Signal-dependent incorporation of MyoD-BAF60c into Brg1-based SWI/SNF chromatin-remodelling complex

EMBO Journal

Volumn 31, Issue 2, 2012, Pages 301-316

  Forcales, Sonia V ^a,f   Albini, Sonia ^a   Giordani, Lorenzo ^a,b   Malecova, Barbora ^a   Cignolo, Luca ^a   Chernov, Andrei ^a   Coutinho, Paula ^a   Saccone, Valentina ^a,b   Consalvi, Silvia ^a,b   Williams, Roy ^a   Wang, Kepeng ^c   Wu, Zhenguo ^c   Baranovskaya, Svetlana ^d   Miller, Andrew ^d   Dilworth, F Jeffrey ^e   Puri, Pier Lorenzo ^a,b  

^a BURNHAM INSTITUTE   (United States)

^b EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^c HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^d AGILENT TECHNOLOGIES   (United States)

^e OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^f Institute of Predictive and Personalized Medicine of Cancer (IMPPC)   (Spain)

Author keywords

chromatin; gene expression; muscle differentiation; myod; p38

Indexed keywords

BRG1 PROTEIN; MYOD PROTEIN; PROTEIN SERINE THREONINE KINASE; THREONINE; TRANSCRIPTION FACTOR SNF;

ANIMAL CELL; ARTICLE; CHROMATIN; CONTROLLED STUDY; DIFFERENTIATION; GENE; GENE LOCUS; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; MOUSE; MUSCLE; MYOBLAST; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN BINDING; TRANSCRIPTION INITIATION;

ANIMALS; CELL LINE; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA HELICASES; FIBROBLASTS; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MULTIPROTEIN COMPLEXES; MUSCLE DEVELOPMENT; MUSCLE PROTEINS; MYOBLASTS; MYOD PROTEIN; NUCLEAR PROTEINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PHOSPHOTHREONINE; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84857190263     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.391     Document Type: Article

References (59)

1. Albini S, Puri PL (2010) SWI/SNF complexes, chromatin remodeling and skeletal myogenesis: it's time to exchange!. Exp Cell Res 316: 3073-3080
2. Allalou A, Wählby C (2009) BlobFinder, a tool for fluorescence microscopy image cytometry. Comput Methods Programs Biomed 94: 58-65
3. Berghella L, De Angelis L, De Buysscher T, Mortazavi A, Biressi S, Forcales SV, Sirabella D, Cossu G, Wold BJ (2008) A highly conserved molecular switch binds MSY-3 to regulate myogenin repression in postnatal muscle. Genes Dev 22: 2125-2138
4. Bergstrom DA, Penn BH, Strand A, Perry RL, Rudnicki MA, Tapscott SJ (2002) Promoter-specific regulation of MyoD binding and signal transduction cooperate to pattern gene expression. Mol Cell 9: 587-600 (Pubitemid 34273789)
5. Berkes CA, Bergstrom DA, Penn BH, Seaver KJ, Knoepfler PS, Tapscott SJ (2004) Pbx marks genes for activation by MyoD indicating a role for a homeodomain protein in establishing myogenic potential. Mol Cell 14: 465-477 (Pubitemid 38648800)
6. Blais A, Tsikitis M, Acosta-Alvear D, Sharan R, Kluger Y, Dynlacht BD (2005) An initial blueprint for myogenic differentiation. Genes Dev 19: 553-569 (Pubitemid 40314988)
7. Brickner JH (2009) Transcriptional memory at the nuclear periphery. Curr Opin Cell Biol 1: 127-133
8. Cairns BR (2009) The logic of chromatin architecture and remodelling at promoters. Nature 461: 193-198
9. Cao Y, Kumar RM, Penn BH, Berkes CA, Kooperberg C, Boyer LA, Young RA, Tapscott SJ (2006) Global and gene-specific analyses show distinct roles for Myod and Myog at a common set of promoters. EMBO J 25: 502-511 (Pubitemid 43237657)
10. Cao Y, Yao Z, Sarkar D, Lawrence M, Sanchez GJ, Parker MH, MacQuarrie KL, Davison J, Morgan MT, Ruzzo WL, Gentleman RC, Tapscott SJ (2010) Genome-wide MyoD binding in skeletal muscle cells: a potential for broad cellular reprogramming. Dev Cell 18: 662-674
11. Caretti G, Schiltz RL, Dilworth FJ, Di Padova M, Zhao P, Ogryzko V, Fuller-Pace FV, Hoffman EP, Tapscott SJ, Sartorelli V (2006) The RNAhelicases p68/p72 and the noncoding RNA SRA are coregulators of MyoD and skeletal muscle differentiation. Dev Cell 4: 547-560 (Pubitemid 44467725)
12. Chi T (2004) A BAF-centred view of the immune system. Nat Rev Immunol 12: 965-977 (Pubitemid 39620071)
13. Clapier CR, Cairns BR (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78: 273-304
14. De la Serna IL, Carlson KA, Imbalzano AN (2001) Mammalian SWI/SNF complexes promote MyoD-mediated muscle differentiation. Nat Genet 27: 187-190 (Pubitemid 32157446)
15. de la Serna IL, Ohkawa Y, Berkes CA, Bergstrom DA, Dacwag CS, Tapscott SJ, Imbalzano AN (2005) MyoD targets chromatin remodeling complexes to the myogenin locus prior to forming a stable DNA-bound complex. Mol Cell Biol 25: 3997-4009 (Pubitemid 40617649)
16. de la Serna IL, Ohkawa Y, Imbalzano AN (2006) Chromatin remodelling in mammalian differentiation: lessons from ATP-dependent remodellers. Nat Rev Genet 7: 461-473 (Pubitemid 43780489)
17. Debril MB, Gelman L, Fayard E, Annicotte JS, Rocchi S, Auwerx J (2004) Transcription factors and nuclear receptors interact with the SWI/SNF complex through the BAF60c subunit. J Biol Chem 279: 16677-16686 (Pubitemid 38509370)
18. Di Padova M, Caretti G, Zhao P, Hoffman EP, Sartorelli V (2007) MyoD acetylation influences temporal patterns of skeletal muscle gene expression. J Biol Chem 282: 37650-37659
19. Dilworth FJ, Seaver KJ, Fishburn AL, Htet SL, Tapscott SJ (2004) In vitro transcription system delineates the distinct roles of the coactivators pCAF and p300 during MyoD/E47-dependent transactivation. Proc Natl Acad Sci USA 101: 11593-11598 (Pubitemid 39095341)
20. Edmondson DG, Cheng TC, Cserjesi P, Chakraborty T, Olson EN (1992) 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: 3665-3677
21. Flowers S, Nagl Jr NG, Beck Jr GR, Moran E (2009) Antagonistic roles for BRM and BRG1 SWI/SNF complexes in differentiation. J Biol Chem 15: 10067-10075
22. Fredriksson S, Gullberg M, Jarvius J, Olsson C, Pietras K, Gústafsdó ttir SM, Ostman A, Landegren U (2002) Protein detection using proximity-dependent DNA ligation assays. Nat Biotechnol 5: 473-477 (Pubitemid 34495933)
23. Gerber AN, Klesert TR, Bergstrom DA, Tapscott SJ (1997) Two domains of MyoD mediate transcriptional activation of genes in repressive chromatin: a mechanism for lineage determination in myogenesis. Genes Dev 11: 436-450 (Pubitemid 27097643)
24. Gong F, Fahy D, Smerdon MJ (2006) Rad4-Rad23 interaction with SWI/SNF links ATP-dependent chromatin remodeling with nucleotide excision repair. Nat Struct Mol Biol 13: 902-907 (Pubitemid 44527372)
25. Hall TA (1997) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95-98
26. Heidt AB, Rojas A, Harris IS, Black BL (2007) Determinants of myogenic specificity within MyoD are required for noncanonical E box binding. Mol Cell Biol 16: 5910-5920 (Pubitemid 47257843)
27. Kadam S, Emerson BM (2003) Transcriptional specificity of human SWI/SNF BRG1 and BRM chromatin remodeling complexes. Mol Cell 11: 377-389 (Pubitemid 36293832)
28. Khokhlatchev A, Xu S, English J,Wu P, Schaefer E, Cobb MH (1997) Reconstitution of mitogen-activated protein kinase phosphorylation cascades in bacteria. Efficient synthesis of active protein kinases. J Biol Chem 272: 11057-11062 (Pubitemid 27184095)
29. Knoepfler PS, Bergstrom DA, Uetsuki T, Dac-Korytko I, Sun YH, Wright WE, Tapscott SJ, Kamps MP (1999) A conserved motif Nterminal to the DNA-binding domains of myogenic bHLH transcription factors mediates cooperative DNA binding with pbx-Meis/Prep1. Nucleic Acids Res 27: 3752-3761 (Pubitemid 29435757)
30. Lei H, Fukushige T, Niu W, Sarov M, Reinke V, Krause M (2010) A widespread distribution of genomic CeMyoD binding sites revealed and cross validated by ChIP-Chip and ChIP-Seq techniques. PLoS One 5: e15898
31. Lessard J, Crabtree GR (2010) Chromatin regulatory mechanisms in pluripotency. Annu Rev Cell Dev Biol 10: 503-532
32. Li FQ, Coonrod A, Horwitz M (1996) Preferential MyoD homodimer formation demonstrated by a general method of dominant negative mutation employing fusion with a lysosomal protease. J Cell Biol 135: 1043-1057 (Pubitemid 26403777)
33. Lickert H, Takeuchi JK, Von Both I, Walls JR, McAuliffe F, Adamson SL, Henkelman RM, Wrana JL, Rossant J, Bruneau BG (2004) Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature 432: 107-112 (Pubitemid 39490836)
34. Lluis F, Ballestar E, Suelves M, Esteller M, Munoz-Canoves P (2005) E47 phosphorylation by p38 MAPK promotes MyoD/E47 association and muscle-specific gene transcription. EMBO J 24: 974-984 (Pubitemid 40470146)
35. Mal AK (2006) Histone methyltransferase Suv39h1 represses MyoDstimulated myogenic differentiation. EMBO J 25: 3323-3334 (Pubitemid 44141790)
36. Muchardt C, Yaniv M (2001) When the SWI/SNF complex remodelsythe cell cycle. Oncogene 20: 3067-3075 (Pubitemid 32553561)
37. Palacios D, Summerbell D, Rigby PW, Boyes J (2010) Interplay between DNA methylation and transcription factor availability: implications for developmental activation of the mouse Myogenin gene. Mol Cell Biol 15: 3805-3815
38. Park JH, Park EJ, Lee HS, Kim SJ, Hur SK, Imbalzano AN, Kwon J (2006) Mammalian SWI/SNF complexes facilitate DNA-double strand break repair by promoting gamma-H2AX induction. EMBO J 25: 3986-3997 (Pubitemid 44338741)
39. Puri PL, Iezzi S, Stiegler P, Chen TT, Shiltz L, Muscat G, Giordano A, Wang JYJ, Sartorelli V (2001) Class I histone deacetylases sequentially interact with MyoD and pRb during skeletal myogenesis. Mol Cell 8: 885-897 (Pubitemid 33030221)
40. Puri PL, Sartorelli V (2000) Regulation of muscle regulatory factors by DNA-binding, interacting proteins, and post-transcriptional modifications. J Cell Physiol 185: 155-173
41. Puri PL, Sartorelli V, Yang XJ, Hamamori Y, Ogryzko VV, Howard BH, Kedes L, Wang JY, Graessmann A, Nakatani Y, Levrero M (1997) Differential roles of p300 and PCAF acetyltransferases in muscle differentiation. Mol Cell 1: 35-45 (Pubitemid 127376391)
42. Radman-Livaja M, Rando OJ (2010) Nucleosome positioning: how is it established, and why does it matter? Dev Biol 339: 258-266
43. Rampalli S, Li L, Mak E, Ge K, Brand M, Tapscott SJ, Dilworth FJ (2007) p38 MAPK signaling regulates recruitment of Ash2L-containing methyltransferase complexes to specific genes during differentiation. Nat Struct Mol Biol 14: 1150-1156 (Pubitemid 350223328)
44. Reisman D, Glaros S, Thompson EA (2009) The SWI/SNF and cancer. Oncogene 28: 1653-1668
45. Ryme J, Asp P, Böhm S, Cavellán E, Farrants AK (2009) Variations in the composition of mammalian SWI/SNF chromatin remodelling complexes. J Cell Biochem 108: 565-576
46. Sartorelli V, Caretti G (2005) Mechanisms underlying the transcriptional regulation of skeletal myogenesis. Curr Opin Genet Dev 15: 528-535 (Pubitemid 41262409)
47. Sartorelli V, Huang J, Hamamori Y, Kedes L (1997) Molecular mechanisms of myogenic coactivation by p300: direct interaction with the activation domain of MyoD and with the MADS box of MEF2C. Mol Cell Biol 17: 1010-1026 (Pubitemid 27044399)
48. Seenundun S, Rampalli S, Liu QC, Aziz A, Palii C, Hong S, Blais A, Brand M, Ge K, Dilworth FJ (2010) UTX mediates demethylation of H3K27me3 at muscle-specific genes during myogenesis. EMBO J 29: 1401-1411
49. Serra C, Palacios D, Mozzetta C, Forcales SV, Morantte I, Ripani M, Jones DR, Du K, Jhala US, Simone C, Puri PL (2007) Functional interdependence at the chromatin level between the MKK6/p38 and IGF1/PI3K/AKT pathways during muscle differentiation. Mol Cell 28: 200-213 (Pubitemid 47599998)
50. Simone C, Forcales SV, Hill DA, Imbalzano AN, Latella L, Puri PL (2004) p38 pathway targets SWI-SNF chromatin-remodeling complex to muscle-specific loci. Nat Genet 36: 738-743 (Pubitemid 38886636)
51. Singhal N, Graumann J, Wu G, Arauzo-Bravo MJ, Han DW, Greber B, Gentile L, Mann M, Scholer HR (2010) Chromatinremodeling components of the BAF complex facilitate reprogramming. Cell 141: 943-955
52. Sinha M, Watanabe S, Johnson A, Moazed D, Peterson CL (2009) Recombinational repair within heterochromatin requires APdependent chromation remodeling. Cell 138: 1109-1121
53. Takeuchi JK, Bruneau BG (2009) Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature 459: 708-711
54. Tapscott SJ (2005) The circuitry of a master switch: Myod and the regulation of skeletal muscle gene transcription. Development 132: 2685-2695 (Pubitemid 40932860)
55. Wang W, Xue Y, Zhou S, Kuo A, Cairns BR, Crabtree GR (1996) Diversity and specialization of mammalian SWI/SNF complexes. Genes Dev 10: 2117-2130 (Pubitemid 26303868)
56. Weintraub H (1993) The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell 75: 1241-1244 (Pubitemid 24021898)
57. Weintraub H, Tapscott SJ, Davis RL, Thayer MJ, Adam MA, Lassar AB, Miller AD (1989) Activation of muscle-specific genes in pigment, nerve, fat, liver and fibroblast cell lines by forced expression of MyoD. Proc Natl Acad Sci USA 86: 5434-5438 (Pubitemid 19185563)
58. Wu JI, Lessard J, Crabtree GR (2009) Understanding the words of chromatin regulation. Cell 136: 200-206
59. Wu JI, Lessard J, Olave IA, Qiu Z, Ghosh A, Graef IA, Crabtree GR (2007) Regulation of dendritic development by neuron-specific chromatin remodeling complexes. Neuron 56: 94-108 (Pubitemid 47484177)