Transcriptional networks regulating the costamere, sarcomere, and other cytoskeletal structures in striated muscle

Cellular and Molecular Life Sciences

Volumn 71, Issue 9, 2014, Pages 1641-1656

  Estrella, Nelsa L ^a   Naya, Francisco J ^a  

^a USA   (United States)

Author keywords

Costamere; MEF2; Myofibril; Sarcomere; Striated muscle; Transcription factor

Indexed keywords

ANIMALS; COSTAMERES; CYTOSKELETON; GENE REGULATORY NETWORKS; HUMANS; MUSCLE, SKELETAL; MYOCYTES, CARDIAC; SARCOMERES; TRANSCRIPTION FACTORS;

EID: 84899415817     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1512-0     Document Type: Review

References (116)

1. Lin Z, Lu MH, Schultheiss T, Choi J, Holtzer S, DiLullo C, Fischman DA, Holtzer H (1994) Sequential appearance of muscle-specific proteins in myoblasts as a function of time after cell division: evidence for a conserved myoblast differentiation program in skeletal muscle. Cell Motil Cytoskeleton 29(1):1-19 (Pubitemid 24278002)
2. Sanger JW, Kang S, Siebrands CC, Freeman N, Du A, Wang J, Stout AL, Sanger JM (2005) How to build a myofibril. J Muscle Res Cell Motil 26(6-8):343-354
3. Sparrow JC, Schöck F (2009) The initial steps of myofibril assembly: integrins pave the way. Nat Rev Mol Cell Biol 10(4):293-298
4. Clark KA, McElhinny AS, Beckerle MC, Gregorio CC (2002) Striated muscle cytoarchitecture: an intricate web of form and function. Annu Rev Cell Dev Biol 18:637-706 (Pubitemid 35387364)
5. Seidman JG, Seidman C (2001) The genetic basis for cardiomyopathy: from mutation identification to mechanistic paradigms. Cell 104(4):557-567 (Pubitemid 32201950)
6. Nicol RL, Frey N, Olson EN (2000) From the sarcomere to the nucleus: role of genetics and signaling in structural heart disease. Annu Rev Genomics Hum Genet 1:179-223
7. Boateng SY, Goldspink PH (2008) Assembly and maintenance of the sarcomere night and day. Cardiovasc Res 77(4):667-675 (Pubitemid 351301857)
8. Ehler E, Gautel M (2008) The sarcomere and sarcomerogenesis. Adv Exp Med Biol 642:1-14
9. Pyle WG, Solaro RJ (2004) At the crossroads of myocardial signaling: the role of Z-discs in intracellular signaling and cardiac function. Circ Res 94(3):296-305 (Pubitemid 38240720)
10. Frank D, Frey N (2011) Cardiac Z-disc signaling network. J Biol Chem 286(12):9897-9904
11. Miller MK, Granzier H, Ehler E, Gregorio CC (2004) The sensitive giant: the role of titin-based stretch sensing complexes in the heart. Trends Cell Biol 14(3):119-126 (Pubitemid 38293454)
12. Gautel M (2011) The sarcomeric cytoskeleton: who picks up the strain? Curr Opin Cell Biol 23(1):39-46
13. Lange S, Ehler E, Gautel M (2006) From A to Z and back? Multicompartment proteins in the sarcomere. Trends Cell Biol 16(1):11-18 (Pubitemid 43077090)
14. Sanger JM, Sanger JW (2008) The dynamic Z bands of striated muscle cells. Sci Signal 1(32):pe37
15. Danowski BA, Imanaka-Yoshida K, Sanger JM, Sanger JW (1992) Costameres are sites of force transmission to the substratum in adult rat cardiomyocytes. J Cell Biol 118(6):1411-1420
16. Ervasti JM (2003) Costameres: the Achilles' heel of Herculean muscle. J Biol Chem 278(16):13591-13594 (Pubitemid 36799888)
17. Samarel AM (2005) Costameres, focal adhesions, and cardiomyocyte mechanotransduction. Am J Physiol Heart Circ Physiol. 289(6):H2291-H2301
18. Hoshijima M (2006) Mechanical stress-strain sensors embedded in cardiac cytoskeleton: Z disk, titin, and associated structures. Am J Physiol Heart Circ Physiol 290(4):H1313-H1325
19. Rando TA (2001) The dystrophin-glycoprotein complex, cellular signaling, and the regulation of cell survival in the muscular dystrophies. Muscle Nerve 24(12):1575-1594 (Pubitemid 33101403)
20. Ervasti JM (2007) Dystrophin, its interactions with other proteins, and implications for muscular dystrophy. Biochim Biophys Acta 1772(2):108-117 (Pubitemid 46123911)
21. Davies KE, Nowak KJ (2006) Molecular mechanisms of muscular dystrophies: old and new players. Nat Rev Mol Cell Biol 7(10):762-773 (Pubitemid 44450460)
22. Heydemann A, McNally EM (2007) Consequences of disrupting the dystrophin-sarcoglycan complex in cardiac and skeletal myopathy. Trends Cardiovasc Med 17(2):55-59 (Pubitemid 46205328)
23. Severs NJ (1990) The cardiac gap junction and intercalated disc. Int J Cardiol 26(2):137-173 (Pubitemid 20035665)
24. Bennett PM (2012) From myofibril to membrane; the transitional junction at the intercalated disc. Front Biosci (Landmark Ed) 17:1035-1050
25. Charvet B, Ruggiero F, Le Guellec D (2012) The development of the myotendinous junction. A review. Muscles Ligaments Tendons J 2(2):53-63
26. Sanes JR, Lichtman JW (2001) Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci 2(11):791-805 (Pubitemid 33674061)
27. Burden SJ (2002) Building the vertebrate neuromuscular synapse. J Neurobiol 53(4):501-511 (Pubitemid 35375581)
28. Olson EN, Nordheim A (2010) Linking actin dynamics and gene transcription to drive cellular motile functions. Nat Rev Mol Cell Biol 11(5):353-365
29. Black BL, Olson EN (1998) Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Annu Rev Cell Dev Biol 14:167-196 (Pubitemid 29001453)
30. Naya FJ, Olson E (1999) MEF2: a transcriptional target for signaling pathways controlling skeletal muscle growth and differentiation. Curr Opin Cell Biol 11(6):683-688
31. Potthoff MJ, Olson EN (2007) MEF2: a central regulator of diverse developmental programs. Development 134(23):4131-4140
32. Bour BA, O'Brien MA, Lockwood WL, Goldstein ES, Bodmer R, Taghert PH, Abmayr SM, Nguyen HT (1995) Drosophila MEF2, a transcription factor that is essential for myogenesis. Genes Dev 9(6):730-741
33. Lilly B, Zhao B, Ranganayakulu G, Paterson BM, Schulz RA, Olson EN (1995) Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila. Science 267(5198):688-693
34. Ranganayakulu G, Zhao B, Dokidis A, Molkentin JD, Olson EN, Schulz RA (1995) A series of mutations in the D-MEF2 transcription factor reveal multiple functions in larval and adult myogenesis in Drosophila. Dev Biol 171(1):169-181
35. Naya FJ, Black BL, Wu H, Bassel-Duby R, Richardson JA, Hill JA, Olson EN (2002) Mitochondrial deficiency and cardiac sudden death in mice lacking the MEF2A transcription factor. Nat Med 8(11):1303-1309 (Pubitemid 35373564)
36. Potthoff MJ, Arnold MA, McAnally J, Richardson JA, Bassel-Duby R, Olson EN (2007) Regulation of skeletal muscle sarcomere integrity and postnatal muscle function by Mef2c. Mol Cell Biol 27(23):8143-8151 (Pubitemid 350234229)
37. Durham JT, Brand OM, Arnold M, Reynolds JG, Muthukumar L, Weiler H, Richardson JA, Naya FJ (2006) Myospryn is a direct transcriptional target for MEF2A that encodes a striated muscle, alpha-actinin-interacting, costamere-localized protein. J Biol Chem 281(10):6841-6849 (Pubitemid 43847620)
38. Huang HT, Brand OM, Mathew M, Ignatiou C, Ewen EP, McCalmon SA, Naya FJ (2006) Myomaxin is a novel transcriptional target of MEF2A that encodes a Xin-related alpha-actinin interacting protein. J Biol Chem 281(51):39370-39379 (Pubitemid 46041896)
39. Ewen EP, Snyder CM, Wilson M, Desjardins D, Naya FJ (2011) The Mef2A transcription factor coordinately regulates a costamere gene program in cardiac muscle. J Biol Chem 286(34):29644-29653
40. McKinsey TA, Zhang CL, Olson EN (2002) MEF2: a calcium-dependent regulator of cell division, differentiation and death. Trends Biochem Sci 27(1):40-47 (Pubitemid 34131624)
41. Shen H, McElhinny AS, Cao Y, Gao P, Liu J, Bronson R, Griffin JD, Wu L (2006) The Notch coactivator, MAML1, functions as a novel coactivator for MEF2C-mediated transcription and is required for normal myogenesis. Genes Dev 20(6):675-688
42. Miano JM (2010) Role of serum response factor in the pathogenesis of disease. Lab Invest 90(9):1274-1284
43. Posern G, Treisman R (2006) Actin' together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol 16(11):588-596 (Pubitemid 44636222)
44. Miano JM, Long X, Fujiwara K (2007) Serum response factor: master regulator of the actin cytoskeleton and contractile apparatus. Am J Physiol Cell Physiol 292(1):C70-C81
45. Arsenian S, Weinhold B, Oelgeschläger M, Rüther U, Nordheim A (1998) Serum response factor is essential for mesoderm formation during mouse embryogenesis. EMBO J 17(21):6289-6299 (Pubitemid 28497801)
46. Miano JM, Ramanan N, Georger MA, de Mesy Bentley KL, Emerson RL, Balza RO Jr, Xiao Q, Weiler H, Ginty DD, Misra RP (2004) Restricted inactivation of serum response factor to the cardiovascular system. Proc Natl Acad Sci USA 101(49):17132-17137 (Pubitemid 39627786)
47. Niu Z, Iyer D, Conway SJ, Martin JF, Ivey K, Srivastava D, Nordheim A, Schwartz RJ (2008) Serum response factor orchestrates nascent sarcomerogenesis and silences the biomineralization gene program in the heart. Proc Natl Acad Sci USA 105(46):17824-17829
48. Balza RO Jr, Misra RP (2006) Role of the serum response factor in regulating contractile apparatus gene expression and sarcomeric integrity in cardiomyocytes. J Biol Chem 281(10):6498-6510 (Pubitemid 43847583)
49. Lu J, McKinsey TA, Zhang CL, Olson EN (2000) Regulation of skeletal myogenesis by association of the MEF2 transcription factor with class II histone deacetylases. Mol Cell 6(2):233-244
50. Cohen TJ, Barrientos T, Hartman ZC, Garvey SM, Cox GA, Yao TP (2009) The deacetylase HDAC4 controls myocyte enhancing factor-2-dependent structural gene expression in response to neural activity. FASEB J 23(1):99-106
51. Silverstein RA, Ekwall K (2005) Sin3: a flexible regulator of global gene expression and genome stability. Curr Genet 47(1):1-17 (Pubitemid 40069110)
52. van Oevelen C, Wang J, Asp P, Yan Q, Kaelin WG Jr, Kluger Y, Dynlacht BD (2008) A role for mammalian Sin3 in permanent gene silencing. Mol Cell 32(3):359-370
53. van Oevelen C, Bowman C, Pellegrino J, Asp P, Cheng J, Parisi F, Micsinai M, Kluger Y, Chu A, Blais A, David G, Dynlacht BD (2010) The mammalian Sin3 proteins are required for muscle development and sarcomere specification. Mol Cell Biol 30(24):5686-5697
54. Sandmann T, Jensen LJ, Jakobsen JS, Karzynski MM, Eichenlaub MP, Bork P, Furlong EE (2006) A temporal map of transcription factor activity: mef2 directly regulates target genes at all stages of muscle development. Dev Cell 10(6):797-807 (Pubitemid 43779116)
55. Kelly KK, Meadows SM, Cripps RM (2002) Drosophila MEF2 is a direct regulator of Actin57B transcription in cardiac, skeletal, and visceral muscle lineages. Mech Dev 110(1-2):39-50 (Pubitemid 34020625)
56. Stronach BE, Renfranz PJ, Lilly B, Beckerle MC (1999) Muscle LIM proteins are associated with muscle sarcomeres and require dMEF2 for their expression during Drosophila myogenesis. Mol Biol Cell 10(7):2329-2342 (Pubitemid 29343138)
57. Lin MH, Nguyen HT, Dybala C, Storti RV (1996) Myocyte-specific enhancer factor 2 acts cooperatively with a muscle activator region to regulate Drosophila tropomyosin gene muscle expression. Proc Natl Acad Sci USA 93(10):4623-4628 (Pubitemid 26162813)
58. Marín MC, Rodríguez JR, Ferrús A (2004) Transcription of Drosophila troponin I gene is regulated by two conserved, functionally identical, synergistic elements. Mol Biol Cell 15(3):1185-1196 (Pubitemid 38316226)
59. Wang YX, Qian LX, Yu Z, Jiang Q, Dong YX, Liu XF, Yang XY, Zhong TP, Song HY (2005) Requirements of myocyte-specific enhancer factor 2A in zebrafish cardiac contractility. FEBS Lett 579(21):4843-4850 (Pubitemid 41218673)
60. Hinits Y, Hughes SM (2007) Mef2s are required for thick filament formation in nascent muscle fibres. Development 134(13):2511-2519 (Pubitemid 47074145)
61. Zhou P, He A, Pu WT (2012) Regulation of GATA4 transcriptional activity in cardiovascular development and disease. Curr Top Dev Biol 100:143-169
62. Oka T, Xu J, Molkentin JD (2007) Re-employment of developmental transcription factors in adult heart disease. Semin Cell Dev Biol 18(1):117-131 (Pubitemid 46330840)
63. Charron F, Tsimiklis G, Arcand M, Robitaille L, Liang Q, Molkentin JD, Meloche S, Nemer M (2001) Tissue-specific GATA factors are transcriptional effectors of the small GTPase RhoA. Genes Dev 15(20):2702-2719 (Pubitemid 32988880)
64. Chen B, Zhong L, Roush SF, Pentassuglia L, Peng X, Samaras S, Davidson JM, Sawyer DB, Lim CC (2012) Disruption of a GATA4/Ankrd1 signaling axis in cardiomyocytes leads to sarcomere disarray: implications for anthracycline cardiomyopathy. PLoS ONE 7(4):e35743
65. Bodmer R (1993) The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development 118(3):719-729 (Pubitemid 23232780)
66. Lyons I, Parsons LM, Hartley L, Li R, Andrews JE, Robb L, Harvey RP (1995) Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nk2-5. Genes Dev 9(13):1654-1666
67. Tanaka M, Chen Z, Bartunkova S, Yamasaki N, Izumo S (1999) The cardiac homeobox gene Csx/Nkx2.5 lies genetically upstream of multiple genes essential for heart development. Development 126(6):1269-1280 (Pubitemid 29182122)
68. Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247-269 (Pubitemid 41740635)
69. Maillet M, Lynch JM, Sanna B, York AJ, Zheng Y, Molkentin JD (2009) Cdc42 is an antihypertrophic molecular switch in the mouse heart. J Clin Invest 119(10):3079-3088
70. Qian L, Wythe JD, Liu J, Cartry J, Vogler G, Mohapatra B, Otway RT, Huang Y, King IN, Maillet M, Zheng Y, Crawley T, Taghli-Lamallem O, Semsarian C, Dunwoodie S, Winlaw D, Harvey RP, Fatkin D, Towbin JA, Molkentin JD, Srivastava D, Ocorr K, Bruneau BG, Bodmer R (2011) Tinman/Nk2-5 acts via miR-1 and upstream of Cdc42 to regulate heart function across species. J Cell Biol 193(7):1181-1196
71. Kasahara H, Ueyama T, Wakimoto H, Liu MK, Maguire CT, Converso KL, Kang PM, Manning WJ, Lawitts J, Paul DL, Berul CI, Izumo S (2003) Nkx2.5 homeoprotein regulates expression of gap junction protein connexin 43 and sarcomere organization in postnatal cardiomyocytes. J Mol Cell Cardiol 35(3):243-256 (Pubitemid 36382915)
72. Kirk EP, Sunde M, Costa MW, Rankin SA, Wolstein O, Castro ML, Butler TL, Hyun C, Guo G, Otway R, Mackay JP, Waddell LB, Cole AD, Hayward C, Keogh A, Macdonald P, Griffiths L, Fatkin D, Sholler GF, Zorn AM, Feneley MP, Winlaw DS, Harvey RP (2007) Mutations in cardiac T-box factor gene TBX20 are associated with diverse cardiac pathologies, including defects of septation and valvulogenesis and cardiomyopathy. Am J Hum Genet 81(2):280-291 (Pubitemid 47236076)
73. Qian L, Mohapatra B, Akasaka T, Liu J, Ocorr K, Towbin JA, Bodmer R (2008) Transcription factor neuromancer/TBX20 is required for cardiac function in Drosophila with implications for human heart disease. Proc Natl Acad Sci USA 105(50):19833-19838
74. Shen T, Aneas I, Sakabe N, Dirschinger RJ, Wang G, Smemo S, Westlund JM, Cheng H, Dalton N, Gu Y, Boogerd CJ, Cai CL, Peterson K, Chen J, Nobrega MA, Evans SM (2011) Tbx20 regulates a genetic program essential to adult mouse cardiomyocyte function. J Clin Invest 121(12):4640-4654
75. Francois M, Harvey NL, Hogan BM (2011) The transcriptional control of lymphatic vascular development. Physiology (Bethesda) 26(3):146-155
76. Hope KJ, Sauvageau G (2011) Roles for MSI2 and PROX1 in hematopoietic stem cell activity. Curr Opin Hematol 18(4):203-207
77. Oliver G, Sosa-Pineda B, Geisendorf S, Spana EP, Doe CQ, Gruss P (1993) Prox 1, a prospero-related homeobox gene expressed during mouse development. Mech Dev 44(1):3-16 (Pubitemid 24037694)
78. Risebro CA, Searles RG, Melville AA, Ehler E, Jina N, Shah S, Pallas J, Hubank M, Dillard M, Harvey NL, Schwartz RJ, Chien KR, Oliver G, Riley PR (2009) Prox1 maintains muscle structure and growth in the developing heart. Development 136(3):495-505
79. Hayden MS, Ghosh S (2008) Shared principles in NF-kappaB signaling. Cell 132(3):344-362
80. Wang H, Hertlein E, Bakkar N, Sun H, Acharyya S, Wang J, Carathers M, Davuluri R, Guttridge DC (2007) NF-kappaB regulation of YY1 inhibits skeletal myogenesis through transcriptional silencing of myofibrillar genes. Mol Cell Biol 27(12):4374-4387 (Pubitemid 46906562)
81. Tang RH, Zheng XL, Callis TE, Stansfield WE, He J, Baldwin AS, Wang DZ, Selzman CH (2008) Myocardin inhibits cellular proliferation by inhibiting NF-kappaB (p65)-dependent cell cycle progression. Proc Natl Acad Sci USA 105(9):3362-3367 (Pubitemid 351723558)
82. Speck NA, Gilliland DG (2002) Core-binding factors in haematopoiesis and leukaemia. Nat Rev Cancer 2(7):502-513 (Pubitemid 37328932)
83. Chiba N, Watanabe T, Nomura S, Tanaka Y, Minowa M, Niki M, Kanamaru R, Satake M (1997) Differentiation-dependent expression and distinct subcellular localization of the protooncogene product, PEBP2beta/CBFbeta, in muscle development. Oncogene 14(21):2543-2552 (Pubitemid 27273516)
84. Meder B, Just S, Vogel B, Rudloff J, Gärtner L, Dahme T, Huttner I, Zankl A, Katus HA, Rottbauer W (2010) JunB-CBFbeta signaling is essential to maintain sarcomeric Z-disc structure and when defective leads to heart failure. J Cell Sci 123(Pt 15):2613-2620
85. Wang X, Blagden C, Fan J, Nowak SJ, Taniuchi I, Littman DR, Burden SJ (2005) Runx1 prevents wasting, myofibrillar disorganization, and autophagy of skeletal muscle. Genes Dev 19(14):1715-1722 (Pubitemid 41058367)
86. Buckingham M (2001) Skeletal muscle formation in vertebrates. Curr Opin Genet Dev 11(4):440-448 (Pubitemid 32614204)
87. Jagla K, Bellard M, Frasch M (2001) A cluster of Drosophila homeobox genes involved in mesoderm differentiation programs. BioEssays 23(2):125-133 (Pubitemid 32116645)
88. Maqbool T, Soler C, Jagla T, Daczewska M, Lodha N, Palliyil S, VijayRaghavan K, Jagla K (2006) Shaping leg muscles in Drosophila: role of ladybird, a conserved regulator of appendicular myogenesis. PLoS ONE 1:e122
89. Ochi H, Westerfield M (2009) Lbx2 regulates formation of myofibrils. BMC Dev Biol 9:13
90. Semenza GL (2012) Hypoxia-inducible factors in physiology and medicine. Cell 148(3):399-408
91. Iyer NV, Kotch LE, Agani F, Leung SW, Laughner E, Wenger RH, Gassmann M, Gearhart JD, Lawler AM, Yu AY, Semenza GL (1998) Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev 12(2):149-162 (Pubitemid 28060446)
92. Krishnan J, Ahuja P, Bodenmann S, Knapik D, Perriard E, Krek W, Perriard JC (2008) Essential role of developmentally activated hypoxia-inducible factor 1alpha for cardiac morphogenesis and function. Circ Res 103(10):1139-1146
93. Koster MI, Roop DR (2004) The role of p63 in development and differentiation of the epidermis. J Dermatol Sci 34(1):3-9 (Pubitemid 38134467)
94. Rouleau M, Medawar A, Hamon L, Shivtiel S, Wolchinsky Z, Zhou H, De Rosa L, Candi E, de la Forest Divonne S, Mikkola ML, van Bokhoven H, Missero C, Melino G, Pucéat M, Aberdam D (2011) TAp63 is important for cardiac differentiation of embryonic stem cells and heart development. Stem Cells 29(11):1672-1683
95. Pipes GC, Creemers EE, Olson EN (2006) The myocardin family of transcriptional coactivators: versatile regulators of cell growth, migration, and myogenesis. Genes Dev 20(12):1545-1556 (Pubitemid 43901093)
96. Parmacek MS (2007) Myocardin-related transcription factors: critical coactivators regulating cardiovascular development and adaptation. Circ Res 100(5):633-644 (Pubitemid 46594877)
97. Small EM, Warkman AS, Wang DZ, Sutherland LB, Olson EN, Krieg PA (2005) Myocardin is sufficient and necessary for cardiac gene expression in Xenopus. Development 132(5):987-997 (Pubitemid 40484933)
98. Huang J, Min Lu M, Cheng L, Yuan LJ, Zhu X, Stout AL, Chen M, Li J, Parmacek MS (2009) Myocardin is required for cardiomyocyte survival and maintenance of heart function. Proc Natl Acad Sci USA 106(44):18734-18739
99. Kaynak B, von Heydebreck A, Mebus S, Seelow D, Hennig S, Vogel J, Sperling HP, Pregla R, Alexi-Meskishvili V, Hetzer R, Lange PE, Vingron M, Lehrach H, Sperling S (2003) Genome-wide array analysis of normal and malformed human hearts. Circulation 107(19):2467-2474 (Pubitemid 36605230)
100. Lange M, Kaynak B, Forster UB, Tönjes M, Fischer JJ, Grimm C, Schlesinger J, Just S, Dunkel I, Krueger T, Mebus S, Lehrach H, Lurz R, Gobom J, Rottbauer W, Abdelilah-Seyfried S, Sperling S (2008) Regulation of muscle development by DPF3, a novel histone acetylation and methylation reader of the BAF chromatin remodeling complex. Genes Dev 22(17):2370-2384
101. Mal AK (2006) Histone methyltransferase Suv39h1 represses MyoD-stimulated myogenic differentiation. EMBO J 25(14):3323-3334 (Pubitemid 44141790)
102. Tao Y, Neppl RL, Huang ZP, Chen J, Tang RH, Cao R, Zhang Y, Jin SW, Wang DZ (2011) The histone methyltransferase Set7/9 promotes myoblast differentiation and myofibril assembly. J Cell Biol 194(4):551-565
103. Prokop A, Landgraf M, Rushton E, Broadie K, Bate M (1996) Presynaptic development at the Drosophila neuromuscular junction: assembly and localization of presynaptic active zones. Neuron 17(4):617-626 (Pubitemid 26365342)
104. Paris J, Virtanen C, Lu Z, Takahashi M (2004) Identification of MEF2-regulated genes during muscle differentiation. Physiol Genomics 20(1):143-151
105. Blais A, Tsikitis M, Acosta-Alvear D, Sharan R, Kluger Y, Dynlacht BD (2005) An initial blueprint for myogenic differentiation. Genes Dev 19(5):553-569 (Pubitemid 40314988)
106. Wang ZZ, Washabaugh CH, Yao Y, Wang JM, Zhang L, Ontell MP, Watkins SC, Rudnicki MA, Ontell M (2003) Aberrant development of motor axons and neuromuscular synapses in MyoD-null mice. J Neurosci 23(12):5161-5169 (Pubitemid 36793244)
107. Macharia R, Otto A, Valasek P, Patel K (2010) Neuromuscular junction morphology, fiber-type proportions, and satellite-cell proliferation rates are altered in MyoD(-/-) mice. Muscle Nerve 42(1):38-52
108. Macpherson PC, Cieslak D, Goldman D (2006) Myogenin-dependent nAChR clustering in aneural myotubes. Mol Cell Neurosci 31(4):649-660
109. Hasty P, Bradley A, Morris JH, Edmondson DG, Venuti JM, Olson EN, Klein WH (1993) Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364(6437):501-506 (Pubitemid 23273093)
110. Wang J, Fu XQ, Lei WL, Wang T, Sheng AL, Luo ZG (2010) Nuclear factor kappaB controls acetylcholine receptor clustering at the neuromuscular junction. J Neurosci 30(33):11104-11113
111. Handschin C, Kobayashi YM, Chin S, Seale P, Campbell KP, Spiegelman BM (2007) PGC-1alpha regulates the neuromuscular junction program and ameliorates Duchenne muscular dystrophy. Genes Dev 21(7):770-783 (Pubitemid 46572357)
112. Kasahara H, Wakimoto H, Liu M, Maguire CT, Converso KL, Shioi T, Huang WY, Manning WJ, Paul D, Lawitts J, Berul CI, Izumo S (2001) Progressive atrioventricular conduction defects and heart failure in mice expressing a mutant Csx/Nkx2.5 homeoprotein. J Clin Invest 108(2):189-201 (Pubitemid 32656243)
113. Briggs LE, Takeda M, Cuadra AE, Wakimoto H, Marks MH, Walker AJ, Seki T, Oh SP, Lu JT, Sumners C, Raizada MK, Horikoshi N, Weinberg EO, Yasui K, Ikeda Y, Chien KR, Kasahara H (2008) Perinatal loss of Nk2-5 results in rapid conduction and contraction defects. Circ Res 103(6):580-590
114. Crawford GL, Horowits R (2011) Scaffolds and chaperones in myofibril assembly: putting the striations in striated muscle. Biophys Rev 3(1):25-32
115. Vincentz JW, Barnes RM, Firulli AB (2011) Hand factors as regulators of cardiac morphogenesis and implications for congenital heart defects. Birth Defects Res A Clin Mol Teratol 91(6):485-494
116. Breckenridge RA, Zuberi Z, Gomes J, Orford R, Dupays L, Felkin LE, Clark JE, Magee AI, Ehler E, Birks EJ, Barton PJ, Tinker A, Mohun TJ (2009) Overexpression of the transcription factor Hand1 causes predisposition towards arrhythmia in mice. J Mol Cell Cardiol 47(1):133-141