlr.P005298
39. J.E. Silva Thyroid hormone control of thermogenesis and energy balance Thyroid 5 1995 481 492
40. M. Schena, D. Shalon, R.W. Davis, and P.O. Brown Quantitative monitoring of gene expression patterns with a complementary DNA microarray Science 270 1995 467 470
41. T. Ideker, T. Galitski, and L. Hood A new approach to decoding life: systems biology Annu Rev Genomics Hum Genet 2 2001 343 372 10.1146/annurev.genom.2.1.343
42. D. Yaffe, and O. Saxel Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle Nature 270 1977 725 727
43. H.M. Blau, C.P. Chiu, and C. Webster Cytoplasmic activation of human nuclear genes in stable heterocaryons Cell 32 1983 1171 1180
44. K.V. Pajcini, S.Y. Corbel, J. Sage, J.H. Pomerantz, and H.M. Blau Transient inactivation of Rb and ARF yields regenerative cells from postmitotic mammalian muscle Cell Stem Cell 7 2010 198 213 10.1016/j.stem.2010.05.022
45. J.L. Moran, Y. Li, A.A. Hill, W.M. Mounts, and C.P. Miller Gene expression changes during mouse skeletal myoblast differentiation revealed by transcriptional profiling Physiol Genomics 10 2002 103 111
46. Z. Yan, S. Choi, X. Liu, M. Zhang, J.J. Schageman, and S.Y. Lee Highly coordinated gene regulation in mouse skeletal muscle regeneration J Biol Chem 278 2003 8826 8836 10.1074/jbc.M209879200
47. L. Liu, T.H. Cheung, G.W. Charville, B.M. Hurgo, T. Leavitt, and J. Shih Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging Cell Rep 4 2013 189 204 10.1016/j.celrep.2013.05.043
48. A. Mortazavi, B.A. Williams, K. McCue, L. Schaeffer, and B. Wold Mapping and quantifying mammalian transcriptomes by RNA-Seq Nat Methods 5 2008 621 628 10.1038/nmeth.1226
49. C. Trapnell, B.A. Williams, G. Pertea, A. Mortazavi, G. Kwan, and M.J. van Baren Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation Nat Biotechnol 28 2010 511 515 10.1038/nbt.1621
50. S. Sebastian, H. Faralli, Z. Yao, P. Rakopoulos, C. Palii, and Y. Cao Tissue-specific splicing of a ubiquitously expressed transcription factor is essential for muscle differentiation Genes Dev 27 2013 1247 1259 10.1101/gad.215400.113
51. K. Mousavi, H. Zare, S. Dell'orso, L. Grontved, G. Gutierrez-Cruz, and A. Derfoul eRNAs promote transcription by establishing chromatin accessibility at defined genomic loci Mol Cell 51 2013 606 617 10.1016/j.molcel.2013.07.022
52. A.C. Mueller, M.A. Cichewicz, B.K. Dey, R. Layer, B.J. Reon, and J.R. Gagan MUNC, a long noncoding RNA that facilitates the function of MyoD in skeletal myogenesis Mol Cell Biol 35 2015 498 513 10.1128/MCB.01079-14
53. G. Sohi, and F.J. Dilworth Non-coding RNAs as epigenetic mediators of skeletal muscle regeneration FEBS J 2014 10.1111/febs.13170
54. M. Ballarino, V. Cazzella, D. D'Andrea, L. Grassi, L. Bisceglie, and A. Cipriano Novel long noncoding RNAs (lncRNAs) in myogenesis: a miR-31 overlapping lncRNA transcript controls myoblast differentiation Mol Cell Biol 35 2015 728 736 10.1128/MCB.01394-14
55. G. Pallafacchina, S. Francois, B. Regnault, B. Czarny, V. Dive, and A. Cumano An adult tissue-specific stem cell in its niche: a gene profiling analysis of in vivo quiescent and activated muscle satellite cells Stem Cell Res 4 2009 77 91
56. S. Fukada, A. Uezumi, M. Ikemoto, S. Masuda, M. Segawa, and N. Tanimura Molecular signature of quiescent satellite cells in adult skeletal muscle Stem Cells 25 2007 2448 2459 10.1634/stemcells.2007-0019
57. E. Segal, M. Shapira, A. Regev, D. Pe'er, D. Botstein, and D. Koller Module networks: identifying regulatory modules and their condition-specific regulators from gene expression data Nat Genet 34 2003 166 176
58. C. Wang, J. Xuan, L. Chen, P. Zhao, Y. Wang, and R. Clarke Motif-directed network component analysis for regulatory network inference BMC Bioinforma 9 2008 10.1186/1471-2105-9-S1-S21
59. T. Gong, J. Xuan, C. Wang, H. Li, E. Hoffman, and R. Clarke Gene module identification from microarray data using nonnegative independent component analysis Gene Regul Syst Biol 1 2008 349 363
60. T.M. Kim, Y.J. Chung, M.G. Rhyu, and M.H. Jung Inferring biological functions and associated transcriptional regulators using gene set expression coherence analysis BMC Bioinforma 8 2007 453 10.1186/1471-2105-8-453
61. D. Perez-Montarelo, N.J. Hudson, A.I. Fernandez, Y. Ramayo-Caldas, B.P. Dalrymple, and A. Reverter Porcine tissue-specific regulatory networks derived from meta-analysis of the transcriptome PLoS One 7 2012 e46159 10.1371/journal.pone.0046159
62. N.J. Hudson, A. Reverter, Y. Wang, P.L. Greenwood, and B.P. Dalrymple Inferring the transcriptional landscape of bovine skeletal muscle by integrating co-expression networks PLoS One 4 2009 e7249 10.1371/journal.pone.0007249
63. D.A. Bergstrom, B.H. Penn, A. Strand, R.L. Perry, M.A. Rudnicki, and S.J. Tapscott Promoter-specific regulation of MyoD binding and signal transduction cooperate to pattern gene expression Mol Cell 9 2002 587 600
64. C. Niro, J. Demignon, S. Vincent, Y. Liu, J. Giordani, and N. Sgarioto Six1 and Six4 gene expression is necessary to activate the fast-type muscle gene program in the mouse primary myotome Dev Biol 338 2009 168 182
65. M.J. Potthoff, M.A. Arnold, J. McAnally, J.A. Richardson, R. Bassel-Duby, and E.N. Olson Regulation of skeletal muscle sarcomere integrity and postnatal muscle function by Mef2c Mol Cell Biol 27 2007 8143 8151 10.1128/MCB.01187-07
66. X. Wang, C. Blagden, J. Fan, S.J. Nowak, I. Taniuchi, and D.R. Littman Runx1 prevents wasting, myofibrillar disorganization, and autophagy of skeletal muscle Genes Dev 19 2005 1715 1722 10.1101/gad.1318305
67. M. Lagha, T. Sato, B. Regnault, A. Cumano, A. Zuniga, and J. Licht Transcriptome analyses based on genetic screens for Pax3 myogenic targets in the mouse embryo BMC Genomics 11 2010 10.1186/1471-2164-11-696
68. R.N. Judson, A.M. Tremblay, P. Knopp, R.B. White, R. Urcia, and C. De Bari The Hippo pathway member Yap plays a key role in influencing fate decisions in muscle satellite cells J Cell Sci 125 2012 6009 6019 10.1242/jcs.109546
69. B. Ren, F. Robert, J.J. Wyrick, O. Aparicio, E.G. Jennings, and I. Simon Genome-wide location and function of DNA binding proteins Science 290 2000 2306 2309
70. D.S. Johnson, A. Mortazavi, R.M. Myers, and B. Wold Genome-wide mapping of in vivo protein-DNA interactions Science 316 2007 1497 1502 10.1126/science.1141319
71. S. Impey, S.R. McCorkle, H. Cha-Molstad, J.M. Dwyer, G.S. Yochum, and J.M. Boss Defining the CREB regulon: a genome-wide analysis of transcription factor regulatory regions Cell 119 2004 1041 1054 10.1016/j.cell.2004.10.032
72. A. Blais, M. Tsikitis, D. Acosta-Alvear, R. Sharan, Y. Kluger, and B.D. Dynlacht An initial blueprint for myogenic differentiation Genes Dev 19 2005 553 569
73. Y. Cao, R.M. Kumar, B.H. Penn, C.A. Berkes, C. Kooperberg, and L.A. Boyer Global and gene-specific analyses show distinct roles for Myod and Myog at a common set of promoters EMBO J 25 2006 502 511
74. W.W. Wasserman, and A. Sandelin Applied bioinformatics for the identification of regulatory elements Nat Rev Genet 5 2004 276 287 10.1038/nrg1315
75. Y. Cao, Z. Yao, D. Sarkar, M. Lawrence, G.J. Sanchez, and M.H. Parker Genome-wide MyoD binding in skeletal muscle cells: a potential for broad cellular reprogramming Dev Cell 18 2010 662 674
76. S. Seenundun, S. Rampalli, Q.C. Liu, A. Aziz, C. Palii, and S. Hong UTX mediates demethylation of H3K27me3 at muscle-specific genes during myogenesis EMBO J 29 2010 1401 1411
77. Y. Liu, I. Chakroun, D. Yang, E. Horner, J. Liang, and A. Aziz Six1 regulates MyoD expression in adult muscle progenitor cells PLoS One 8 2013 e67762 10.1371/journal.pone.0067762
78. S. Rampalli, L. Li, E. Mak, K. Ge, M. Brand, and S.J. Tapscott p38 MAPK signaling regulates recruitment of Ash2L-containing methyltransferase complexes to specific genes during differentiation Nat Struct Mol Biol 14 2007 1150 1156 10.1038/nsmb1316
79. A. Benhaddou, C. Keime, T. Ye, A. Morlon, I. Michel, and B. Jost Transcription factor TEAD4 regulates expression of myogenin and the unfolded protein response genes during C2C12 cell differentiation Cell Death Differ 19 2012 220 231 10.1038/cdd.2011.87
80. T. Maeda, D.L. Chapman, and A.F. Stewart Mammalian vestigial-like 2, a cofactor of TEF-1 and MEF2 transcription factors that promotes skeletal muscle differentiation J Biol Chem 277 2002 48889 48898 10.1074/jbc.M206858200
81. V.D. Soleimani, H. Yin, A. Jahani-Asl, H. Ming, C.E. Kockx, and W.F. van Ijcken Snail regulates MyoD binding-site occupancy to direct enhancer switching and differentiation-specific transcription in myogenesis Mol Cell 47 2012 457 468 10.1016/j.molcel.2012.05.046
82. S. Kuang, S.B. Charge, P. Seale, M. Huh, and M.A. Rudnicki Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis J Cell Biol 172 2006 103 113
83. V.D. Soleimani, V.G. Punch, Y. Kawabe, A.E. Jones, G.A. Palidwor, and C.J. Porter Transcriptional dominance of Pax7 in adult myogenesis is due to high-affinity recognition of homeodomain motifs Dev Cell 22 2012 1208 1220 10.1016/j.devcel.2012.03.014
84. P. Asp, R. Blum, V. Vethantham, F. Parisi, M. Micsinai, and J. Cheng Genome-wide remodeling of the epigenetic landscape during myogenic differentiation Proc Natl Acad Sci U S A 108 2011 E149 E158 10.1073/pnas.1102223108
85. V. Vethantham, Y. Yang, C. Bowman, P. Asp, J.H. Lee, and D.G. Skalnik Dynamic loss of H2B ubiquitylation without corresponding changes in H3K4 trimethylation during myogenic differentiation Mol Cell Biol 32 2012 1044 1055 10.1128/MCB.06026-11
86. R. Blum, V. Vethantham, C. Bowman, M. Rudnicki, and B.D. Dynlacht Genome-wide identification of enhancers in skeletal muscle: the role of MyoD1 Genes Dev 26 2012 2763 2779 10.1101/gad.200113.112
87. J. Cheng, R. Blum, C. Bowman, D. Hu, A. Shilatifard, and S. Shen A role for H3K4 monomethylation in gene repression and partitioning of chromatin readers Mol Cell 53 2014 979 992 10.1016/j.molcel.2014.02.032
88. Y. Tao, R.L. Neppl, Z.P. Huang, J. Chen, R.H. Tang, and R. Cao The histone methyltransferase Set7/9 promotes myoblast differentiation and myofibril assembly J Cell Biol 194 2011 551 565 10.1083/jcb.201010090
89. J.E. Lee, C. Wang, S. Xu, Y.W. Cho, L. Wang, and X. Feng H3K4 mono- and di-methyltransferase MLL4 is required for enhancer activation during cell differentiation Elife 2 2013 e01503 10.7554/eLife.01503
90. G. Caretti, M. Di Padova, B. Micales, G.E. Lyons, and V. Sartorelli The Polycomb Ezh2 methyltransferase regulates muscle gene expression and skeletal muscle differentiation Genes Dev 18 2004 2627 2638
91. L. Lu, K. Sun, X. Chen, Y. Zhao, L. Wang, and L. Zhou Genome-wide survey by ChIP-seq reveals YY1 regulation of lincRNAs in skeletal myogenesis EMBO J 32 2013 2575 2588 10.1038/emboj.2013.182
92. A.H. Wang, H. Zare, K. Mousavi, C. Wang, C.E. Moravec, and H.I. Sirotkin The histone chaperone Spt6 coordinates histone H3K27 demethylation and myogenesis EMBO J 32 2013 1075 1086 10.1038/emboj.2013.54
93. F. Lan, P.E. Bayliss, J.L. Rinn, J.R. Whetstine, J.K. Wang, and S. Chen A histone H3 lysine 27 demethylase regulates animal posterior development Nature 449 2007 689 694
94. P.L. Puri, and M. Mercola BAF60 A, B, and Cs of muscle determination and renewal Genes Dev 26 2012 2673 2683 10.1101/gad.207415.112
95. D.C. Hargreaves, and G.R. Crabtree ATP-dependent chromatin remodeling: genetics, genomics and mechanisms Cell Res 21 2011 396 420 10.1038/cr.2011.32
96. J.A. Lessard, and G.R. Crabtree Chromatin regulatory mechanisms in pluripotency Annu Rev Cell Dev Biol 26 2010 503 532 10.1146/annurev-cellbio-051809-102012
97. I.L. de la Serna, Y. Ohkawa, C.A. Berkes, D.A. Bergstrom, C.S. Dacwag, and S.J. Tapscott MyoD targets chromatin remodeling complexes to the myogenin locus prior to forming a stable DNA-bound complex Mol Cell Biol 25 2005 3997 4009 10.1128/MCB.25.10.3997-4009.2005
98. S.V. Forcales, S. Albini, L. Giordani, B. Malecova, L. Cignolo, and A. Chernov Signal-dependent incorporation of MyoD-BAF60c into Brg1-based SWI/SNF chromatin-remodelling complex EMBO J 31 2012 301 316 10.1038/emboj.2011.391
99. A.P. Boyle, S. Davis, H.P. Shulha, P. Meltzer, E.H. Margulies, and Z. Weng High-resolution mapping and characterization of open chromatin across the genome Cell 132 2008 311 322 10.1016/j.cell.2007.12.014
100. K.J. Gaulton, T. Nammo, L. Pasquali, J.M. Simon, P.G. Giresi, and M.P. Fogarty A map of open chromatin in human pancreatic islets Nat Genet 42 2010 255 259 10.1038/ng.530
101. J.D. Buenrostro, P.G. Giresi, L.C. Zaba, H.Y. Chang, and W.J. Greenleaf Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position Nat Methods 10 2013 1213 1218 10.1038/nmeth.2688
102. C. Jin, C. Zang, G. Wei, K. Cui, W. Peng, and K. Zhao H3.3/H2A.Z double variant-containing nucleosomes mark "nucleosome-free regions" of active promoters and other regulatory regions Nat Genet 41 2009 941 945 10.1038/ng.409
103. P. Chen, J. Zhao, Y. Wang, M. Wang, H. Long, and D. Liang H3.3 actively marks enhancers and primes gene transcription via opening higher-ordered chromatin Genes Dev 27 2013 2109 2124 10.1101/gad.222174.113
104. A. Harada, S. Okada, D. Konno, J. Odawara, T. Yoshimi, and S. Yoshimura Chd2 interacts with H3.3 to determine myogenic cell fate EMBO J 31 2012 2994 3007 10.1038/emboj.2012.136
105. C.M. Weber, S. Ramachandran, and S. Henikoff Nucleosomes are context-specific, H2A.Z-modulated barriers to RNA polymerase Mol Cell 53 2014 819 830 10.1016/j.molcel.2014.02.014
106. N. Gevry, H.M. Chan, L. Laflamme, D.M. Livingston, and L. Gaudreau p21 transcription is regulated by differential localization of histone H2A.Z Genes Dev 21 2007 1869 1881 10.1101/gad.1545707
107. M.M. Wong, L.K. Cox, and J.C. Chrivia The chromatin remodeling protein, SRCAP, is critical for deposition of the histone variant H2A.Z at promoters J Biol Chem 282 2007 26132 26139 10.1074/jbc.M703418200
108. A. Cuadrado, N. Corrado, E. Perdiguero, V. Lafarga, P. Munoz-Canoves, and A.R. Nebreda Essential role of p18Hamlet/SRCAP-mediated histone H2A.Z chromatin incorporation in muscle differentiation EMBO J 29 2010 2014 2025 10.1038/emboj.2010.85
109. R.P. Zinzen, C. Girardot, J. Gagneur, M. Braun, and E.E. Furlong Combinatorial binding predicts spatiooral cis-regulatory activity Nature 462 2009 65 70
110. D.Y. Rhee, D.Y. Cho, B. Zhai, M. Slattery, L. Ma, and J. Mintseris Transcription factor networks in Drosophila melanogaster Cell Rep 8 2014 2031 2043 10.1016/j.celrep.2014.08.038
111. G. Junion, M. Spivakov, C. Girardot, M. Braun, E.H. Gustafson, and E. Birney A transcription factor collective defines cardiac cell fate and reflects lineage history Cell 148 2012 473 486 10.1016/j.cell.2012.01.030
112. B. Wilczynski, Y.H. Liu, Z.X. Yeo, and E.E. Furlong Predicting spatial and temporal gene expression using an integrative model of transcription factor occupancy and chromatin state PLoS Comput Biol 8 2012 e1002798 10.1371/journal.pcbi.1002798
113. D. Marbach, S. Roy, F. Ay, P.E. Meyer, R. Candeias, and T. Kahveci Predictive regulatory models in Drosophila melanogaster by integrative inference of transcriptional networks Genome Res 22 2012 1334 1349 10.1101/gr.127191.111
114. modENCODE Consortium S. Roy, J. Ernst, P.V. Kharchenko, P. Kheradpour, and N. Negre Identification of functional elements and regulatory circuits by Drosophila modENCODE Science 330 2010 1787 1797 10.1126/science.1198374
115. M.B. Gerstein, Z.J. Lu, E.L. Van Nostrand, C. Cheng, B.I. Arshinoff, and T. Liu Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project Science 330 2010 1775 1787 10.1126/science.1196914
116. E.L. Van Nostrand, and S.K. Kim Integrative analysis of C. elegans modENCODE ChIP-seq data sets to infer gene regulatory interactions Genome Res 23 2013 941 953 10.1101/gr.152876.112
117. H. Chen, and V. VanBuren A provisional gene regulatory atlas for mouse heart development PLoS One 9 2014 e83364 10.1371/journal.pone.0083364
118. M. Sasai, Y. Kawabata, K. Makishi, K. Itoh, and T.P. Terada Time scales in epigenetic dynamics and phenotypic heterogeneity of embryonic stem cells PLoS Comput Biol 9 2013 e1003380 10.1371/journal.pcbi.1003380
119. E. Walker, M. Ohishi, R.E. Davey, W. Zhang, P.A. Cassar, and T.S. Tanaka Prediction and testing of novel transcriptional networks regulating embryonic stem cell self-renewal and commitment Cell Stem Cell 1 2007 71 86 10.1016/j.stem.2007.04.002
120. S.J. Burden Building the vertebrate neuromuscular synapse J Neurobiol 53 2002 501 511
121. C.F. Bentzinger, Y.X. Wang, J. von Maltzahn, and M.A. Rudnicki The emerging biology of muscle stem cells: implications for cell-based therapies Bioessays 35 2013 231 241 10.1002/bies.201200063
122. T.A. Rando, and H.M. Blau Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy J Cell Biol 125 1994 1275 1287
123. C.F. Bentzinger, Y.X. Wang, N.A. Dumont, and M.A. Rudnicki Cellular dynamics in the muscle satellite cell niche EMBO Rep 14 2013 1062 1072 10.1038/embor.2013.182
124. S. Biressi, and T.A. Rando Heterogeneity in the muscle satellite cell population Semin Cell Dev Biol 21 2010 845 854 10.1016/j.semcdb.2010.09.003
125. N. Motohashi, and A. Asakura Muscle satellite cell heterogeneity and self-renewal Front Cell Dev Biol 2 2014 1 10.3389/fcell.2014.00001
126. C. Trapnell, D. Cacchiarelli, J. Grimsby, P. Pokharel, S. Li, and M. Morse The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells Nat Biotechnol 32 2014 381 386 10.1038/nbt.2859
127. S. Picelli, A.K. Bjorklund, O.R. Faridani, S. Sagasser, G. Winberg, and R. Sandberg Smart-seq2 for sensitive full-length transcriptome profiling in single cells Nat Methods 10 2013 1096 1098 10.1038/nmeth.2639
128. A.K. Shalek, R. Satija, X. Adiconis, R.S. Gertner, J.T. Gaublomme, and R. Raychowdhury Single-cell transcriptomics reveals bimodality in expression and splicing in immune cells Nature 498 2013 236 240 10.1038/nature12172
129. S.R. Hough, M. Thornton, E. Mason, J.C. Mar, C.A. Wells, and M.F. Pera Single-cell gene expression profiles define self-renewing, pluripotent, and lineage primed states of human pluripotent stem cells Stem Cell Rep 2 2014 881 895 10.1016/j.stemcr.2014.04.014
130. J.H. Lee, E.R. Daugharthy, J. Scheiman, R. Kalhor, J.L. Yang, and T.C. Ferrante Highly multiplexed subcellular RNA sequencing in situ Science 343 2014 1360 1363 10.1126/science.1250212
131. A. Blais, C.J. van Oevelen, R. Margueron, D. Acosta-Alvear, and B.D. Dynlacht Retinoblastoma tumor suppressor protein-dependent methylation of histone H3 lysine 27 is associated with irreversible cell cycle exit J Cell Biol 179 2007 1399 1412
132. A.C. Mullen, D.A. Orlando, J.J. Newman, J. Loven, R.M. Kumar, and S. Bilodeau Master transcription factors determine cell-type-specific responses to TGF-beta signaling Cell 147 2011 565 576 10.1016/j.cell.2011.08.050
133. Z. Yao, A.P. Fong, Y. Cao, W.L. Ruzzo, R.C. Gentleman, and S.J. Tapscott Comparison of endogenous and overexpressed MyoD shows enhanced binding of physiologically bound sites Skelet Muscle 3 2013 10.1186/2044-5040-3-8
134. A.P. Fong, Z. Yao, J.W. Zhong, Y. Cao, W.L. Ruzzo, and R.C. Gentleman Genetic and epigenetic determinants of neurogenesis and myogenesis Dev Cell 22 2012 721 735 10.1016/j.devcel.2012.01.015
135. J. Wang, R.M. Kumar, V.J. Biggs, H. Lee, Y. Chen, and M.H. Kagey The Msx1 homeoprotein recruits polycomb to the nuclear periphery during development Dev Cell 21 2011 575 588 10.1016/j.devcel.2011.07.003
136. P. Asp, D. Acosta-Alvear, M. Tsikitis, C. van Oevelen, and B.D. Dynlacht E2f3b plays an essential role in myogenic differentiation through isoform-specific gene regulation Genes Dev 23 2009 37 53 10.1101/gad.1727309
137. K.L. MacQuarrie, Z. Yao, A.P. Fong, S.J. Diede, E.R. Rudzinski, and D.S. Hawkins Comparison of genome-wide binding of MyoD in normal human myogenic cells and rhabdomyosarcomas identifies regional and local suppression of promyogenic transcription factors Mol Cell Biol 33 2013 773 784 10.1128/MCB.00916-12
138. K.L. Macquarrie, Z. Yao, A.P. Fong, and S.J. Tapscott Genome-wide binding of the basic helix-loop-helix myogenic inhibitor musculin has substantial overlap with MyoD: implications for buffering activity Skelet Muscle 3 2013 10.1186/2044-5040-3-26
139. K. Mousavi, H. Zare, A.H. Wang, and V. Sartorelli Polycomb protein Ezh1 promotes RNA polymerase II elongation Mol Cell 45 2012 255 262 10.1016/j.molcel.2011.11.019
140. C. van Oevelen, C. Bowman, J. Pellegrino, P. Asp, J. Cheng, and F. Parisi The mammalian Sin3 proteins are required for muscle development and sarcomere specification Mol Cell Biol 2010 10.1128/MCB.00975-10
141. B. Gayraud-Morel, F. Chretien, A. Jory, R. Sambasivan, E. Negroni, and P. Flamant Myf5 haploinsufficiency reveals distinct cell fate potentials for adult skeletal muscle stem cells J Cell Sci 125 2012 1738 1749 10.1242/jcs.097006
142. D. Montarras, J. Morgan, C. Collins, F. Relaix, S. Zaffran, and A. Cumano Direct isolation of satellite cells for skeletal muscle regeneration Science 309 2005 2064 2067
143. R. Sambasivan, B. Gayraud-Morel, G. Dumas, C. Cimper, S. Paisant, and R.G. Kelly Distinct regulatory cascades govern extraocular and pharyngeal arch muscle progenitor cell fates Dev Cell 16 2009 810 821 10.1016/j.devcel.2009.05.008
144. D. Bosnakovski, Z. Xu, W. Li, S. Thet, O. Cleaver, and R.C. Perlingeiro Prospective isolation of skeletal muscle stem cells with a Pax7 reporter Stem Cells 26 2008 3194 3204 10.1634/stemcells.2007-1017
145. T.S. Moon, C. Lou, A. Tamsir, B.C. Stanton, and C.A. Voigt Genetic programs constructed from layered logic gates in single cells Nature 491 2012 249 253 10.1038/nature11516
146. S. Cabantous, T.C. Terwilliger, and G.S. Waldo Protein tagging and detection with engineered self-assembling fragments of green fluorescent protein Nat Biotechnol 23 2005 102 107 10.1038/nbt1044
147. S. Bonn, R.P. Zinzen, A. Perez-Gonzalez, A. Riddell, A.C. Gavin, and E.E. Furlong Cell type-specific chromatin immunoprecipitation from multicellular complex samples using BiTS-ChIP Nat Protoc 7 2012 978 994 10.1038/nprot.2012.049
148. S. Liu, J. Brind'Amour, M.M. Karimi, K. Shirane, A. Bogutz, and L. Lefebvre Setdb1 is required for germline development and silencing of H3K9me3-marked endogenous retroviruses in primordial germ cells Genes Dev 28 2014 2041 2055 10.1101/gad.244848.114
149. M. Lae, E.H. Ahn, G.E. Mercado, S. Chuai, M. Edgar, and B.R. Pawel Global gene expression profiling of PAX-FKHR fusion-positive alveolar and PAX-FKHR fusion-negative embryonal rhabdomyosarcomas J Pathol 212 2007 143 151 10.1002/path.2170
150. C. De Pitta, L. Tombolan, G. Albiero, F. Sartori, C. Romualdi, and G. Jurman Gene expression profiling identifies potential relevant genes in alveolar rhabdomyosarcoma pathogenesis and discriminates PAX3-FKHR positive and negative tumors Int J Cancer 118 2006 2772 2781 10.1002/ijc.21698
151. J. Khan, R. Simon, M. Bittner, Y. Chen, S.B. Leighton, and T. Pohida Gene expression profiling of alveolar rhabdomyosarcoma with cDNA microarrays Cancer Res 58 1998 5009 5013
152. Y.D. Krom, P.E. Thijssen, J.M. Young, B. den Hamer, J. Balog, and Z. Yao Intrinsic epigenetic regulation of the D4Z4 macrosatellite repeat in a transgenic mouse model for FSHD PLoS Genet 9 2013 e1003415 10.1371/journal.pgen.1003415
153. J.M. Young, J.L. Whiddon, Z. Yao, B. Kasinathan, L. Snider, and L.N. Geng DUX4 binding to retroelements creates promoters that are active in FSHD muscle and testis PLoS Genet 9 2013 e1003947 10.1371/journal.pgen.1003947
154. X. Xu, K. Tsumagari, J. Sowden, R. Tawil, A.P. Boyle, and L. Song DNaseI hypersensitivity at gene-poor, FSH dystrophy-linked 4q35.2 Nucleic Acids Res 37 2009 7381 7393 10.1093/nar/gkp833
155. J.N. Haslett, D. Sanoudou, A.T. Kho, R.R. Bennett, S.A. Greenberg, and I.S. Kohane Gene expression comparison of biopsies from Duchenne muscular dystrophy (DMD) and normal skeletal muscle Proc Natl Acad Sci U S A 99 2002 15000 15005 10.1073/pnas.192571199
156. M. Bakay, P. Zhao, J. Chen, and E.P. Hoffman A web-accessible complete transcriptome of normal human and DMD muscle Neuromuscul Disord 12 2002 S125 S141
157. V. Saccone, S. Consalvi, L. Giordani, C. Mozzetta, I. Barozzi, and M. Sandona HDAC-regulated myomiRs control BAF60 variant exchange and direct the functional phenotype of fibro-adipogenic progenitors in dystrophic muscles Genes Dev 28 2014 841 857 10.1101/gad.234468.113
158. P.G. Giresi, E.J. Stevenson, J. Theilhaber, A. Koncarevic, J. Parkington, and R.A. Fielding Identification of a molecular signature of sarcopenia Physiol Genomics 21 2005 253 263 10.1152/physiolgenomics.00249.2004
159. M.J. Drummond, J.J. McCarthy, M. Sinha, H.M. Spratt, E. Volpi, and K.A. Esser Aging and microRNA expression in human skeletal muscle: a microarray and bioinformatics analysis Physiol Genomics 43 2011 595 603 10.1152/physiolgenomics.00148.2010
160. M. Barns, C. Gondro, R.L. Tellam, H.G. Radley-Crabb, M.D. Grounds, and T. Shavlakadze Molecular analyses provide insight into mechanisms underlying sarcopenia and myofibre denervation in old skeletal muscles of mice Int J Biochem Cell Biol 53 2014 174 185 10.1016/j.biocel.2014.04.025
161. R.W. Jackman, C.L. Wu, and S.C. Kandarian The ChIP-seq-defined networks of Bcl-3 gene binding support its required role in skeletal muscle atrophy PLoS One 7 2012 e51478 10.1371/journal.pone.0051478