Brahma is required for cell cycle arrest and late muscle gene expression during skeletal myogenesis

EMBO Reports

Volumn 16, Issue 8, 2015, Pages 1037-1050

  Albini, Sonia ^a   Coutinho Toto, Paula ^a   Dall'Agnese, Alessandra ^a   Malecova, Barbora ^a   Cenciarelli, Carlo ^b   Felsani, Armando ^c   Caruso, Maurizia ^c   Bultman, Scott J ^d   Puri, Pier Lorenzo ^a,c  

^a BURNHAM INSTITUTE   (United States)

^b INSTITUTE OF TRANSLATIONAL PHARMACOLOGY   (Italy)

^c IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Brahma; cyclin D1; skeletal myogenesis; SNF SWI; transcription

Indexed keywords

ACTIN; BRG1 PROTEIN; BRM PROTEIN; CYCLIN D1; CYCLIN DEPENDENT KINASE 4; MYOGENIN; PROTEIN SWI; TRANSCRIPTION FACTOR SNF; CCND1 PROTEIN, MOUSE; DNA HELICASE; NUCLEAR PROTEIN; SMARCA2 PROTEIN, MOUSE; SMARCA4 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CYCLE ARREST; CELL CYCLE REGULATION; CELL PROLIFERATION; CONTROLLED STUDY; G1 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; GENE FUNCTION; GENE REPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MUSCLE CELL; MUSCLE DEVELOPMENT; MUSCLE FUNCTION; MUSCLE INJURY; MUSCLE REGENERATION; MYOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SATELLITE CELL; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; ANIMAL; CELL CYCLE CHECKPOINT; DEFICIENCY; GENETICS; METABOLISM;

MUS;

ANIMALS; CELL CYCLE CHECKPOINTS; CYCLIN D1; DNA HELICASES; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; MICE; MUSCLE CELLS; MUSCLE DEVELOPMENT; NUCLEAR PROTEINS; TRANSCRIPTION FACTORS;

EID: 84938749833     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201540159     Document Type: Article

References (56)

1. Dilworth FJ, Blais A, (2011) Epigenetic regulation of satellite cell activation during muscle regeneration. Stem Cell Res Ther 2: 18
2. Fong AP, Tapscott SJ, (2013) Skeletal muscle programming and re-programming. Curr Opin Genet Dev 23: 568-573
3. 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
4. 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
5. Guasconi V, Puri PL, (2009) Chromatin: the interface between extrinsic cues and the epigenetic regulation of muscle regeneration. Trends Cell Biol 19: 286-294
6. 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
7. 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
8. Ohkawa Y, Yoshimura S, Higashi C, Marfella CG, Dacwag CS, Tachibana T, Imbalzano AN, (2007) Myogenin and the SWI/SNF ATPase Brg1 maintain myogenic gene expression at different stages of skeletal myogenesis. J Biol Chem 282: 6564-6570
9. Puri PL, Mercola M, (2012) BAF60 A, B, and Cs of muscle determination and renewal. Genes Dev 26: 2673-2683
10. Wu JI, Lessard J, Crabtree GR, (2009) Understanding the words of chromatin regulation. Cell 136: 200-206
11. Albini S, Puri PL, (2010) SWI/SNF complexes, chromatin remodeling and skeletal myogenesis: it's time to exchange!. Exp Cell Res 316: 3073-3080
12. Cairns BR, (2009) The logic of chromatin architecture and remodelling at promoters. Nature 461: 193-198
13. Lessard JA, Crabtree GR, (2010) Chromatin regulatory mechanisms in pluripotency. Annu Rev Cell Dev Biol 26: 503-532
14. Wilson BG, Roberts CW, (2011) SWI/SNF nucleosome remodellers and cancer. Nat Rev Cancer 11: 481-492
15. Yaniv M, (2014) Chromatin remodeling: from transcription to cancer. Cancer Genet 207: 352-357
16. Kowenz-Leutz E, Leutz A, (1999) A C/EBP beta isoform recruits the SWI/SNF complex to activate myeloid genes. Mol Cell 4: 735-743
17. Muchardt C, Yaniv M, (1993) A human homologue of Saccharomyces cerevisiae SNF2/SWI2 and Drosophila brm genes potentiates transcriptional activation by the glucocorticoid receptor. EMBO J 12: 4279-4290
18. Sena JA, Wang L, Hu CJ, (2013) BRG1 and BRM chromatin-remodeling complexes regulate the hypoxia response by acting as coactivators for a subset of hypoxia-inducible transcription factor target genes. Mol Cell Biol 33: 3849-3863
19. Willis MS, Homeister JW, Rosson GB, Annayev Y, Holley D, Holly SP, Madden VJ, Godfrey V, Parise LV, Bultman SJ, (2012) Functional redundancy of SWI/SNF catalytic subunits in maintaining vascular endothelial cells in the adult heart. Circ Res 111: e111-e122
20. Wilson BG, Helming KC, Wang X, Kim Y, Vazquez F, Jagani Z, Hahn WC, Roberts CW, (2014) Residual complexes containing SMARCA2 (BRM) underlie the oncogenic drive of SMARCA4 (BRG1) mutation. Mol Cell Biol 34: 1136-1144
21. Zhang M, Chen M, Kim JR, Zhou J, Jones RE, Tune JD, Kassab GS, Metzger D, Ahlfeld S, Conway SJ, et al, (2011) SWI/SNF complexes containing Brahma or Brahma-related gene 1 play distinct roles in smooth muscle development. Mol Cell Biol 31: 2618-2631
22. de la Serna IL, Carlson KA, Imbalzano AN, (2001) Mammalian SWI/SNF complexes promote MyoD-mediated muscle differentiation. Nat Genet 27: 187-190
23. 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
24. Mallappa C, Nasipak BT, Etheridge L, Androphy EJ, Jones SN, Sagerstrom CG, Ohkawa Y, Imbalzano AN, (2010) Myogenic microRNA expression requires ATP-dependent chromatin remodeling enzyme function. Mol Cell Biol 30: 3176-3186
25. Forcales SV, Albini S, Giordani L, Malecova B, Cignolo L, Chernov A, Coutinho P, Saccone V, Consalvi S, Williams R, et al, (2012) Signal-dependent incorporation of MyoD-BAF60c into Brg1-based SWI/SNF chromatin-remodelling complex. EMBO J 31: 301-316
26. Bultman S, Gebuhr T, Yee D, La Mantia C, Nicholson J, Gilliam A, Randazzo F, Metzger D, Chambon P, Crabtree G, et al, (2000) A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol Cell 6: 1287-1295
27. Klochendler-Yeivin A, Fiette L, Barra J, Muchardt C, Babinet C, Yaniv M, (2000) The murine SNF5/INI1 chromatin remodeling factor is essential for embryonic development and tumor suppression. EMBO Rep 1: 500-506
28. Reyes JC, Barra J, Muchardt C, Camus A, Babinet C, Yaniv M, (1998) Altered control of cellular proliferation in the absence of mammalian brahma (SNF2alpha). EMBO J 17: 6979-6991
29. Muchardt C, Bourachot B, Reyes JC, Yaniv M, (1998) ras transformation is associated with decreased expression of the brm/SNF2alpha ATPase from the mammalian SWI-SNF complex. EMBO J 17: 223-231
30. Kadam S, Emerson BM, (2003) Transcriptional specificity of human SWI/SNF BRG1 and BRM chromatin remodeling complexes. Mol Cell 11: 377-389
31. Fujio Y, Guo K, Mano T, Mitsuuchi Y, Testa JR, Walsh K, (1999) Cell cycle withdrawal promotes myogenic induction of Akt, a positive modulator of myocyte survival. Mol Cell Biol 19: 5073-5082
32. Guttridge DC, Albanese C, Reuther JY, Pestell RG, Baldwin AS Jr, (1999) NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol Cell Biol 19: 5785-5799
33. Skapek SX, Rhee J, Kim PS, Novitch BG, Lassar AB, (1996) Cyclin-mediated inhibition of muscle gene expression via a mechanism that is independent of pRB hyperphosphorylation. Mol Cell Biol 16: 7043-7053
34. Skapek SX, Rhee J, Spicer DB, Lassar AB, (1995) Inhibition of myogenic differentiation in proliferating myoblasts by cyclin D1-dependent kinase. Science 267: 1022-1024
35. Zhang JM, Zhao X, Wei Q, Paterson BM, (1999) Direct inhibition of G(1) cdk kinase activity by MyoD promotes myoblast cell cycle withdrawal and terminal differentiation. EMBO J 18: 6983-6993
36. Asp P, Blum R, Vethantham V, Parisi F, Micsinai M, Cheng J, Bowman C, Kluger Y, Dynlacht BD, (2011) Genome-wide remodeling of the epigenetic landscape during myogenic differentiation. Proc Natl Acad Sci USA 108: E149-E158
37. Andres V, Walsh K, (1996) Myogenin expression, cell cycle withdrawal, and phenotypic differentiation are temporally separable events that precede cell fusion upon myogenesis. J Cell Biol 132: 657-666
38. 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: 501-506
39. Liu QC, Zha XH, Faralli H, Yin H, Louis-Jeune C, Perdiguero E, Pranckeviciene E, Munoz-Canoves P, Rudnicki MA, Brand M, et al, (2012) Comparative expression profiling identifies differential roles for Myogenin and p38alpha MAPK signaling in myogenesis. J Mol Cell Biol 4: 386-397
40. Ohkawa Y, Marfella CG, Imbalzano AN, (2006) Skeletal muscle specification by myogenin and Mef2D via the SWI/SNF ATPase Brg1. EMBO J 25: 490-501
41. Novitch BG, Mulligan GJ, Jacks T, Lassar AB, (1996) Skeletal muscle cells lacking the retinoblastoma protein display defects in muscle gene expression and accumulate in S and G2 phases of the cell cycle. J Cell Biol 135: 441-456
42. Novitch BG, Spicer DB, Kim PS, Cheung WL, Lassar AB, (1999) pRb is required for MEF2-dependent gene expression as well as cell-cycle arrest during skeletal muscle differentiation. Curr Biol 9: 449-459
43. Sellers WR, Novitch BG, Miyake S, Heith A, Otterson GA, Kaye FJ, Lassar AB, Kaelin WG Jr, (1998) Stable binding to E2F is not required for the retinoblastoma protein to activate transcription, promote differentiation, and suppress tumor cell growth. Genes Dev 12: 95-106
44. 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
45. Cao Y, Yao Z, Sarkar D, Lawrence M, Sanchez GJ, Parker MH, MacQuarrie KL, Davison J, Morgan MT, Ruzzo WL, et al, (2010) Genome-wide MyoD binding in skeletal muscle cells: a potential for broad cellular reprogramming. Dev Cell 18: 662-674
46. Mauro A, (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9: 493-495
47. Brack AS, Rando TA, (2012) Tissue-specific stem cells: lessons from the skeletal muscle satellite cell. Cell Stem Cell 10: 504-514
48. Yin H, Price F, Rudnicki MA, (2013) Satellite cells and the muscle stem cell niche. Physiol Rev 93: 23-67
49. Blais A, van Oevelen CJ, Margueron R, Acosta-Alvear D, Dynlacht BD, (2007) Retinoblastoma tumor suppressor protein-dependent methylation of histone H3 lysine 27 is associated with irreversible cell cycle exit. J Cell Biol 179: 1399-1412
50. Caretti G, Di Padova M, Micales B, Lyons GE, Sartorelli V, (2004) The Polycomb Ezh2 methyltransferase regulates muscle gene expression and skeletal muscle differentiation. Genes Dev 18: 2627-2638
51. Ho L, Crabtree GR, (2010) Chromatin remodelling during development. Nature 463: 474-484
52. Atchison L, Ghias A, Wilkinson F, Bonini N, Atchison ML, (2003) Transcription factor YY1 functions as a PcG protein in vivo. EMBO J 22: 1347-1358
53. Zhang HS, Gavin M, Dahiya A, Postigo AA, Ma D, Luo RX, Harbour JW, Dean DC, (2000) Exit from G1 and S phase of the cell cycle is regulated by repressor complexes containing HDAC-Rb-hSWI/SNF and Rb-hSWI/SNF. Cell 101: 79-89
54. Joliot V, Ait-Mohamed O, Battisti V, Pontis J, Philipot O, Robin P, Ito H, Ait-Si-Ali S, (2014) The SWI/SNF subunit/tumor suppressor BAF47/INI1 is essential in cell cycle arrest upon skeletal muscle terminal differentiation. PLoS ONE 9: e108858
55. Mozzetta C, Consalvi S, Saccone V, Tierney M, Diamantini A, Mitchell KJ, Marazzi G, Borsellino G, Battistini L, Sassoon D, 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
56. Albini S, Coutinho P, Malecova B, Giordani L, Savchenko A, Forcales SV, Puri PL, (2013) Epigenetic reprogramming of human embryonic stem cells into skeletal muscle cells and generation of contractile myospheres. Cell Rep 3: 661-670