Spatial re-organization of myogenic regulatory sequences temporally controls gene expression

Nucleic Acids Research

Volumn 43, Issue 4, 2015, Pages 2008-2021

  Harada, Akihito ^a   Mallappa, Chandrashekara ^b   Okada, Seiji ^a   Butler, John T ^b   Baker, Stephen P ^b   Lawrence, Jeanne B ^b   Ohkawa, Yasuyuki ^a,b   Imbalzano, Anthony N ^b  

^a KYUSHU UNIVERSITY   (Japan)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA HELICASE; HISTONE DEACETYLASE 2; MYOD PROTEIN; NUCLEAR PROTEIN; REPRESSOR PROTEIN; SMARCA4 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL; CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE; MUSCLE DEVELOPMENT; PHYSIOLOGY; PROMOTER REGION; REGULATORY SEQUENCE; SKELETAL MUSCLE;

ANIMALS; CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMES, MAMMALIAN; DNA HELICASES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONE DEACETYLASE 2; MICE; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; MYOD PROTEIN; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; REGULATORY ELEMENTS, TRANSCRIPTIONAL; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS;

EID: 84941042333     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv046     Document Type: Article

References (86)

1. Cao,Y., Kumar,R. M., Penn,B. H., Berkes,C. A., Kooperberg,C., Boyer,L. A., Young,R. A. and Tapscott,S. J. (2006) Global and gene-specific analyses show distinct roles for Myod and Myog at a common set of promoters. EMBO J., 25, 502-511.
2. Ohkawa,Y., Marfella,C. G. and Imbalzano,A. N. (2006) Skeletal muscle specification by myogenin and Mef2D via the SWI/SNF ATPase Brg1. EMBO J., 25, 490-501.
3. Blais,A., Tsikitis,M., Acosta-Alvear,D., Sharan,R., Kluger,Y. and Dynlacht,B. D. (2005) An initial blueprint for myogenic differentiation. Genes Dev., 19, 553-569.
4. Cao,Y., Yao,Z., Sarkar,D., Lawrence,M., Sanchez,G. J., Parker,M. H., MacQuarrie,K. L., Davison,J., Morgan,M. T., Ruzzo,W. L. et al. (2010) Genome-wide MyoD binding in skeletal muscle cells: a potential for broad cellular reprogramming. Dev. Cell, 18, 662-674.
5. Dekker,J., Rippe,K., Dekker,M. and Kleckner,N. (2002) Capturing chromosome conformation. Science, 295, 1306-1311.
6. Sanyal,A., Bau,D., Marti-Renom,M. A. and Dekker,J. (2011) Chromatin globules: a common motif of higher order chromosome structure? Curr. Opin. Cell Biol., 23, 325-331.
7. Ethier,S. D.,Miura,H. and Dostie,J. (2011) Discovering genome regulation with 3C and 3C-related technologies. Biochim. Biophys. Acta, 1819, 401-410.
8. Hakim,O., Sung,M. H. and Hager,G. L. (2010) 3D shortcuts to gene regulation. Curr. Opin. Cell Biol., 22, 305-313.
9. Cope,N. F., Fraser,P. and Eskiw,C. H. (2010) The yin and yang of chromatin spatial organization. Genome Biol., 11, 204.
10. Williams,A., Spilianakis,C. G. and Flavell,R. A. (2010) Interchromosomal association and gene regulation in trans. Trends Genet., 26, 188-197.
11. Zhang,Y., McCord,R. P., Ho,Y. J., Lajoie,B. R., Hildebrand,D. G., Simon,A. C., Becker,M. S., Alt,F. W. and Dekker,J. (2012) Spatial organization of the mouse genome and its role in recurrent chromosomal translocations. Cell, 148, 908-921.
12. Osborne,C. S., Chakalova,L.,Mitchell,J. A., Horton,A., Wood,A. L., Bolland,D. J., Corcoran,A. E. and Fraser,P. (2007) Myc dynamically and preferentially relocates to a transcription factory occupied by Igh. PLoS Biol., 5, e192.
13. Hakim,O., Resch,W., Yamane,A., Klein,I., Kieffer-Kwon,K. R., Jankovic,M., Oliveira,T., Bothmer,A., Voss,T. C., Ansarah-Sobrinho,C. et al. (2012) DNA damage defines sites of recurrent chromosomal translocations in B lymphocytes. Nature, 484, 69-74.
14. Fanucchi,S., Shibayama,Y., Burd,S., Weinberg,M. S. and Mhlanga,M. M. (2013) Chromosomal contact permits transcription between coregulated genes. Cell, 155, 606-620.
15. Park,S. K., Xiang,Y., Feng,X. and Garrard,W. T. (2014) Pronounced cohabitation of active immunoglobulin genes from three different chromosomes in transcription factories during maximal antibody synthesis. Genes Dev., 28, 1159-1164.
16. Zhang,Y., McCord,R. P., Ho,Y. J., Lajoie,B. R., Hildebrand,D. G., Simon,A. C., Becker,M. S., Alt,F. W. and Dekker,J. (2012) Spatial organization of the mouse genome and its role in recurrent chromosomal translocations. Cell, 148, 908-921.
17. McNeil,J. A., Johnson,C. V., Carter,K. C., Singer,R. H. and Lawrence,J. B. (1991) Localizing DNA and RNA within nuclei and chromosomes by fluorescence in situ hybridization. Genet. Anal. Tech. Appl., 8, 41-58.
18. de La Serna,I. L., Carlson,K. A., Hill,D. A., Guidi,C. J., Stephenson,R. O., Sif,S., Kingston,R. E. and Imbalzano,A. N. (2000) Mammalian SWI-SNF complexes contribute to activation of the hsp70 gene. Mol . Cell. Biol., 20, 2839-2851.
19. Novitch,B. G., Mulligan,G. J., Jacks,T. and Lassar,A. B. (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.
20. de la Serna,I. L., Carlson,K. A. and Imbalzano,A. N. (2001) Mammalian SWI/SNF complexes promote MyoD-mediated muscle differentiation. Nat. Genet., 27, 187-190.
21. Harada,A., Okada,S., Konno,D., Odawara,J., Yoshimi,T., Yoshimura,S., Kumamaru,H., Saiwai,H., Tsubota,T., Kurumizaka,H. et al. (2012) Chd2 interacts with H3. 3 to determine myogenic cell fate. EMBO J., 31, 2994-3007.
22. de la Serna,I. L., Ohkawa,Y., Berkes,C. A., Bergstrom,D. A., Dacwag,C. S., Tapscott,S. J. and Imbalzano,A. N. (2005) MyoD targets chromatin remodeling complexes to the myogenin locus prior to forming a stable DNA-bound complex. Mol. Cell. Biol., 25, 3997-4009.
23. Bergstrom,D. A., Penn,B. H., Strand,A., Perry,R. L., Rudnicki,M. A. and Tapscott,S. J. (2002) Promoter-specific regulation of MyoD binding and signal transduction cooperate to pattern gene expression. Mol. Cell, 9, 587-600.
24. Ohkawa,Y., Harada,A., Nakamura,M., Yoshimura,S. and Tachibana,T. (2009) Production of a rat monoclonal antibody against Brg1. Hybridoma (Larchmt), 28, 463-466.
25. Clemson,C. M., McNeil,J. A., Willard,H. F. and Lawrence,J. B. (1996) XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. J. Cell. Biol., 132, 259-275.
26. Lawrence,J. B., Singer,R. H. and Marselle,L. M. (1989) Highly localized tracks of specific transcripts within interphase nuclei visualized by in situ hybridization. Cell, 57, 493-502.
27. Tam,R., Smith,K. P. and Lawrence,J. B. (2004) The 4q subtelomere harboring the FSHD locus is specifically anchored with peripheral heterochromatin unlike most human telomeres. J. Cell Biol., 167, 269-279.
28. Liang,K. Y. and Zeger,S. L. (1986) Longitudinal data analysis using generalized linear models. Biometrika, 73, 13-22.
29. Wolfinger,R. and O'Connell,M. (1993) Generalized linear mixed models: a pseudo-likelihood approach. J. Statist. Comput. Simul., 48, 233-243.
30. McCullagh,P. and Nelder,J. A. (1989) Generalized Linear Models. 2nd edn. Chapman and Hall, London
31. Hosmer,D. W. and Lemeshow,S. (1989) Applied Logistic Regression. John Wiley and Sons, Inc., NY
32. SAS. (2008) SAS/STAT 9. 2 User's Guide, Chapter 38: The GLIMMIX Procedure. SAS Publishing, Cary, NC
33. Mantel,N. and Byar,D. P. (1978) Marginal homogeneity, symmetry and independence. Commun. Stat. A-Theory Methods, 7, 953-976.
34. Shafer,G. and Olkin,I. (1983) Adjusting p values to account for selection over dichotomies. J. Am. Stat. Assoc., 78, 674-678.
35. Davis,R. L.,Weintraub,H. and Lassar,A. B. (1987) Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell, 51, 987-1000.
36. Furst,D. O., Osborn,M. and Weber,K. (1989) Myogenesis in the mouse embryo: differential onset of expression of myogenic proteins and the involvement of titin in myofibril assembly. J. Cell Biol., 109, 517-527.
37. Schaart,G., Viebahn,C., Langmann,W. and Ramaekers,F. (1989) Desmin and titin expression in early postimplantation mouse embryos. Development, 107, 585-596.
38. Londhe,P. and Davie,J. K. (2011) Sequential association of myogenic regulatory factors and E proteins at muscle-specific genes. Skeletal Muscle, 1, 14.
39. Li,H., Choudhary,S. K.,Milner,D. J., Munir,M. I., Kuisk,I. R. and Capetanaki,Y. (1994) Inhibition of desmin expression blocks myoblast fusion and interferes with the myogenic regulators MyoD and myogenin. J. Cell Biol., 124, 827-841.
40. Li,Z. L. and Paulin,D. (1991) High level desmin expression depends on a muscle-specific enhancer. J. Biol. Chem., 266, 6562-6570.
41. Li,H. and Capetanaki,Y. (1993) Regulation of the mouse desmin gene: transactivated by MyoD, myogenin, MRF4 and Myf5. Nucleic Acids Res., 21, 335-343.
42. Chang,B. H., Smith,L., Huang,J. and Thayer,M. (2007) Chromosomes with delayed replication timing lead to checkpoint activation, delayed recruitment of Aurora B and chromosome instability. Oncogene, 26, 1852-1861.
43. Casas-Delucchi,C. S., Brero,A., Rahn,H. P., Solovei,I.,Wutz,A., Cremer,T., Leonhardt,H. and Cardoso,M. C. (2011) Histone acetylation controls the inactive X chromosome replication dynamics. Nat. Commun., 2, 222.
44. Imbalzano,A. N., Kwon,H., Green,M. R. and Kingston,R. E. (1994) Facilitated binding of TATA-binding protein to nucleosomal DNA. Nature, 370, 481-485.
45. Kwon,H., Imbalzano,A. N., Khavari,P. A., Kingston,R. E. and Green,M. R. (1994) Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex. Nature, 370, 477-481.
46. Wang,W., Cote,J., Xue,Y., Zhou,S., Khavari,P. A., Biggar,S. R., Muchardt,C., Kalpana,G. V., Goff,S. P., Yaniv,M. et al. (1996) Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. EMBO J, 15, 5370-5382.
47. 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 muscle-specific loci. Nat. Genet., 36, 738-743.
48. Khavari,P. A., Peterson,C. L., Tamkun,J. W., Mendel,D. B. and Crabtree,G. R. (1993) BRG1 contains a conserved domain of the SWI2/SNF2 family necessary for normal mitotic growth and transcription. Nature, 366, 170-174.
49. Ohkawa,Y., Yoshimura,S., Higashi,C., Marfella,C. G., Dacwag,C. S., Tachibana,T. and Imbalzano,A. N. (2007) Myogenin and the SWI/SNF ATPase Brg1 maintain myogenic gene expression at different stages of skeletal myogenesis. J. Biol. Chem., 282, 6564-6570.
50. Simonis,M., Klous,P., Splinter,E., Moshkin,Y., Willemsen,R., de Wit,E., van Steensel,B. and de Laat,W. (2006) Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat. Genet., 38, 1348-1354.
51. Zhao,Z., Tavoosidana,G., Sjolinder,M., Gondor,A., Mariano,P., Wang,S., Kanduri,C., Lezcano,M., Sandhu,K. S., Singh,U. et al. (2006) Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra-and interchromosomal interactions. Nat. Genet., 38, 1341-1347.
52. Schoenfelder,S., Sexton,T., Chakalova,L., Cope,N. F., Horton,A., Andrews,S., Kurukuti,S., Mitchell,J. A., Umlauf,D., Dimitrova,D. S. et al. (2010) Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat. Genet., 42, 53-61.
53. Zhang,C., Kho,Y. S., Wang,Z., Chiang,Y. T., Ng,G. K., Shaw,P. C., Wang,Y. and Qi,R. Z. (2014) Transmembrane and coiled-coil domain family 1 is a novel protein of the endoplasmic reticulum. PLoS One, 9, e85206.
54. Yoneyama,S., Guo,Y., Lanktree,M. B., Barnes,M. R., Elbers,C. C., Karczewski,K. J., Padmanabhan,S., Bauer,F., Baumert,J., Beitelshees,A. et al. (2014) Gene-centric meta-analyses for central adiposity traits in up to 57 412 individuals of European descent confirm known loci and reveal several novel associations. Hum. Mol. Genet., 23, 2498-2510.
55. Cho,O. H., Mallappa,C., Hernandez-Hernandez,J. M., Rivera-Perez,J. A. and Imbalzano,A. N. (2015) Contrasting roles for MyoD in organizing myogenic promoter structures during embryonic skeletal muscle development. Dev. Dyn., 244, 43-55.
56. 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.
57. Apostolou,E. and Thanos,D. (2008) Virus Infection Induces NF-kappaB-dependent interchromosomal associations mediating monoallelic IFN-beta gene expression. Cell, 134, 85-96.
58. Hu,Q., Kwon,Y. S., Nunez,E., Cardamone,M. D., Hutt,K. R., Ohgi,K. A., Garcia-Bassets,I., Rose,D. W., Glass,C. K., Rosenfeld,M. G. et al. (2008) Enhancing nuclear receptor-induced transcription requires nuclear motor and LSD1-dependent gene networking in interchromatin granules. Proc. Natl. Acad. Sci. U. S. A., 105, 19199-19204.
59. Lomvardas,S., Barnea,G., Pisapia,D. J., Mendelsohn,M., Kirkland,J. and Axel,R. (2006) Interchromosomal interactions and olfactory receptor choice. Cell, 126, 403-413.
60. Fullwood,M. J., Liu,M. H., Pan,Y. F., Liu,J., Xu,H., Mohamed,Y. B., Orlov,Y. L., Velkov,S., Ho,A., Mei,P. H. et al. (2009) An oestrogen-receptor-alpha-bound human chromatin interactome. Nature, 462, 58-64.
61. Li,G., Ruan,X., Auerbach,R. K., Sandhu,K. S., Zheng,M., Wang,P., Poh,H. M., Goh,Y., Lim,J., Zhang,J. et al. (2012) Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell, 148, 84-98.
62. Handoko,L., Xu,H., Li,G., Ngan,C. Y., Chew,E., Schnapp,M., Lee,C. W., Ye,C., Ping,J. L., Mulawadi,F. et al. (2011) CTCF-mediated functional chromatin interactome in pluripotent cells. Nat. Genet., 43, 630-638.
63. Spilianakis,C. G., Lalioti,M. D., Town,T., Lee,G. R. and Flavell,R. A. (2005) Interchromosomal associations between alternatively expressed loci. Nature, 435, 637-645.
64. Rudnicki,M. A., Schnegelsberg,P. N., Stead,R. H., Braun,T., Arnold,H. H. and Jaenisch,R. (1993) MyoD or Myf-5 is required for the formation of skeletal muscle. Cell, 75, 1351-1359.
65. Rudnicki,M. A., Braun,T., Hinuma,S. and Jaenisch,R. (1992) Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell, 71, 383-390.
66. Braun,T., Buschhausen-Denker,G., Bober,E., Tannich,E. and Arnold,H. H. (1989) A novel human muscle factor related to but distinct from MyoD1 induces myogenic conversion in 10T1/2 fibroblasts. EMBO J., 8, 701-709.
67. Roy,K., de la Serna,I. L. and Imbalzano,A. N. (2002) The myogenic basic helix-loop-helix family of transcription factors shows similar requirements for SWI/SNF chromatin remodeling enzymes during muscle differentiation in culture. J. Biol. Chem., 277, 33818-33824.
68. Hasty,P., Bradley,A., Morris,J. H., Edmondson,D. G., Venuti,J. M., Olson,E. N. and Klein,W. H. (1993) Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature, 364, 501-506.
69. Nabeshima,Y., Hanaoka,K., Hayasaka,M., Esumi,E., Li,S. and Nonaka,I. (1993) Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature, 364, 532-535.
70. Papantonis,A. and Cook,P. R. (2013) Transcription factories: genome organization and gene regulation. Chem. Rev., 113, 8683-8705.
71. Edelman,L. B. and Fraser,P. (2012) Transcription factories: genetic programming in three dimensions. Curre. Opin. Genet. Dev., 22, 110-114.
72. Badeaux,A. I. and Shi,Y. (2013) Emerging roles for chromatin as a signal integration and storage platform. Nat. Rev. Mol. Cell Biol., 14, 211-224.
73. LeBlanc,S. E.,Wu,Q., Barutcu,A. R., Xiao,H., Ohkawa,Y. and Imbalzano,A. N. (2014) The PPARgamma locus makes long-range chromatin interactions with selected tissue-specific gene loci during adipocyte differentiation in a protein kinase A dependent manner. PLoS One, 9, e86140.
74. Papantonis,A., Kohro,T., Baboo,S., Larkin,J. D., Deng,B., Short,P., Tsutsumi,S., Taylor,S., Kanki,Y., Kobayashi,M. et al. (2012) TNFalpha signals through specialized factories where responsive coding and miRNA genes are transcribed. EMBO J., 31, 4404-4414.
75. Knight,J. D. and Kothary,R. (2011) The myogenic kinome: protein kinases critical to mammalian skeletal myogenesis. Skeletal Muscle, 1, 29.
76. Aziz,A., Sebastian,S. and Dilworth,F. J. (2012) The origin and fate of muscle satellite cells. Stem Cell Rev., 8, 609-622.
77. Forcales,S. V., 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.
78. Keren,A., Tamir,Y. and Bengal,E. (2006) The p38 MAPK signaling pathway: a major regulator of skeletal muscle development. Mol. Cell. Endocrinol., 252, 224-230.
79. 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.
80. Cai,S., Lee,C. C. and Kohwi-Shigematsu,T. (2006) SATB1 packages densely looped, transcriptionally active chromatin for coordinated expression of cytokine genes. Nat. Genet., 38, 1278-1288.
81. Kim,S. I., Bresnick,E. H. and Bultman,S. J. (2009) BRG1 directly regulates nucleosome structure and chromatin looping of the alpha globin locus to activate transcription. Nucleic Acids Res., 37, 6019-6027.
82. Kim,S. I., Bultman,S. J., Kiefer,C. M., Dean,A. and Bresnick,E. H. (2009) BRG1 requirement for long-range interaction of a locus control region with a downstream promoter. Proc . Natl. Acad. Sci. U. S. A., 106, 2259-2264.
83. Ni,Z., Abou El Hassan,M., Xu,Z., Yu,T. and Bremner,R. (2008) The chromatin-remodeling enzyme BRG1 coordinates CIITA induction through many interdependent distal enhancers. Nat. Immunol., 9, 785-793.
84. Euskirchen,G. M., Auerbach,R. K., Davidov,E., Gianoulis,T. A., Zhong,G., Rozowsky,J., Bhardwaj,N., Gerstein,M. B. and Snyder,M. (2011) Diverse roles and interactions of the SWI/SNF chromatin remodeling complex revealed using global approaches. PLoS Genet., 7, e1002008.
85. Muchardt,C. and 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.
86. Hakim,O., Sung,M. H., Voss,T. C., Splinter,E., John,S., Sabo,P. J., Thurman,R. E., Stamatoyannopoulos,J. A., de Laat,W. and Hager,G. L. (2011) Diverse gene reprogramming events occur in the same spatial clusters of distal regulatory elements. Genome Res., 21, 697-706.