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Comparative and Functional Genomics
Volume 2012 (2012), Article ID 256892, 12 pages
http://dx.doi.org/10.1155/2012/256892
Review Article

Epigenetic Alterations in Muscular Disorders

CNR Institute of Cellular Biology and Neurobiology, IRCCS Santa Lucia Foundation, Via Del Fosso di Fiorano 64, 00143 Rome, Italy

Received 2 February 2012; Revised 11 April 2012; Accepted 19 April 2012

Academic Editor: Daniela Palacios

Copyright © 2012 Chiara Lanzuolo. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. Beisel and R. Paro, “Silencing chromatin: comparing modes and mechanisms,” Nature Reviews Genetics, vol. 12, no. 2, pp. 123–135, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. E. I. Campos and D. Reinberg, “Histones: annotating chromatin,” Annual Review of Genetics, vol. 43, pp. 559–599, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. A. M. Deaton and A. Bird, “CpG islands and the regulation of transcription,” Genes and Development, vol. 25, no. 10, pp. 1010–1022, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. C. Lanzuolo and V. Orlando, “The function of the epigenome in cell reprogramming,” Cellular and Molecular Life Sciences, vol. 64, no. 9, pp. 1043–1062, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. Y. S. Mao, B. Zhang, and D. L. Spector, “Biogenesis and function of nuclear bodies,” Trends in Genetics, vol. 27, no. 8, pp. 295–306, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. S. B. Baylin and P. A. Jones, “A decade of exploring the cancer epigenome—biological and translational implications,” Nature Reviews Cancer, vol. 11, pp. 726–773, 2011. View at Google Scholar
  7. S. R. Bhaumik, E. Smith, and A. Shilatifard, “Covalent modifications of histones during development and disease pathogenesis,” Nature Structural and Molecular Biology, vol. 14, no. 11, pp. 1008–1016, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. Z. Siegfried, S. Eden, M. Mendelsohn, X. Feng, B. Z. Tsuberi, and H. Cedar, “DNA methylation represses transcription in vivo,” Nature Genetics, vol. 22, no. 2, pp. 203–206, 1999. View at Publisher · View at Google Scholar · View at Scopus
  9. Y. Q. Feng, R. Desprat, H. Fu et al., “DNA methylation supports intrinsic epigenetic memory in mammalian cells,” PLoS Genetics, vol. 2, no. 4, article e65, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Bird, M. Taggart, M. Frommer, O. J. Miller, and D. Macleod, “A fraction of the mouse genome that is derived from islands of nonmethylated, CpG-rich DNA,” Cell, vol. 40, no. 1, pp. 91–99, 1985. View at Google Scholar · View at Scopus
  11. R. S. Illingworth and A. P. Bird, “CpG islands—“a rough guide”,” FEBS Letters, vol. 583, no. 11, pp. 1713–1720, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. R. S. Illingworth, U. Gruenewald-Schneider, S. Webb et al., “Orphan CpG Islands Identify numerous conserved promoters in the mammalian genome,” PLoS Genetics, vol. 6, no. 9, article e1001134, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Kriaucionis and N. Heintz, “The nuclear DNA base 5-hydroxymethylcytosine is present in purkinje neurons and the brain,” Science, vol. 324, no. 5929, pp. 929–930, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Tahiliani, K. P. Koh, Y. Shen et al., “Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1,” Science, vol. 324, no. 5929, pp. 930–935, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Ito, A. C. D’Alessio, O. V. Taranova, K. Hong, L. C. Sowers, and Y. Zhang, “Role of tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification,” Nature, vol. 466, no. 7310, pp. 1129–1133, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. P. Zhang, L. Su, Z. Wang, S. Zhang, J. Guan et al., “The involvement of 5-hydroxymethylcytosine in active DNA demethylation in mice,” Biology of Reproduction, vol. 86, no. 4, p. 104, 2012. View at Google Scholar
  17. A. Munshi, G. Shafi, N. Aliya, and A. Jyothy, “Histone modifications dictate specific biological readouts,” Journal of Genetics and Genomics, vol. 36, no. 2, pp. 75–88, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Altaf, N. Saksouk, and J. Côté, “Histone modifications in response to DNA damage,” Mutation Research, vol. 618, no. 1-2, pp. 81–90, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. O. Bell, M. Schwaiger, E. J. Oakeley et al., “Accessibility of the Drosophila genome discriminates PcG repression, H4K16 acetylation and replication timing,” Nature Structural and Molecular Biology, vol. 17, no. 7, pp. 894–900, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. B. E. Bernstein, M. Kamal, K. Lindblad-Toh et al., “Genomic maps and comparative analysis of histone modifications in human and mouse,” Cell, vol. 120, no. 2, pp. 169–181, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. M. L. Eaton, J. A. Prinz, H. K. MacAlpine, G. Tretyakov, P. V. Kharchenko, and D. M. MacAlpine, “Chromatin signatures of the Drosophila replication program,” Genome Research, vol. 21, no. 2, pp. 164–174, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. G. J. Filion, J. G. van Bemmel, U. Braunschweig, W. Talhout, and J. Kind, “Systematic protein location mapping reveals five principal chromatin types in Drosophila cells,” Cell, vol. 143, pp. 212–224, 2010. View at Google Scholar
  23. V. Krishnan, M. Z. Y. Chow, Z. Wang et al., “Histone H4 lysine 16 hypoacetylation is associated with defective DNA repair and premature senescence in Zmpste24-deficient mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 30, pp. 12325–12330, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Schübeler, D. M. MacAlpine, D. Scalzo et al., “The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote,” Genes and Development, vol. 18, no. 11, pp. 1263–1271, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Henikoff and K. Ahmad, “Assembly of variant histones into chromatin,” Annual Review of Cell and Developmental Biology, vol. 21, pp. 133–153, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Schuettengruber, A. M. Martinez, N. Iovino, and G. Cavalli, “Trithorax group proteins: switching genes on and keeping them active,” Nature Reviews Molecular Cell Biology, vol. 12, pp. 799–814, 2011. View at Google Scholar
  27. E. Splinter and W. de Laat, “The complex transcription regulatory landscape of our genome: control in three dimensions,” EMBO Journal, vol. 30, pp. 4345–4355, 2011. View at Google Scholar
  28. G. Li and D. Reinberg, “Chromatin higher-order structures and gene regulation,” Current Opinion in Genetics and Development, vol. 21, no. 2, pp. 175–186, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. P. Fraser and W. Bickmore, “Nuclear organization of the genome and the potential for gene regulation,” Nature, vol. 447, no. 7143, pp. 413–417, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. C. Lanctôt, T. Cheutin, M. Cremer, G. Cavalli, and T. Cremer, “Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions,” Nature Reviews Genetics, vol. 8, no. 2, pp. 104–115, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. E. Soutoglou and T. Misteli, “Mobility and immobility of chromatin in transcription and genome stability,” Current Opinion in Genetics and Development, vol. 17, no. 5, pp. 435–442, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Schoenfelder, I. Clay, and P. Fraser, “The transcriptional interactome: gene expression in 3D,” Current Opinion in Genetics and Development, vol. 20, no. 2, pp. 127–133, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. T. Klymenko, B. Papp, W. Fischle et al., “A polycomb group protein complex with sequence-specific DNA-binding and selective methyl-lysine-binding activities,” Genes and Development, vol. 20, no. 9, pp. 1110–1122, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. J. C. Scheuermann, A. G. de Ayala Alonso, K. Oktaba et al., “Histone H2A deubiquitinase activity of the Polycomb repressive complex PR-DUB,” Nature, vol. 465, no. 7295, pp. 243–247, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. R. Cao, L. Wang, H. Wang et al., “Role of histone H3 lysine 27 methylation in polycomb-group silencing,” Science, vol. 298, no. 5595, pp. 1039–1043, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. B. Czermin, R. Melfi, D. McCabe, V. Seitz, A. Imhof, and V. Pirrotta, “Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites,” Cell, vol. 111, no. 2, pp. 185–196, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Kuzmichev, K. Nishioka, H. Erdjument-Bromage, P. Tempst, and D. Reinberg, “Histone methyltransferase activity associated with a human multiprotein complex containing the enhancer of zeste protein,” Genes and Development, vol. 16, no. 22, pp. 2893–2905, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. J. Müller, C. M. Hart, N. J. Francis et al., “Histone methyltransferase activity of a Drosophila Polycomb group repressor complex,” Cell, vol. 111, no. 2, pp. 197–208, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. H. Wang, L. Wang, H. Erdjument-Bromage et al., “Role of histone H2A ubiquitination in Polycomb silencing,” Nature, vol. 431, no. 7010, pp. 873–878, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Ku, R. P. Koche, E. Rheinbay et al., “Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains,” PLoS Genetics, vol. 4, no. 10, article e1000242, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Schoeftner, A. K. Sengupta, S. Kubicek et al., “Recruitment of PRC1 function at the initiation of X inactivation independent of PRC2 and silencing,” EMBO Journal, vol. 25, no. 13, pp. 3110–3122, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. D. Cmarko, P. J. Verschure, A. P. Otte, R. van Driel, and S. Fakan, “Polycomb group gene silencing proteins are concentrated in the perichromatin compartment of the mammalian nucleus,” Journal of Cell Science, vol. 116, no. 2, pp. 335–343, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. F. Bantignies, V. Roure, I. Comet et al., “Polycomb-dependent regulatory contacts between distant hox loci in drosophila,” Cell, vol. 144, no. 2, pp. 214–226, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Lanzuolo, V. Roure, J. Dekker, F. Bantignies, and V. Orlando, “Polycomb response elements mediate the formation of chromosome higher-order structures in the bithorax complex,” Nature Cell Biology, vol. 9, no. 10, pp. 1167–1174, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. F. Cléard, Y. Moshkin, F. Karch, and R. K. Maeda, “Probing long-distance regulatory interactions in the Drosophila melanogaster bithorax complex using Dam identification,” Nature Genetics, vol. 38, no. 8, pp. 931–935, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. T. Sexton, E. Yaffe, E. Kenigsberg, F. Bantignies, and B. Leblanc, “Three-dimensional folding and functional organization principles of the Drosophila genome,” Cell, vol. 148, pp. 458–472, 2012. View at Google Scholar
  47. S. Kheradmand Kia, P. Solaimani Kartalaei, E. Farahbakhshian, F. Pourfarzad, and M. von Lindern, “EZH2-dependent chromatin looping controls INK4a and INK4b, but not ARF, during human progenitor cell differentiation and cellular senescence,” Epigenetics & Chromatin, vol. 2, no. 1, p. 16, 2009. View at Google Scholar
  48. D. Noordermeer, M. Leleu, E. Splinter, J. Rougemont, and W. De Laat, “The dynamic architecture of Hox gene clusters,” Science, vol. 334, pp. 222–225, 2011. View at Google Scholar
  49. V. K. Tiwari, K. M. McGarvey, J. D. F. Licchesi et al., “PcG proteins, DNA methylation, and gene repression by chromatin looping,” PLoS Biology, vol. 6, no. 12, pp. 2911–2927, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. K. H. Hansen, A. P. Bracken, D. Pasini et al., “A model for transmission of the H3K27me3 epigenetic mark,” Nature Cell Biology, vol. 10, no. 11, pp. 1291–1300, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. R. Margueron, N. Justin, K. Ohno et al., “Role of the polycomb protein EED in the propagation of repressive histone marks,” Nature, vol. 461, no. 7265, pp. 762–767, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Chen, L. R. Bohrer, A. N. Rai et al., “Cyclin-dependent kinases regulate epigenetic gene silencing through phosphorylation of EZH2,” Nature Cell Biology, vol. 12, no. 11, pp. 1108–1114, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Kaneko, G. Li, J. Son et al., “Phosphorylation of the PRC2 component Ezh2 is cell cycle-regulated and up-regulates its binding to ncRNA,” Genes and Development, vol. 24, no. 23, pp. 2615–2620, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. C. Lanzuolo, F. Lo Sardo, A. Diamantini, and V. Orlando, “PcG complexes set the stage for epigenetic inheritance of gene silencing in early S phase before replication,” PLoS Genetics, vol. 7, article e1002370, 2011. View at Google Scholar
  55. C. Lanzuolo, F. Lo Sardo, and V. Orlando, “Concerted epigenetic signatures inheritance at PcG targets through replication,” Cell Cycle, vol. 11, no. 7, pp. 1296–1300, 2012. View at Google Scholar
  56. N. Brockdorff, “Chromosome silencing mechanisms in X-chromosome inactivation: unknown unknowns,” Development, vol. 138, pp. 5057–5065, 2011. View at Google Scholar
  57. C. Prezioso and V. Orlando, “Polycomb proteins in mammalian cell differentiation and plasticity,” FEBS Letters, vol. 585, no. 13, pp. 2067–2077, 2011. View at Publisher · View at Google Scholar · View at Scopus
  58. C. L. Fisher and A. G. Fisher, “Chromatin states in pluripotent, differentiated, and reprogrammed cells,” Current Opinion in Genetics and Development, vol. 21, no. 2, pp. 140–146, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. R. Margueron and D. Reinberg, “The Polycomb complex PRC2 and its mark in life,” Nature, vol. 469, no. 7330, pp. 343–349, 2011. View at Publisher · View at Google Scholar · View at Scopus
  60. M. C. Trask and J. Mager, “Complexity of polycomb group function: diverse mechanisms of target specificity,” Journal of Cellular Physiology, vol. 226, no. 7, pp. 1719–1721, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. K. Williams, J. Christensen, M. T. Pedersen et al., “TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity,” Nature, vol. 473, no. 7347, pp. 343–349, 2011. View at Publisher · View at Google Scholar · View at Scopus
  62. H. Wu, A. C. D'Alessio, S. Ito et al., “Dual functions of Tet1 in transcriptional regulation in mouse embryonic stem cells,” Nature, vol. 473, no. 7347, pp. 389–394, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. H. Wu, A. C. D'Alessio, S. Ito et al., “Genome-wide analysis of 5-hydroxymethylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells,” Genes and Development, vol. 25, no. 7, pp. 679–684, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. K. E. Davies and K. J. Nowak, “Molecular mechanisms of muscular dystrophies: old and new players,” Nature Reviews Molecular Cell Biology, vol. 7, no. 10, pp. 762–773, 2006. View at Publisher · View at Google Scholar · View at Scopus
  65. K. Matsumura, F. M. S. Tome, H. Collin et al., “Expression of dystrophin-associated proteins in dystrophin-positive muscle fibers (revertants) in Duchenne muscular dystrophy,” Neuromuscular Disorders, vol. 4, no. 2, pp. 115–120, 1994. View at Publisher · View at Google Scholar · View at Scopus
  66. J. M. Ervasti and K. J. Sonnemann, “Biology of the Striated Muscle Dystrophin-Glycoprotein Complex,” International Review of Cytology, vol. 265, pp. 191–225, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. C. Colussi, C. Mozzetta, A. Gurtner et al., “HDAC2 blockade by nitric oxide and histone deacetylase inhibitors reveals a common target in Duchenne muscular dystrophy treatment,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 49, pp. 19183–19187, 2008. View at Publisher · View at Google Scholar · View at Scopus
  68. D. Cacchiarelli, J. Martone, E. Girardi et al., “MicroRNAs involved in molecular circuitries relevant for the duchenne muscular dystrophy pathogenesis are controlled by the dystrophin/nNOS pathway,” Cell Metabolism, vol. 12, no. 4, pp. 341–351, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. D. Cacchiarelli, T. Incitti, J. Martone et al., “MiR-31 modulates dystrophin expression: new implications for Duchenne muscular dystrophy therapy,” EMBO Reports, vol. 12, no. 2, pp. 136–141, 2011. View at Publisher · View at Google Scholar · View at Scopus
  70. G. C. Minetti, C. Colussi, R. Adami et al., “Functional and morphological recovery of dystrophic muscles in mice treated with deacetylase inhibitors,” Nature Medicine, vol. 12, no. 10, pp. 1147–1150, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. S. Consalvi, V. Saccone, L. Giordani, G. Minetti, C. Mozzetta, and P. L. Puri, “Histone deacetylase inhibitors in the treatment of muscular dystrophies: epigenetic drugs for genetic diseases,” Molecular Medicine, vol. 17, no. 5-6, pp. 457–465, 2011. View at Publisher · View at Google Scholar · View at Scopus
  72. M. Gomes-Pereira, T. A. Cooper, and G. Gourdon, “Myotonic dystrophy mouse models: towards rational therapy development,” Trends in Molecular Medicine, vol. 17, no. 9, pp. 506–517, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. J. W. Day and L. P. W. Ranum, “RNA pathogenesis of the myotonic dystrophies,” Neuromuscular Disorders, vol. 15, no. 1, pp. 5–16, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. L. A. Boyer, K. Plath, J. Zeitlinger et al., “Polycomb complexes repress developmental regulators in murine embryonic stem cells,” Nature, vol. 441, no. 7091, pp. 349–353, 2006. View at Publisher · View at Google Scholar · View at Scopus
  75. A. P. Bracken, N. Dietrich, D. Pasini, K. H. Hansen, and K. Helin, “Genome-wide mapping of polycomb target genes unravels their roles in cell fate transitions,” Genes and Development, vol. 20, no. 9, pp. 1123–1136, 2006. View at Publisher · View at Google Scholar · View at Scopus
  76. T. I. Lee, R. G. Jenner, L. A. Boyer et al., “Control of developmental regulators by polycomb in human embryonic stem cells,” Cell, vol. 125, no. 2, pp. 301–313, 2006. View at Publisher · View at Google Scholar · View at Scopus
  77. N. Nègre, J. Hennetin, L. V. Sun et al., “Chromosomal distribution of PcG proteins during Drosophila development,” PLoS Biology, vol. 4, no. 6, article e170, 2006. View at Publisher · View at Google Scholar · View at Scopus
  78. Y. B. Schwartz, T. G. Kahn, D. A. Nix et al., “Genome-wide analysis of Polycomb targets in Drosophila melanogaster,” Nature Genetics, vol. 38, no. 6, pp. 700–705, 2006. View at Publisher · View at Google Scholar · View at Scopus
  79. S. L. Squazzo, H. O'Geen, V. M. Komashko et al., “Suz12 binds to silenced regions of the genome in a cell-type-specific manner,” Genome Research, vol. 16, no. 7, pp. 890–900, 2006. View at Publisher · View at Google Scholar · View at Scopus
  80. B. Tolhuis, I. Muijrers, E. De Wit et al., “Genome-wide profiling of PRC1 and PRC2 Polycomb chromatin binding in Drosophila melanogaster,” Nature Genetics, vol. 38, no. 6, pp. 694–699, 2006. View at Publisher · View at Google Scholar · View at Scopus
  81. P. Asp, R. Blum, V. Vethantham et al., “Genome-wide remodeling of the epigenetic landscape during myogenic differentiation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 22, pp. E149–E158, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. 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 and Development, vol. 18, pp. 2627–2638, 2004. View at Google Scholar
  83. A. H. Juan, R. M. Kumar, J. G. Marx, R. A. Young, and V. Sartorelli, “Mir-214-dependent regulation of the polycomb protein Ezh2 in skeletal muscle and embryonic stem cells,” Molecular Cell, vol. 36, no. 1, pp. 61–74, 2009. View at Publisher · View at Google Scholar · View at Scopus
  84. L. Stojic, Z. Jasencakova, C. Prezioso, A. Stutzer, and B. Bodega, “Chromatin regulated interchange between polycomb repressive complex 2 (PRC2)-Ezh2 and PRC2-Ezh1 complexes controls myogenin activation in skeletal muscle cells,” Epigenetics Chromatin, vol. 4, article 16, 2011. View at Google Scholar
  85. A. H. Juan, A. Derfoul, X. Feng et al., “Polycomb EZH2 controls self-renewal and safeguards the transcriptional identity of skeletal muscle stem cells,” Genes and Development, vol. 25, no. 8, pp. 789–794, 2011. View at Publisher · View at Google Scholar · View at Scopus
  86. M. Cesana, D. Cacchiarelli, I. Legnini, T. Santini, and O. Sthandier, “A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA,” Cell, vol. 147, pp. 358–369, 2011. View at Google Scholar
  87. M. V. Neguembor and D. Gabellini, “In junk we trust: repetitive DNA, epigenetics and facioscapulohumeral muscular dystrophy,” Epigenomics, vol. 2, no. 2, pp. 271–287, 2010. View at Publisher · View at Google Scholar · View at Scopus
  88. D. Palacios, C. Mozzetta, S. Consalvi et al., “TNF/p38α/polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration,” Cell Stem Cell, vol. 7, no. 4, pp. 455–469, 2010. View at Publisher · View at Google Scholar · View at Scopus
  89. A. Mattout, B. L. Pike, B. D. Towbin, E. M. Bank, A. Gonzalez-Sandoval, and et al., “An EDMD mutation in C. elegans lamin blocks muscle-specific gene relocation and compromises muscle integrity,” Current Biology, vol. 21, pp. 1603–1614, 2011. View at Google Scholar
  90. R. Tawil and S. M. Van Der Maarel, “Facioscapulohumeral muscular dystrophy,” Muscle and Nerve, vol. 34, no. 1, pp. 1–15, 2006. View at Publisher · View at Google Scholar · View at Scopus
  91. R. Tawil, D. Storvick, T. E. Feasby, B. Weiffenbach, and R. C. Griggs, “Extreme variability of expression in monozygotic twins with FSH muscular dystrophy,” Neurology, vol. 43, no. 2, pp. 345–348, 1993. View at Google Scholar · View at Scopus
  92. R. C. Griggs, R. Tawil, M. McDermott, J. Forrester, D. Figlewicz, and B. Weiffenbach, “Monozygotic twins with facioscapulohumeral dystrophy (FSHD): implications for genotype/phenotype correlation,” Muscle and Nerve, vol. 18, no. 2, pp. S50–S55, 1995. View at Google Scholar · View at Scopus
  93. J. C. T. Van Deutekom, C. Wijmenga, E. A. E. Van Tienhoven et al., “FSHD associated DNA rearrangements are due to deletions of integral copies of a 3.2 kb tandemly repeated unit,” Human Molecular Genetics, vol. 2, no. 12, pp. 2037–2042, 1993. View at Google Scholar · View at Scopus
  94. J. C. T. van Deutekom, E. Bakker, R. J. L. F. Lemmers et al., “Evidence for subtelomeric exchange of 3.3 kb tandemly repeated units between chromosomes 4q35 and 10q26: implications for genetic counselling and etiology of FSHD1,” Human Molecular Genetics, vol. 5, no. 12, pp. 1997–2003, 1996. View at Google Scholar · View at Scopus
  95. P. W. Lunt, P. E. Jardine, M. C. Koch et al., “Correlation between fragment size at D4F104S1 and age at onset or at wheelchair use, with a possible generational effect, accounts for much phenotypic variation in 4q35-facioscapulohumeral muscular dystrophy (FSHD),” Human Molecular Genetics, vol. 4, no. 5, pp. 951–958, 1995. View at Google Scholar · View at Scopus
  96. E. Ricci, G. Galluzzi, G. Deidda, S. Cacurri, and L. Colantoni, “Progress in the molecular diagnosis of facioscapulohumeral muscular dystrophy and correlation between the number of KpnI repeats at the 4q35 locus and clinical phenotype,” Annals of Neurology, vol. 45, pp. 751–757, 1999. View at Google Scholar
  97. R. Tawil, J. Forrester, R. C. Griggs et al., “Evidence for anticipation and association of deletion size with severity in facioscapulohumeral muscular systrophy,” Annals of Neurology, vol. 39, no. 6, pp. 744–748, 1996. View at Google Scholar · View at Scopus
  98. R. Tupler, A. Berardinelli, L. Barbierato et al., “Monosomy of distal 4q does not cause facioscapulohumeral muscular dystrophy,” Journal of Medical Genetics, vol. 33, no. 5, pp. 366–370, 1996. View at Google Scholar · View at Scopus
  99. R. J. L. F. Lemmers, P. De Kievit, L. Sandkuijl et al., “Facioscapulohumeral muscular dystrophy is uniquely associated with one of the two variants of the 4q subtelomere,” Nature Genetics, vol. 32, no. 2, pp. 235–236, 2002. View at Publisher · View at Google Scholar · View at Scopus
  100. R. J. L. F. Lemmers, P. J. Van Der Vliet, R. Klooster et al., “A unifying genetic model for facioscapulohumeral muscular dystrophy,” Science, vol. 329, no. 5999, pp. 1650–1653, 2010. View at Publisher · View at Google Scholar · View at Scopus
  101. R. J. F. L. Lemmers, M. Wohlgemuth, R. R. Frants, G. W. Padberg, E. Morava, and S. M. Van Der Maarel, “Contractions of D4Z4 on 4qB subtelomeres do not cause facioscapulohumeral muscular dystrophy,” American Journal of Human Genetics, vol. 75, no. 6, pp. 1124–1130, 2004. View at Publisher · View at Google Scholar · View at Scopus
  102. N. S. T. Thomas, K. Wiseman, G. Spurlock, M. MacDonald, D. Üstek, and M. Upadhyaya, “A large patient study confirming that facioscapulohumeral muscular dystrophy (FSHD) disease expression is almost exclusively associated with an FSHD locus located on a 4qA-defined 4qter subtelomere,” Journal of Medical Genetics, vol. 44, no. 3, pp. 215–218, 2007. View at Publisher · View at Google Scholar · View at Scopus
  103. R. Lyle, T. J. Wright, L. N. Clark, and J. E. Hewitt, “The FSHD-associated repeat, D4Z4, is a member of a dispersed family of homeobox-containing repeats, subsets of which are clustered on the short arms of the acrocentric chromosomes,” Genomics, vol. 28, no. 3, pp. 389–397, 1995. View at Publisher · View at Google Scholar · View at Scopus
  104. E. Bakker, C. Wijmenga, R. H. A. M. Vossen et al., “The FSHD-linked locus D4F104S1 (p13E-11) on 4q35 has a homologue on 10qter,” Muscle and Nerve, vol. 18, no. 2, pp. S39–S44, 1995. View at Google Scholar · View at Scopus
  105. G. Deidda, S. Cacurri, P. Grisanti, E. Vigneti, N. Piazzo, and L. Felicetti, “Physical mapping evidence for a duplicated region on chromosome 10qter showing high homology with the facioscapulohumeral muscular dystrophy locus on chromosome 4qter,” European Journal of Human Genetics, vol. 3, no. 3, pp. 155–167, 1995. View at Google Scholar · View at Scopus
  106. R. J. L. F. Lemmers, P. de Kievit, M. van Geel et al., “Complete allele information in the diagnosis of facioscapulohumeral muscular dystrophy by triple DNA analysis,” Annals of Neurology, vol. 50, no. 6, pp. 816–819, 2001. View at Publisher · View at Google Scholar · View at Scopus
  107. D. Gabellini, M. R. Green, and R. Tupler, “Inappropriate gene activation in FSHD: a repressor complex binds a chromosomal repeat deleted in dystrophic muscle,” Cell, vol. 110, no. 3, pp. 339–348, 2002. View at Publisher · View at Google Scholar · View at Scopus
  108. B. Bodega, G. D. Ramirez, F. Grasser et al., “Remodeling of the chromatin structure of the facioscapulohumeral muscular dystrophy (FSHD) locus and upregulation of FSHD-related gene 1 (FRG1) expression during human myogenic differentiation,” BMC Biology, vol. 7, article 41, 2009. View at Publisher · View at Google Scholar · View at Scopus
  109. D. Gabellini, G. D'Antona, M. Moggio et al., “Facioscapulohumeral muscular dystrophy in mice overexpressing FRG1,” Nature, vol. 439, no. 7079, pp. 973–977, 2006. View at Publisher · View at Google Scholar · View at Scopus
  110. G. Jiang, F. Yang, P. G. M. van Overveld, V. Vedanarayanan, S. van der Maarel, and M. Ehrlich, “Testing the position-effect variegation hypothesis for facioscapulohumeral muscular dystrophy by analysis of histone modification and gene expression in subtelomeric 4q,” Human Molecular Genetics, vol. 12, no. 22, pp. 2909–2921, 2003. View at Publisher · View at Google Scholar · View at Scopus
  111. R. J. Osborne, S. Welle, S. L. Venance, C. A. Thornton, and R. Tawil, “Expression profile of FSHD supports a link between retinal vasculopathy and muscular dystrophy,” Neurology, vol. 68, no. 8, pp. 569–577, 2007. View at Publisher · View at Google Scholar · View at Scopus
  112. S. van Koningsbruggen, R. W. Dirks, A. M. Mommaas et al., “FRG1P is localised in the nucleolus, Cajal bodies, and speckles,” Journal of Medical Genetics, vol. 41, no. 4, article e46, 2004. View at Google Scholar · View at Scopus
  113. S. van Koningsbruggen, K. R. Straasheijm, E. Sterrenburg et al., “FRG1P-mediated aggregation of proteins involved in pre-mRNA processing,” Chromosoma, vol. 116, no. 1, pp. 53–64, 2007. View at Publisher · View at Google Scholar · View at Scopus
  114. L. Snider, L. N. Geng, R. J. Lemmers et al., “Facioscapulohumeral dystrophy: incomplete suppression of a retrotransposed gene,” PLoS Genetics, vol. 6, no. 10, article e1001181, 2010. View at Google Scholar · View at Scopus
  115. M. Dixit, E. Ansseau, A. Tassin et al., “DUX4, a candidate gene of facioscapulohumeral muscular dystrophy, encodes a transcriptional activator of PITX1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 46, pp. 18157–18162, 2007. View at Publisher · View at Google Scholar · View at Scopus
  116. L. Snider, A. Asawachaicharn, A. E. Tyler et al., “RNA transcripts, miRNA-sized fragments and proteins produced from D4Z4 units: new candidates for the pathophysiology of facioscapulohumeral dystrophy,” Human Molecular Genetics, vol. 18, no. 13, pp. 2414–2430, 2009. View at Publisher · View at Google Scholar · View at Scopus
  117. V. Kowaljow, A. Marcowycz, E. Ansseau et al., “The DUX4 gene at the FSHD1A locus encodes a pro-apoptotic protein,” Neuromuscular Disorders, vol. 17, no. 8, pp. 611–623, 2007. View at Publisher · View at Google Scholar · View at Scopus
  118. D. Bosnakovski, S. Lamb, T. Simsek et al., “DUX4c, an FSHD candidate gene, interferes with myogenic regulators and abolishes myoblast differentiation,” Experimental Neurology, vol. 214, no. 1, pp. 87–96, 2008. View at Publisher · View at Google Scholar · View at Scopus
  119. L. N. Geng, Z. Yao, L. Snider, A. P. Fong, and J. N. Cech, “DUX4 activates germline genes, retroelements, and immune mediators: implications for facioscapulohumeral dystrophy,” Developmental Cell, vol. 22, pp. 38–51, 2012. View at Google Scholar
  120. D. S. Cabianca and D. Gabellini, “FSHD: copy number variations on the theme of muscular dystrophy,” Journal of Cell Biology, vol. 191, no. 6, pp. 1049–1060, 2010. View at Publisher · View at Google Scholar · View at Scopus
  121. S. M. Van der Maarel, R. Tawil, and S. J. Tapscott, “Facioscapulohumeral muscular dystrophy and DUX4: breaking the silence,” Trends in Molecular Medicine, vol. 17, no. 5, pp. 252–258, 2011. View at Publisher · View at Google Scholar · View at Scopus
  122. J. E. Hewitt, R. Lyle, L. N. Clark et al., “Analysis of the tandem repeat locus D4Z4 associated with facioscapulohumeral muscular dystrophy,” Human Molecular Genetics, vol. 3, no. 8, pp. 1287–1295, 1994. View at Google Scholar · View at Scopus
  123. J. C. de Greef, R. J. Lemmers, B. G. van Engelen et al., “Common epigenetic changes of D4Z4 in contraction-dependent and contraction-independent FSHD,” Human Mutation, vol. 30, no. 10, pp. 1449–1459, 2009. View at Google Scholar · View at Scopus
  124. P. G. M. Van Overveld, R. J. F. L. Lemmers, G. Deidda et al., “Interchromosomal repeat array interactions between chromosomes 4 and 10: a model for subtelomeric plasticity,” Human Molecular Genetics, vol. 9, no. 19, pp. 2879–2884, 2000. View at Google Scholar · View at Scopus
  125. W. Zeng, J. C. De Greef, Y. Y. Chen et al., “Specific loss of histone H3 lysine 9 trimethylation and HP1γ/cohesin binding at D4Z4 repeats is associated with facioscapulohumeral dystrophy (FSHD),” PLoS Genetics, vol. 5, no. 7, article e1000559, 2009. View at Publisher · View at Google Scholar · View at Scopus
  126. J. Dekker, K. Rippe, M. Dekker, and N. Kleckner, “Capturing chromosome conformation,” Science, vol. 295, no. 5558, pp. 1306–1311, 2002. View at Publisher · View at Google Scholar · View at Scopus
  127. P. S. Masny, U. Bengtsson, S. A. Chung et al., “Localization of 4q35.2 to the nuclear periphery: is FSHD a nuclear envelope disease?” Human Molecular Genetics, vol. 13, no. 17, pp. 1857–1871, 2004. View at Publisher · View at Google Scholar · View at Scopus
  128. R. Tam, K. P. Smith, and J. B. Lawrence, “The 4q subtelomere harboring the FSHD locus is specifically anchored with peripheral heterochromatin unlike most human telomeres,” Journal of Cell Biology, vol. 167, no. 2, pp. 269–279, 2004. View at Publisher · View at Google Scholar · View at Scopus
  129. B. Bodega, M. F. Cardone, S. Müller et al., “Evolutionary genomic remodelling of the human 4q subtelomere (4q35.2),” BMC Evolutionary Biology, vol. 7, article 39, 2007. View at Publisher · View at Google Scholar · View at Scopus
  130. A. Ottaviani, C. Schluth-Bolard, S. Rival-Gervier et al., “Identification of a perinuclear positioning element in human subtelomeres that requires A-type lamins and CTCF,” EMBO Journal, vol. 28, no. 16, pp. 2428–2436, 2009. View at Publisher · View at Google Scholar · View at Scopus
  131. I. Scionti, G. Fabbri, C. Fiorillo, G. Ricci, and F. Greco, “Facioscapulohumeral muscular dystrophy: new insights from compound heterozygotes and implication for prenatal genetic counselling,” Journal of Medical Genetics, vol. 49, pp. 171–178, 2012. View at Google Scholar
  132. G. Patrizi and M. Poger, “The ultrastructure of the nuclear periphery. The Zonula Nucleum Limitans,” Journal of Ultrasructure Research, vol. 17, no. 1-2, pp. 127–136, 1967. View at Google Scholar · View at Scopus
  133. F. Lin and H. J. Worman, “Structural organization of the human gene encoding nuclear lamin A and nuclear lamin C,” The Journal of Biological Chemistry, vol. 268, no. 22, pp. 16321–16326, 1993. View at Google Scholar · View at Scopus
  134. A. E. Rusiñol and M. S. Sinensky, “Farnesylated lamins, progeroid syndromes and farnesyl transferase inhibitors,” Journal of Cell Science, vol. 119, no. 16, pp. 3265–3272, 2006. View at Publisher · View at Google Scholar · View at Scopus
  135. G. Krohne, I. Waizenegger, and T. H. Hoger, “The conserved carboxy-terminal cysteine of nuclear lamins is essential for lamin association with the nuclear envelope,” Journal of Cell Biology, vol. 109, no. 5, pp. 2003–2011, 1989. View at Google Scholar · View at Scopus
  136. S. G. Young, L. G. Fong, and S. Michaelis, “Prelamin A, Zmpste24, misshapen cell nuclei, and progeria—new evidence suggesting that protein farnesylation could be important for disease pathogenesis,” Journal of Lipid Research, vol. 46, no. 12, pp. 2531–2558, 2005. View at Publisher · View at Google Scholar · View at Scopus
  137. J. L. V. Broers, B. M. Machiels, H. J. H. Kuijpers et al., “A- and B-type lamins are differentially expressed in normal human tissues,” Histochemistry and Cell Biology, vol. 107, no. 6, pp. 505–517, 1997. View at Publisher · View at Google Scholar · View at Scopus
  138. L. Guelen, L. Pagie, E. Brasset et al., “Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions,” Nature, vol. 453, no. 7197, pp. 948–951, 2008. View at Publisher · View at Google Scholar · View at Scopus
  139. H. Pickersgill, B. Kalverda, E. De Wit, W. Talhout, M. Fornerod, and B. Van Steensel, “Characterization of the Drosophila melanogaster genome at the nuclear lamina,” Nature Genetics, vol. 38, no. 9, pp. 1005–1014, 2006. View at Publisher · View at Google Scholar · View at Scopus
  140. J. L. V. Broers, F. C. S. Ramaekers, G. Bonne, R. Ben Yaou, and C. J. Hutchison, “Nuclear lamins: laminopathies and their role in premature ageing,” Physiological Reviews, vol. 86, no. 3, pp. 967–1008, 2006. View at Publisher · View at Google Scholar · View at Scopus
  141. B. R. Johnson, R. T. Nitta, R. L. Frock et al., “A-type lamins regulate retinoblastoma protein function by promoting subnuclear localization and preventing proteasomal degradation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 26, pp. 9677–9682, 2004. View at Publisher · View at Google Scholar · View at Scopus
  142. V. L. R. M. Verstraeten, J. L. V. Broers, F. C. S. Ramaekers, and M. A. M. van Steensel, “The nuclear envelope, a key structure in cellular integrity and gene expression,” Current Medicinal Chemistry, vol. 14, no. 11, pp. 1231–1248, 2007. View at Publisher · View at Google Scholar · View at Scopus
  143. N. D. Willis, T. R. Cox, S. F. Rahman-Casañs et al., “Lamin A/C is a risk biomarker in colorectal cancer,” PLoS ONE, vol. 3, no. 8, article e2988, 2008. View at Publisher · View at Google Scholar · View at Scopus
  144. P. Hozak, A. M. J. Sasseville, Y. Raymond, and P. R. Cook, “Lamin proteins form an internal nucleoskeleton as well as a peripheral lamina in human cells,” Journal of Cell Science, vol. 108, no. 2, pp. 635–644, 1995. View at Google Scholar · View at Scopus
  145. L. Vergnes, M. Péterfy, M. O. Bergo, S. G. Young, and K. Reue, “Lamin B1 is required for mouse development and nuclear integrity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 28, pp. 10428–10433, 2004. View at Publisher · View at Google Scholar · View at Scopus
  146. T. Sullivan, D. Escalante-Alcalde, H. Bhatt et al., “Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy,” Journal of Cell Biology, vol. 147, no. 5, pp. 913–919, 1999. View at Publisher · View at Google Scholar · View at Scopus
  147. B. C. Capell and F. S. Collins, “Human laminopathies: nuclei gone genetically awry,” Nature Reviews Genetics, vol. 7, no. 12, pp. 940–952, 2006. View at Publisher · View at Google Scholar · View at Scopus
  148. I. Landires, J. M. Pascale, and J. Motta, “The position of the mutation within the LMNA gene determines the type and extent of tissue involvement in laminopathies [1],” Clinical Genetics, vol. 71, no. 6, pp. 592–596, 2007. View at Publisher · View at Google Scholar · View at Scopus
  149. J. Scharner, V. F. Gnocchi, J. A. Ellis, and P. S. Zammit, “Genotype-phenotype correlations in laminopathies: how does fate translate?” Biochemical Society Transactions, vol. 38, no. 1, pp. 257–262, 2010. View at Publisher · View at Google Scholar · View at Scopus
  150. D. K. Shumaker, T. Dechat, A. Kohlmaier et al., “Mutant nuclear lamin A leads to progressive alterations of epigenetic control in premature aging,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 23, pp. 8703–8708, 2006. View at Publisher · View at Google Scholar · View at Scopus
  151. Y. Wang, A. J. Herron, and H. J. Worman, “Pathology and nuclear abnormalities in hearts of transgenic mice expressing M371K lamin A encoded by an LMNA mutation causing Emery-Dreifuss muscular dystrophy,” Human Molecular Genetics, vol. 15, no. 16, pp. 2479–2489, 2006. View at Publisher · View at Google Scholar · View at Scopus
  152. V. Andrés and J. M. González, “Role of A-type lamins in signaling, transcription, and chromatin organization,” Journal of Cell Biology, vol. 187, no. 7, pp. 945–957, 2009. View at Publisher · View at Google Scholar · View at Scopus
  153. S. Marmiroli, J. Bertacchini, F. Beretti et al., “A-type lamins and signaling: the PI 3-kinase/Akt pathway moves forward,” Journal of Cellular Physiology, vol. 220, no. 3, pp. 553–564, 2009. View at Publisher · View at Google Scholar · View at Scopus
  154. P. L. Puri, S. Iezzi, P. Stiegler et al., “Class I histone deacetylases sequentially interact with MyoD and pRb during skeletal myogenesis,” Molecular Cell, vol. 8, no. 4, pp. 885–897, 2001. View at Publisher · View at Google Scholar · View at Scopus
  155. J. H. Van Berlo, J. W. Voncken, N. Kubben et al., “A-type lamins are essential for TGF-β1 induced PP2A to dephosphorylate transcription factors,” Human Molecular Genetics, vol. 14, no. 19, pp. 2839–2849, 2005. View at Publisher · View at Google Scholar · View at Scopus
  156. R. L. Frock, B. A. Kudlow, A. M. Evans, S. A. Jameson, S. D. Hauschka, and B. K. Kennedy, “Lamin A/C and emerin are critical for skeletal muscle satellite cell differentiation,” Genes and Development, vol. 20, no. 4, pp. 486–500, 2006. View at Publisher · View at Google Scholar · View at Scopus
  157. Y. E. Park, Y. K. Hayashi, K. Goto et al., “Nuclear changes in skeletal muscle extend to satellite cells in autosomal dominant Emery-Dreifuss muscular dystrophy/limb-girdle muscular dystrophy 1B,” Neuromuscular Disorders, vol. 19, no. 1, pp. 29–36, 2009. View at Publisher · View at Google Scholar · View at Scopus
  158. J. Wang, R. M. Kumar, V. J. Biggs, H. Lee, Y. Chen et al., “The Msx1 homeoprotein recruits polycomb to the nuclear periphery during development,” Developmental Cell, vol. 21, pp. 575–588, 2011. View at Google Scholar
  159. A. Mattout, B. L. Pike, B. D. Towbin, E. M. Bank, and A. Gonzalez-Sandoval, “An EDMD mutation in C. elegans lamin blocks muscle-specific gene relocation and compromises muscle integrity,” Current Biology, vol. 21, no. 19, pp. 1603–1614, 2011. View at Google Scholar
  160. L. Giacinti, P. Vici, and M. Lopez, “Epigenome: a new target in cancer therapy,” Clinica Terapeutica, vol. 159, no. 5, pp. 347–360, 2008. View at Google Scholar · View at Scopus
  161. C. Ptak and A. Petronis, “Epigenetics and complex disease: from etiology to new therapeutics,” Annual Review of Pharmacology and Toxicology, vol. 48, pp. 257–276, 2008. View at Publisher · View at Google Scholar · View at Scopus
  162. S. Pepke, B. Wold, and A. Mortazavi, “Computation for ChIP-seq and RNA-seq studies,” Nature methods, vol. 6, no. 11, pp. S22–S32, 2009. View at Google Scholar · View at Scopus
  163. J. Peedicayil, “Pharmacoepigenetics and pharmacoepigenomics,” Pharmacogenomics, vol. 9, no. 12, pp. 1785–1786, 2008. View at Publisher · View at Google Scholar · View at Scopus
  164. B. Claes, I. Buysschaert, and D. Lambrechts, “Pharmaco-epigenomics: discovering therapeutic approaches and biomarkers for cancer therapy,” Heredity, vol. 105, no. 1, pp. 152–160, 2010. View at Publisher · View at Google Scholar · View at Scopus