Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015, Article ID 347571, 17 pages
http://dx.doi.org/10.1155/2015/347571
Review Article

The Roles of SNF2/SWI2 Nucleosome Remodeling Enzymes in Blood Cell Differentiation and Leukemia

Department of Biosciences and Nutrition, Karolinska Institute, 141 57 Huddinge, Sweden

Received 23 November 2014; Accepted 27 January 2015

Academic Editor: Andre Van Wijnen

Copyright © 2015 Punit Prasad et al. 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. L. Neigeborn and M. Carlson, “Genes affecting the regulation of SUC2 gene expression by glucose repression in Saccharomyces cerevisiae,” Genetics, vol. 108, no. 4, pp. 845–858, 1984. View at Google Scholar · View at Scopus
  2. M. Stern, R. Jensen, and I. Herskowitz, “Five SWI genes are required for expression of the HO gene in yeast,” Journal of Molecular Biology, vol. 178, no. 4, pp. 853–868, 1984. View at Publisher · View at Google Scholar · View at Scopus
  3. J. N. Hirschhorn, S. A. Brown, C. D. Clark, and F. Winston, “Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure,” Genes and Development, vol. 6, no. 12, pp. 2288–2298, 1992. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Côté, J. Quinn, J. L. Workman, and C. L. Peterson, “Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex,” Science, vol. 265, no. 5168, pp. 53–60, 1994. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Flaus, D. M. A. Martin, G. J. Barton, and T. Owen-Hughes, “Identification of multiple distinct Snf2 subfamilies with conserved structural motifs,” Nucleic Acids Research, vol. 34, no. 10, pp. 2887–2905, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. P. B. Becker and J. L. Workman, “Nucleosome remodeling and epigenetics,” Cold Spring Harbor Perspectives in Biology, vol. 5, no. 9, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. C. R. Clapier and B. R. Cairns, “The biology of chromatin remodeling complexes,” Annual Review of Biochemistry, vol. 78, pp. 273–304, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. S. H. Orkin and L. I. Zon, “Hematopoiesis: an evolving paradigm for stem cell biology,” Cell, vol. 132, no. 4, pp. 631–644, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. J. I. Sive and B. Göttgens, “Transcriptional network control of normal and leukaemic haematopoiesis,” Experimental Cell Research, vol. 329, no. 2, pp. 255–264, 2014. View at Publisher · View at Google Scholar
  10. D. Lara-Astiaso, A. Weiner, E. Lorenzo-Vivas et al., “Immunogenetics. Chromatin state dynamics during blood formation,” Science, vol. 345, no. 6199, pp. 943–949, 2014. View at Google Scholar
  11. A. Valouev, S. M. Johnson, S. D. Boyd, C. L. Smith, A. Z. Fire, and A. Sidow, “Determinants of nucleosome organization in primary human cells,” Nature, vol. 474, no. 7352, pp. 516–520, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Luyten, C. Zang, X. S. Liu, and R. A. Shivdasani, “Active enhancers are delineated de novo during hematopoiesis, with limited lineage fidelity among specified primary blood cells,” Genes & Development, vol. 28, no. 16, pp. 1827–1839, 2014. View at Publisher · View at Google Scholar
  13. H. T. Huang, K. L. Kathrein, A. Barton et al., “A network of epigenetic regulators guides developmental haematopoiesis in vivo,” Nature Cell Biology, vol. 15, no. 12, pp. 1516–1525, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. J. A. Martens and F. Winston, “Recent advances in understanding chromatin remodeling by Swi/Snf complexes,” Current Opinion in Genetics and Development, vol. 13, no. 2, pp. 136–142, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. W. Wang, J. Côté, Y. Xue et al., “Purification and biochemical heterogeneity of the mammalian SWI-SNF complex,” The EMBO Journal, vol. 15, no. 19, pp. 5370–5382, 1996. View at Google Scholar · View at Scopus
  16. Y. Xue, J. C. Canman, C. S. Lee et al., “The human SWI/SNF-B chromatin-remodeling complex is related to yeast Rsc and localizes at kinetochores of mitotic chromosomes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 24, pp. 13015–13020, 2000. View at Publisher · View at Google Scholar · View at Scopus
  17. J. C. Reyes, J. Barra, C. Muchardt, A. Camus, C. Babinet, and M. Yaniv, “Altered control of cellular proliferation in the absence of mammalian brahma (SNF2alpha),” The EMBO Journal, vol. 17, no. 23, pp. 6979–6991, 1998. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Ho and G. R. Crabtree, “Chromatin remodelling during development,” Nature, vol. 463, no. 7280, pp. 474–484, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Ko, D. H. Sohn, H. Chung, and R. H. Seong, “Chromatin remodeling, development and disease,” Mutation Research, vol. 647, no. 1-2, pp. 59–67, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. V. Krasteva, M. Buscarlet, A. Diaz-Tellez, M.-A. Bernard, G. R. Crabtree, and J. A. Lessard, “The BAF53a subunit of SWI/SNF-like BAF complexes is essential for hemopoietic stem cell function,” Blood, vol. 120, no. 24, pp. 4720–4732, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. J. A. Armstrong, J. J. Bieker, and B. M. Emerson, “A SWI/SNF-related chromatin remodeling complex, E-RC1, is required for tissue-specific transcriptional regulation by EKLF in vitro,” Cell, vol. 95, no. 1, pp. 93–104, 1998. View at Publisher · View at Google Scholar · View at Scopus
  22. T. C. Gebuhr, G. I. Kovalev, S. Bultman, V. Godfrey, L. Su, and T. Magnuson, “The role of Brg1, a catalytic subunit of mammalian chromatin-remodeling complexes, in T cell development,” Journal of Experimental Medicine, vol. 198, no. 12, pp. 1937–1949, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. D. Vradii, S. Wagner, D. N. Doan et al., “Brg1, the ATPase subunit of the SWI/SNF chromatin remodeling complex, is required for myeloid differentiation to granulocytes,” Journal of Cellular Physiology, vol. 206, no. 1, pp. 112–118, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. D. H. Sohn, K. Y. Lee, C. Lee et al., “SRG3 interacts directly with the major components of the SWI/SNF chromatin remodeling complex and protects them from proteasomal degradation,” Journal of Biological Chemistry, vol. 282, no. 14, pp. 10614–10624, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. J. K. Kim, S.-O. Huh, H. Choi et al., “Srg3, a mouse homolog of yeast SWI3, is essential for early embryogenesis and involved in brain development,” Molecular and Cellular Biology, vol. 21, no. 22, pp. 7787–7795, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. D. Han, S. Jeon, D. H. Sohn et al., “SRG3, a core component of mouse SWI/SNF complex, is essential for extra-embryonic vascular development,” Developmental Biology, vol. 315, no. 1, pp. 136–146, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. C. W. M. Roberts, M. M. Leroux, M. D. Fleming, and S. H. Orkin, “Highly penetrant, rapid tumorigenesis through conditional inversion of the tumor suppressor gene Snf5,” Cancer Cell, vol. 2, no. 5, pp. 415–425, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. P. Prasad, M. Ronnerblad, E. Arner et al., “High-throughput transcription profiling identifies putative epigenetic regulators of hematopoiesis,” Blood, vol. 123, no. 17, pp. e46–e57, 2014. View at Publisher · View at Google Scholar
  29. S. J. Bultman, T. C. Gebuhr, and T. Magnuson, “A Brg1 mutation that uncouples ATPase activity from chromatin remodeling reveals an essential role for SWI/SNF-related complexes in β-globin expression and erythroid development,” Genes & Development, vol. 19, no. 23, pp. 2849–2861, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. C. T. Griffin, J. Brennan, and T. Magnuson, “The chromatin-remodeling enzyme BRG1 plays an essential role in primitive erythropoiesis and vascular development,” Development, vol. 135, no. 3, pp. 493–500, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. T. H. Chi, M. Wan, P. P. Lee et al., “Sequential roles of Brg, the ATPase subunit of BAF chromatin remodeling complexes, in thymocyte development,” Immunity, vol. 19, no. 2, pp. 169–182, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. T. Chi, “A BAF-centred view of the immune system,” Nature Reviews Immunology, vol. 4, no. 12, pp. 965–977, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. K. Zhao, W. Wang, O. J. Rando et al., “Rapid and phosphoinositol-dependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling,” Cell, vol. 95, no. 5, pp. 625–636, 1998. View at Publisher · View at Google Scholar · View at Scopus
  34. I. Taniuchi, W. Ellmeier, and D. R. Littman, “The CD4/CD8 lineage choice: new insights into epigenetic regulation during T cell development,” Advances in Immunology, vol. 83, pp. 55–89, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. T. H. Chi, M. Wan, K. Zhao et al., “Reciprocal regulation of CD4/CD8 expression by SWI/SNF-like BAF complexes,” Nature, vol. 418, no. 6894, pp. 195–199, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Wan, J. Zhang, D. Lai et al., “Molecular basis of CD4 repression by the Swi/Snf-like BAF chromatin remodeling complex,” European Journal of Immunology, vol. 39, no. 2, pp. 580–588, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. A. F. Holloway, S. Rao, X. Chen, and M. F. Shannon, “Changes in chromatin accessibility across the GM-CSF promoter upon T cell activation are dependent on nuclear factor κB proteins,” Journal of Experimental Medicine, vol. 197, no. 4, pp. 413–423, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. J. Choi, M. Ko, S. Jeon et al., “The SWI/SNF-like BAF complex is essential for early B cell development,” Journal of Immunology, vol. 188, no. 8, pp. 3791–3803, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Tsukada, Y. Yoshida, Y. Kominato, and P. E. Auron, “The CCAAT/enhancer (C/EBP) family of basic-leucine zipper (bZIP) transcription factors is a multifaceted highly-regulated system for gene regulation,” Cytokine, vol. 54, no. 1, pp. 6–19, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. L. M. Scott, C. I. Civin, P. Rorth, and A. D. Friedman, “A novel temporal expression pattern of three C/EBP family members in differentiating myelomonocytic cells,” Blood, vol. 80, no. 7, pp. 1725–1735, 1992. View at Google Scholar · View at Scopus
  41. E. Kowenz-Leutz and A. Leutz, “A C/EBPβ isoform recruits the SWI/SNF complex to activate myeloid genes,” Molecular Cell, vol. 4, no. 5, pp. 735–743, 1999. View at Publisher · View at Google Scholar · View at Scopus
  42. F. Erdel and K. Rippe, “Chromatin remodelling in mammalian cells by ISWI-type complexes—where, when and why?” The FEBS Journal, vol. 278, no. 19, pp. 3608–3618, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. B. Bartholomew, “ISWI chromatin remodeling: one primary actor or a coordinated effort?” Current Opinion in Structural Biology, vol. 24, no. 1, pp. 150–155, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. B. Bartholomew, “Regulating the chromatin landscape: structural and mechanistic perspectives,” Annual Review of Biochemistry, vol. 83, no. 1, pp. 671–696, 2014. View at Publisher · View at Google Scholar
  45. T. Stopka and A. I. Skoultchi, “The ISWI ATPase Snf2h is required for early mouse development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 2, pp. 14097–14102, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. J. W. Landry, S. Banerjee, B. Taylor, P. D. Aplan, A. Singer, and C. Wu, “Chromatin remodeling complex NURF regulates thymocyte maturation,” Genes & Development, vol. 25, no. 3, pp. 275–286, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. J. K. Sims and P. A. Wade, “SnapShot: chromatin remodeling: CHD,” Cell, vol. 144, no. 4, p. 626, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Qin, Y. Liu, W. Tempel et al., “Structural basis for histone mimicry and hijacking of host proteins by influenza virus protein NS1,” Nature Communications, vol. 5, article 3952, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. J. C. Eissenberg, “Structural biology of the chromodomain: form and function,” Gene, vol. 496, no. 2, pp. 69–78, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Ramírez and J. Hagman, “The Mi-2/NuRD complex: a critical epigenetic regulator of hematopoietic development, differentiation and cancer,” Epigenetics, vol. 4, no. 8, pp. 532–536, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. R. Bajpai, D. A. Chen, A. Rada-Iglesias et al., “CHD7 cooperates with PBAF to control multipotent neural crest formation,” Nature, vol. 463, no. 7283, pp. 958–962, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Radman-Livaja, T. K. Quan, L. Valenzuela et al., “A key role for Chd1 in histone H3 dynamics at the 3′ ends of long genes in yeast,” PLoS Genetics, vol. 8, no. 7, Article ID e1002811, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Lange, S. Demajo, P. Jain, and L. di Croce, “Combinatorial assembly and function of chromatin regulatory complexes,” Epigenomics, vol. 3, no. 5, pp. 567–580, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Gaspar-Maia, A. Alajem, F. Polesso et al., “Chd1 regulates open chromatin and pluripotency of embryonic stem cells,” Nature, vol. 460, no. 7257, pp. 863–868, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. J. Pointner, J. Persson, P. Prasad et al., “CHD1 remodelers regulate nucleosome spacing in vitro and align nucleosomal arrays over gene coding regions in S. pombe,” The EMBO Journal, vol. 31, no. 23, pp. 4388–4403, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. T. Gkikopoulos, P. Schofield, V. Singh et al., “A role for Snf2-related nucleosome-spacing enzymes in genome-wide nucleosome organization,” Science, vol. 333, no. 6050, pp. 1758–1760, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. Y.-X. Chen, J. Yan, K. Keeshan et al., “The tumor suppressor menin regulates hematopoiesis and myeloid transformation by influencing Hox gene expression,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 4, pp. 1018–1023, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. P. Nagarajan, T. M. Onami, S. Rajagopalan, S. Kania, R. Donnell, and S. Venkatachalam, “Role of chromodomain helicase DNA-binding protein 2 in DNA damage response signaling and tumorigenesis,” Oncogene, vol. 28, no. 8, pp. 1053–1062, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. N. J. Bowen, N. Fujita, M. Kajita, and P. A. Wade, “Mi-2/NuRD: multiple complexes for many purposes,” Biochimica et Biophysica Acta—Gene Structure and Expression, vol. 1677, no. 1–3, pp. 52–57, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. C. Dege and J. Hagman, “Mi-2/NuRD chromatin remodeling complexes regulate B and T-lymphocyte development and function,” Immunological Reviews, vol. 261, no. 1, pp. 126–140, 2014. View at Publisher · View at Google Scholar
  61. T. Yoshida, I. Hazan, J. Zhang et al., “The role of the chromatin remodeler Mi-2β in hematopoietic stem cell self-renewal and multilineage differentiation,” Genes & Development, vol. 22, no. 9, pp. 1174–1189, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. R. Sridharan and S. T. Smale, “Predominant interaction of both Ikaros and Helios with the NuRD complex in immature thymocytes,” The Journal of Biological Chemistry, vol. 282, no. 41, pp. 30227–30238, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. J. Zhang, A. F. Jackson, T. Naito et al., “Harnessing of the nucleosome-remodeling-deacetylase complex controls lymphocyte development and prevents leukemogenesis,” Nature Immunology, vol. 13, no. 1, pp. 86–94, 2012. View at Publisher · View at Google Scholar · View at Scopus
  64. H. Maier, R. Ostraat, H. Gao et al., “Early B cell factor cooperates with Runx1 and mediates epigenetic changes associated with mb-1 transcription,” Nature Immunology, vol. 5, no. 10, pp. 1069–1077, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. H. Gao, K. Lukin, J. Ramírez, S. Fields, D. Lopez, and J. Hagman, “Opposing effects of SWI/SNF and Mi-2/NuRD chromatin remodeling complexes on epigenetic reprogramming by EBF and Pax5,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 27, pp. 11258–11263, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. V. R. Ramirez-Carrozzi, A. A. Nazarian, C. C. Li et al., “Selective and antagonistic functions of SWI/SNF and Mi-2beta nucleosome remodeling complexes during an inflammatory response,” Genes & Development, vol. 20, no. 3, pp. 282–296, 2006. View at Publisher · View at Google Scholar · View at Scopus
  67. C. J. Williams, T. Naito, P. Gómez-Del Arco et al., “The chromatin remodeler Mi-2β is required for CD4 expression and T cell development,” Immunity, vol. 20, no. 6, pp. 719–733, 2004. View at Publisher · View at Google Scholar · View at Scopus
  68. V. B. Cismasiu, K. Adamo, J. Gecewicz, J. Duque, Q. Lin, and D. Avram, “BCL11B functionally associates with the NuRD complex in T lymphocytes to repress targeted promoter,” Oncogene, vol. 24, no. 45, pp. 6753–6764, 2005. View at Publisher · View at Google Scholar · View at Scopus
  69. T. M. Geiman and K. Muegge, “Lsh, an SNF2/helicase family member, is required for proliferation of mature T lymphocytes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 9, pp. 4772–4777, 2000. View at Publisher · View at Google Scholar · View at Scopus
  70. T. Ueda, R. Watanabe-fukunaga, H. Ogawa et al., “Critical role of the p400/mDomino chromatin-remodeling ATPase in embryonic hematopoiesis,” Genes to Cells, vol. 12, no. 5, pp. 581–592, 2007. View at Publisher · View at Google Scholar · View at Scopus
  71. T. Fujii, T. Ueda, S. Nagata, and R. Fukunaga, “Essential role of p400/mDomino chromatin-remodeling ATPase in bone marrow hematopoiesis and cell-cycle progression,” Journal of Biological Chemistry, vol. 285, no. 39, pp. 30214–30223, 2010. View at Publisher · View at Google Scholar · View at Scopus
  72. O. Barak, M. A. Lazzaro, N. S. Cooch, D. J. Picketts, and R. Shiekhattar, “A tissue-specific, naturally occurring human SNF2L variant inactivates chromatin remodeling,” The Journal of Biological Chemistry, vol. 279, no. 43, pp. 45130–45138, 2004. View at Publisher · View at Google Scholar · View at Scopus
  73. P. M. Thompson, T. Gotoh, M. Kok, P. S. White, and G. M. Brodeur, “CHD5, a new member of the chromodomain gene family, is preferentially expressed in the nervous system,” Oncogene, vol. 22, no. 7, pp. 1002–1011, 2003. View at Publisher · View at Google Scholar · View at Scopus
  74. J. I. Wu, J. Lessard, I. A. Olave et al., “Regulation of dendritic development by neuron-specific chromatin remodeling complexes,” Neuron, vol. 56, no. 1, pp. 94–108, 2007. View at Publisher · View at Google Scholar · View at Scopus
  75. M. Lange, B. Kaynak, U. B. Forster et al., “Regulation of muscle development by DPF3, a novel histone acetylation and methylation reader of the BAF chromatin remodeling complex,” Genes and Development, vol. 22, no. 17, pp. 2370–2384, 2008. View at Publisher · View at Google Scholar · View at Scopus
  76. H. Lickert, J. K. Takeuchi, I. von Both et al., “Baf60c is essential for function of BAF chromatin remodelling complexes in heart development,” Nature, vol. 432, no. 7013, pp. 107–112, 2004. View at Publisher · View at Google Scholar · View at Scopus
  77. S. Kadam and B. M. Emerson, “Transcriptional specificity of human SWI/SNF BRG1 and BRM chromatin remodeling complexes,” Molecular Cell, vol. 11, no. 2, pp. 377–389, 2003. View at Publisher · View at Google Scholar · View at Scopus
  78. M. L. Phelan, S. Sif, G. J. Narlikar, and R. E. Kingston, “Reconstitution of a core chromatin remodeling complex from SWI/SNF subunits,” Molecular Cell, vol. 3, no. 2, pp. 247–253, 1999. View at Publisher · View at Google Scholar · View at Scopus
  79. I. J. Miller and J. J. Bieker, “A novel, erythroid cell-specific murine transcription factor that binds to the CACCC element and is related to the Kruppel family of nuclear proteins,” Molecular and Cellular Biology, vol. 13, no. 5, pp. 2776–2786, 1993. View at Google Scholar · View at Scopus
  80. C.-H. Lee, M. R. Murphy, J.-S. Lee, and J. H. Chung, “Targeting a SWI/SNF-related chromatin remodeling complex to the β- globin promoter in erythroid cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 22, pp. 12311–12315, 1999. View at Publisher · View at Google Scholar · View at Scopus
  81. P. McDonel, I. Costello, and B. Hendrich, “Keeping things quiet: roles of NuRD and Sin3 co-repressor complexes during mammalian development,” International Journal of Biochemistry and Cell Biology, vol. 41, no. 1, pp. 108–116, 2009. View at Publisher · View at Google Scholar · View at Scopus
  82. X. Li, S. Jia, S. Wang, Y. Wang, and A. Meng, “Mta3-NuRD complex is a master regulator for initiation of primitive hematopoiesis in vertebrate embryos,” Blood, vol. 114, no. 27, pp. 5464–5472, 2009. View at Publisher · View at Google Scholar · View at Scopus
  83. N. Fujita, D. L. Jaye, C. Geigerman et al., “MTA3 and the Mi-2/NuRD complex regulate cell fate during B lymphocyte differentiation,” Cell, vol. 119, no. 1, pp. 75–86, 2004. View at Publisher · View at Google Scholar · View at Scopus
  84. X. Le Guezennec, M. Vermeulen, A. B. Brinkman et al., “MBD2/NuRD and MBD3/NuRD, two distinct complexes with different biochemical and functional properties,” Molecular and Cellular Biology, vol. 26, no. 3, pp. 843–851, 2006. View at Publisher · View at Google Scholar · View at Scopus
  85. B. Hendrich, J. Guy, B. Ramsahoye, V. A. Wilson, and A. Bird, “Closely related proteins MBD2 and MBD3 play distinctive but interacting roles in mouse development,” Genes and Development, vol. 15, no. 6, pp. 710–723, 2001. View at Publisher · View at Google Scholar · View at Scopus
  86. K. Kaji, I. M. Caballero, R. MacLeod, J. Nichols, V. A. Wilson, and B. Hendrich, “The NuRD component Mbd3 is required for pluripotency of embryonic stem cells,” Nature Cell Biology, vol. 8, no. 3, pp. 285–292, 2006. View at Publisher · View at Google Scholar · View at Scopus
  87. Y. Shi, F. Lan, C. Matson et al., “Histone demethylation mediated by the nuclear amine oxidase homolog LSD1,” Cell, vol. 119, no. 7, pp. 941–953, 2004. View at Publisher · View at Google Scholar · View at Scopus
  88. S. Y. R. Dent and J. Chandra, “The lasting influence of LSD1 in the blood,” eLife, vol. 2013, no. 2, Article ID e00963, 2013. View at Publisher · View at Google Scholar · View at Scopus
  89. N. Pottier, W. Yang, M. Assem et al., “The SWI/SNF chromatin-remodeling complex and glucocorticoid resistance in acute lymphoblastic leukemia,” Journal of the National Cancer Institute, vol. 100, no. 24, pp. 1792–1803, 2008. View at Publisher · View at Google Scholar · View at Scopus
  90. C. Plass, S. M. Pfister, A. M. Lindroth, O. Bogatyrova, R. Claus, and P. Lichter, “Mutations in regulators of the epigenome and their connections to global chromatin patterns in cancer,” Nature Reviews Genetics, vol. 14, no. 11, pp. 765–780, 2013. View at Publisher · View at Google Scholar · View at Scopus
  91. Y. Qu, A. Lennartsson, V. I. Gaidzik et al., “Differential methylation in CN-AML preferentially targets non-CGI regions and is dictated by DNMT3A mutational status and associated with predominant hypomethylation of HOX genes,” Epigenetics, vol. 9, no. 8, pp. 1108–1119, 2014. View at Publisher · View at Google Scholar
  92. The Cancer Genome Atlas Research Network, “Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia,” The New England Journal of Medicine, vol. 368, no. 22, pp. 2059–2074, 2013. View at Publisher · View at Google Scholar
  93. V. I. Kashuba, R. Z. Gizatullin, A. I. Protopopov et al., “NotI linking/jumping clones of human chromosome 3: mapping of the TFRC, RAB7 and HAUSP genes to regions rearranged in leukemia and deleted in solid tumors,” FEBS Letters, vol. 419, no. 2-3, pp. 181–185, 1997. View at Publisher · View at Google Scholar · View at Scopus
  94. A. Rynditch, Y. Pekarsky, S. Schnittger, and K. Gardiner, “Leukemia breakpoint region in 3q21 is gene rich,” Gene, vol. 193, no. 1, pp. 49–57, 1997. View at Publisher · View at Google Scholar · View at Scopus
  95. T. Stopka, D. Zakova, O. Fuchs et al., “Chromatin remodeling gene SMARCA5 is dysregulated in primitive hematopoietic cells of acute leukemia,” Leukemia, vol. 14, no. 7, pp. 1247–1252, 2000. View at Publisher · View at Google Scholar · View at Scopus
  96. V. Torrano, I. Chernukhin, F. Docquier et al., “CTCF regulates growth and erythroid differentiation of human myeloid leukemia cells,” The Journal of Biological Chemistry, vol. 280, no. 30, pp. 28152–28161, 2005. View at Publisher · View at Google Scholar · View at Scopus
  97. F. Rosenbauer, S. Koschmieder, U. Steidl, and D. G. Tenen, “Effect of transcription-factor concentrations on leukemic stem cells,” Blood, vol. 106, no. 5, pp. 1519–1524, 2005. View at Publisher · View at Google Scholar · View at Scopus
  98. M. Dluhosova, N. Curik, J. Vargova, A. Jonasova, T. Zikmund, and T. Stopka, “Epigenetic control of SPI1 gene by CTCF and ISWI ATPase SMARCA5,” PLoS ONE, vol. 9, no. 2, Article ID e87448, 2014. View at Publisher · View at Google Scholar · View at Scopus
  99. I. V. Tereshchenko, H. Zhong, M. A. Chekmareva et al., “ERG and CHD1 heterogeneity in prostate cancer: use of confocal microscopy in assessment of microscopic foci,” The Prostate, vol. 74, no. 15, pp. 1551–1559, 2014. View at Publisher · View at Google Scholar
  100. S. C. Baca, D. Prandi, M. S. Lawrence et al., “Punctuated evolution of prostate cancer genomes,” Cell, vol. 153, no. 3, pp. 666–677, 2013. View at Google Scholar
  101. J. Burrage, A. Termanis, A. Geissner, K. Myant, K. Gordon, and I. Stancheva, “The SNF2 family ATPase LSH promotes phosphorylation of H2AX and efficient repair of DNA double-strand breaks in mammalian cells,” Journal of Cell Science, vol. 125, no. 22, pp. 5524–5534, 2012. View at Publisher · View at Google Scholar · View at Scopus
  102. K. Myant and I. Stancheva, “LSH cooperates with DNA methyltransferases to repress transcription,” Molecular and Cellular Biology, vol. 28, no. 1, pp. 215–226, 2008. View at Publisher · View at Google Scholar · View at Scopus
  103. K. Myant, A. Termanis, A. Y. M. Sundaram et al., “LSH and G9a/GLP complex are required for developmentally programmed DNA methylation,” Genome Research, vol. 21, no. 1, pp. 83–94, 2011. View at Publisher · View at Google Scholar · View at Scopus
  104. S. Xi, H. Zhu, H. Xu, A. Schmidtmann, T. M. Geiman, and K. Muegge, “Lsh controls Hox gene silencing during development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 36, pp. 14366–14371, 2007. View at Publisher · View at Google Scholar · View at Scopus
  105. R. A. Alharbi, R. Pettengell, H. S. Pandha, and R. Morgan, “The role of HOX genes in normal hematopoiesis and acute leukemia,” Leukemia, vol. 27, no. 5, pp. 1000–1008, 2013. View at Publisher · View at Google Scholar · View at Scopus
  106. J. Krosl, A. Mamo, J. Chagraoui et al., “Amutant allele of the Swi/Snf member BAF250a determines the pool size of fetal liver hemopoietic stem cell populations,” Blood, vol. 116, no. 10, pp. 1678–1684, 2010. View at Publisher · View at Google Scholar · View at Scopus
  107. H. Huang, S.-M. Chen, L.-B. Pan, J. Yao, and H.-T. Ma, “Loss of function of SWI/SNF chromatin remodeling genes leads to genome instability of human lung cancer,” Oncology Reports, pp. 283–291, 2014. View at Publisher · View at Google Scholar
  108. M. Khursheed, J. N. Kolla, V. Kotapalli et al., “ARID1B, a member of the human SWI/SNF chromatin remodeling complex, exhibits tumour-suppressor activities in pancreatic cancer cell lines,” British Journal of Cancer, vol. 108, no. 10, pp. 2056–2062, 2013. View at Publisher · View at Google Scholar · View at Scopus
  109. M. Buscarlet, V. Krasteva, L. Ho et al., “Essential role of BRG, the ATPase subunit of BAF chromatin remodeling complexes, in leukemia maintenance,” Blood, vol. 123, no. 11, pp. 1720–1728, 2014. View at Publisher · View at Google Scholar · View at Scopus
  110. J. Shi, W. A. Whyte, C. J. Zepeda-Mendoza et al., “Role of SWI/SNF in acute leukemia maintenance and enhancer-mediated Myc regulation,” Genes & Development, vol. 27, no. 24, pp. 2648–2662, 2013. View at Publisher · View at Google Scholar · View at Scopus
  111. D. W. Lee, K. Zhang, Z.-Q. Ning et al., “Proliferation-associated SNF2-like gene (PASG): a SNF2 family member altered in leukemia,” Cancer Research, vol. 60, no. 13, pp. 3612–3622, 2000. View at Google Scholar · View at Scopus
  112. F. Grand, S. Kulkarni, A. Chase, J. M. Goldman, M. Gordon, and N. C. P. Cross, “Frequent deletion of hSNF5/INI1, a component of the SWI/SNF complex, in chronic myeloid leukemia,” Cancer Research, vol. 59, no. 16, pp. 3870–3874, 1999. View at Google Scholar · View at Scopus
  113. B. G. Wilson and C. W. M. Roberts, “SWI/SNF nucleosome remodellers and cancer,” Nature Reviews Cancer, vol. 11, no. 7, pp. 481–492, 2011. View at Publisher · View at Google Scholar · View at Scopus
  114. A. H. Shain and J. R. Pollack, “The spectrum of SWI/SNF mutations, ubiquitous in human cancers,” PLoS ONE, vol. 8, no. 1, Article ID e55119, 2013. View at Publisher · View at Google Scholar · View at Scopus
  115. F. O. Bagger, N. Rapin, K. Theilgaard-Mönch et al., “HemaExplorer: a database of mRNA expression profiles in normal and malignant haematopoiesis,” Nucleic Acids Research, vol. 41, pp. D1034–D1039, 2013. View at Publisher · View at Google Scholar · View at Scopus