Skip to main content
Log in

ATP Dependent Chromatin Remodeling Enzymes in Embryonic Stem Cells

  • Published:
Stem Cell Reviews and Reports Aims and scope Submit manuscript

Abstract

Embryonic stem (ES) cells are pluripotent cells that can self renew or be induced to differentiate into multiple cell lineages, and thus have the potential to be utilized in regenerative medicine. Key pluripotency specific factors (Oct 4/Sox2/Nanog/Klf4) maintain the pluripotent state by activating expression of pluripotency specific genes and by inhibiting the expression of developmental regulators. Pluripotent ES cells are distinguished from differentiated cells by a specialized chromatin state that is required to epigenetically regulate the ES cell phenotype. Recent studies show that in addition to pluripotency specific factors, chromatin remodeling enzymes play an important role in regulating ES cell chromatin and the capacity to self-renew and to differentiate. Here we review recent studies that delineate the role of ATP dependent chromatin remodeling enzymes in regulating ES cell chromatin structure.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Okita, K., Ichisaka, T., & Yamanaka, S. (2007). Generation of germline-competent induced pluripotent stem cells. Nature, 448, 313–317.

    Article  PubMed  CAS  Google Scholar 

  2. Takahashi, K., & Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126, 663–676.

    Article  PubMed  CAS  Google Scholar 

  3. Wernig, M., Meissner, A., Foreman, R., et al. (2007). In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature, 448, 318–324.

    Article  PubMed  CAS  Google Scholar 

  4. Yu, J., Vodyanik, M. A., Smuga-Otto, K., et al. (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science, 318, 1917–1920.

    Article  PubMed  CAS  Google Scholar 

  5. Jiang, J., Chan, Y. S., Loh, Y. H., et al. (2008). A core Klf circuitry regulates self-renewal of embryonic stem cells. Nat Cell Biol, 10, 353–360.

    Article  PubMed  CAS  Google Scholar 

  6. Kim, J., Chu, J., Shen, X., Wang, J., & Orkin, S. H. (2008). An extended transcriptional network for pluripotency of embryonic stem cells. Cell, 132, 1049–1061.

    Article  PubMed  CAS  Google Scholar 

  7. Loh, Y. H., Wu, Q., Chew, J. L., et al. (2006). The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet, 38, 431–440.

    Article  PubMed  CAS  Google Scholar 

  8. Keenen, B., & de la Serna, I. L. (2009). Chromatin remodeling in embryonic stem cells: regulating the balance between pluripotency and differentiation. J Cell Physiol, 219, 1–7.

    Article  PubMed  CAS  Google Scholar 

  9. Hayes, J. J., & Wolffe, A. P. (1992). The interaction of transcription factors with nucleosomal DNA. Bioessays, 14, 597–603.

    Article  PubMed  CAS  Google Scholar 

  10. Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F., & Richmond, T. J. (1997). Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature, 389, 251–260.

    Article  PubMed  CAS  Google Scholar 

  11. Segal, E., & Widom, J. (2009). What controls nucleosome positions? Trends Genet, 25, 335–343.

    Article  PubMed  CAS  Google Scholar 

  12. Simpson, R. T. (1990). Nucleosome positioning can affect the function of a cis-acting DNA element in vivo. Nature, 343, 387–389.

    Article  PubMed  CAS  Google Scholar 

  13. Simpson, R. T. (1991). Nucleosome positioning: occurrence, mechanisms, and functional consequences. Prog Nucleic Acid Res Mol Biol, 40, 143–184.

    Article  PubMed  CAS  Google Scholar 

  14. Imbalzano, A. N., Kwon, H., Green, M. R., & Kingston, R. E. (1994). Facilitated binding of TATA-binding protein to nucleosomal DNA. Nature, 370, 481–485.

    Article  PubMed  CAS  Google Scholar 

  15. Bernstein, E., & Hake, S. B. (2006). The nucleosome: a little variation goes a long way. Biochem Cell Biol, 84, 505–517.

    Article  PubMed  CAS  Google Scholar 

  16. Luger, K. (2006). Dynamic nucleosomes. Chromosome Res, 14, 5–16.

    Article  PubMed  CAS  Google Scholar 

  17. Ruthenburg, A. J., Li, H., Patel, D. J., & Allis, C. D. (2007). Multivalent engagement of chromatin modifications by linked binding modules. Nature Reviews. Molecular Cell Biology, 8, 983–994.

    Article  PubMed  CAS  Google Scholar 

  18. Dekker, J. (2003). A closer look at long-range chromosomal interactions. Trends Biochem Sci, 28, 277–280.

    Article  PubMed  CAS  Google Scholar 

  19. Dillon, N. (2004). Heterochromatin structure and function. Biol Cell, 96, 631–637.

    Article  PubMed  CAS  Google Scholar 

  20. Fan, Y., Nikitina, T., Zhao, J., et al. (2005). Histone H1 depletion in mammals alters global chromatin structure but causes specific changes in gene regulation. Cell, 123, 1199–1212.

    Article  PubMed  CAS  Google Scholar 

  21. Faast, R., Thonglairoam, V., Schulz, T. C., et al. (2001). Histone variant H2A.Z is required for early mammalian development. Curr Biol, 11, 1183–1187.

    Article  PubMed  CAS  Google Scholar 

  22. Creyghton, M. P., Markoulaki, S., Levine, S. S., et al. (2008). H2AZ is enriched at polycomb complex target genes in ES cells and is necessary for lineage commitment. Cell, 135, 649–661.

    Article  PubMed  CAS  Google Scholar 

  23. Thakar A, Gupta P, Ishibashi T, et al (2009) H2A.Z and H3.3 histone variants affect nucleosome structure: biochemical and biophysical studies. Biochem

  24. Li, B., Pattenden, S. G., Lee, D., et al. (2005). Preferential occupancy of histone variant H2AZ at inactive promoters influences local histone modifications and chromatin remodeling. Proc Natl Acad Sci USA, 102, 18385–18390.

    Article  PubMed  CAS  Google Scholar 

  25. Barski, A., Cuddapah, S., Cui, K., et al. (2007). High-resolution profiling of histone methylations in the human genome. Cell, 129, 823–837.

    Article  PubMed  CAS  Google Scholar 

  26. Kouzarides, T. (2007). Chromatin modifications and their function. Cell, 128, 693–705.

    Article  PubMed  CAS  Google Scholar 

  27. Azuara, V., Perry, P., Sauer, S., et al. (2006). Chromatin signatures of pluripotent cell lines. Nat Cell Biol, 8, 532–538.

    Article  PubMed  CAS  Google Scholar 

  28. Bernstein, B. E., Mikkelsen, T. S., Xie, X., et al. (2006). A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell, 125, 315–326.

    Article  PubMed  CAS  Google Scholar 

  29. Meshorer, E., & Misteli, T. (2006). Chromatin in pluripotent embryonic stem cells and differentiation. Nature Reviews. Molecular Cell biology, 7, 540–546.

    Article  PubMed  CAS  Google Scholar 

  30. Meshorer, E., Yellajoshula, D., George, E., Scambler, P. J., Brown, D. T., & Misteli, T. (2006). Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Developments in Cell, 10, 105–116.

    Article  CAS  Google Scholar 

  31. Efroni, S., Duttagupta, R., Cheng, J., et al. (2008). Global transcription in pluripotent embryonic stem cells. Cell Stem Cell, 2, 437–447.

    Article  PubMed  CAS  Google Scholar 

  32. Dai, B., & Rasmussen, T. P. (2007). Global epiproteomic signatures distinguish embryonic stem cells from differentiated cells. Stem Cells, 25, 2567–2574.

    Article  PubMed  CAS  Google Scholar 

  33. Wen, B., Wu, H., Shinkai, Y., Irizarry, R. A., & Feinberg, A. P. (2009). Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nat Genet, 41, 246–250.

    Article  PubMed  CAS  Google Scholar 

  34. Marks, H., Chow, J. C., Denissov, S., et al. (2009). High-resolution analysis of epigenetic changes associated with X inactivation. Genome Res, 19, 1361–1373.

    Article  PubMed  CAS  Google Scholar 

  35. Wong, L. H., Ren, H., Williams, E., et al. (2009). Histone H3.3 incorporation provides a unique and functionally essential telomeric chromatin in embryonic stem cells. Genome Res, 19, 404–414.

    Article  PubMed  CAS  Google Scholar 

  36. Boyer, L. A., Plath, K., Zeitlinger, J., et al. (2006). Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature, 441, 349–353.

    Article  PubMed  CAS  Google Scholar 

  37. Kirmizis, A., Bartley, S. M., Kuzmichev, A., et al. (2004). Silencing of human polycomb target genes is associated with methylation of histone H3 Lys 27. Genes Dev, 18, 1592–1605.

    Article  PubMed  CAS  Google Scholar 

  38. Schuettengruber, B., Chourrout, D., Vervoort, M., Leblanc, B., & Cavalli, G. (2007). Genome regulation by polycomb and trithorax proteins. Cell, 128, 735–745.

    Article  PubMed  CAS  Google Scholar 

  39. Cloos, P. A., Christensen, J., Agger, K., & Helin, K. (2008). Erasing the methyl mark: histone demethylases at the center of cellular differentiation and disease. Genes Dev, 22, 1115–1140.

    Article  PubMed  CAS  Google Scholar 

  40. Loh, Y. H., Zhang, W., Chen, X., George, J., & Ng, H. H. (2007). Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate self-renewal in embryonic stem cells. Genes Dev, 21, 2545–2557.

    Article  PubMed  CAS  Google Scholar 

  41. Pasini, D., Hansen, K. H., Christensen, J., Agger, K., Cloos, P. A., & Helin, K. (2008). Coordinated regulation of transcriptional repression by the RBP2 H3K4 demethylase and Polycomb-Repressive Complex 2. Genes Dev, 22, 1345–1355.

    Article  PubMed  CAS  Google Scholar 

  42. Duncan, E. M., Muratore-Schroeder, T. L., Cook, R. G., et al. (2008). Cathepsin L proteolytically processes histone H3 during mouse embryonic stem cell differentiation. Cell, 135, 284–294.

    Article  PubMed  CAS  Google Scholar 

  43. Gutierrez, J. L., Chandy, M., Carrozza, M. J., & Workman, J. L. (2007). Activation domains drive nucleosome eviction by SWI/SNF. European Molecular Biology Organization journal, 26, 730–740.

    CAS  Google Scholar 

  44. Li, B., Carey, M., & Workman, J. L. (2007). The role of chromatin during transcription. Cell, 128, 707–719.

    Article  PubMed  CAS  Google Scholar 

  45. Sif, S. (2004). ATP-dependent nucleosome remodeling complexes: enzymes tailored to deal with chromatin. J Cell Biol, 91, 1087–1098.

    CAS  Google Scholar 

  46. de la Serna, I. L., Ohkawa, Y., & Imbalzano, A. N. (2006). Chromatin remodelling in mammalian differentiation: lessons from ATP-dependent remodellers. Nature Reviews. Genetics, 7, 461–473.

    Article  PubMed  CAS  Google Scholar 

  47. Phelan, M. L., Sif, S., Narlikar, G. J., & Kingston, R. E. (1999). Reconstitution of a core chromatin remodeling complex from SWI/SNF subunits. Molecular Cell, 3, 247–253.

    Article  PubMed  CAS  Google Scholar 

  48. Moshkin, Y. M., Mohrmann, L., van Ijcken, W. F., & Verrijzer, C. P. (2007). Functional differentiation of SWI/SNF remodelers in transcription and cell cycle control. Mol Cell Biol, 27, 651–661.

    Article  PubMed  CAS  Google Scholar 

  49. Wang, Z., Zhai, W., Richardson, J. A., et al. (2004). Polybromo protein BAF180 functions in mammalian cardiac chamber maturation. Genes Dev, 18, 3106–3116.

    Article  PubMed  CAS  Google Scholar 

  50. Hsiao, P. W., Fryer, C. J., Trotter, K. W., Wang, W., & Archer, T. K. (2003). BAF60a mediates critical interactions between nuclear receptors and the BRG1 chromatin-remodeling complex for transactivation. Mol Cell Biol, 23, 6210–6220.

    Article  PubMed  CAS  Google Scholar 

  51. Link, K. A., Burd, C. J., Williams, E., et al. (2005). BAF57 governs androgen receptor action and androgen-dependent proliferation through SWI/SNF. Mol Cell Biol, 25, 2200–2215.

    Article  PubMed  CAS  Google Scholar 

  52. Simone, C., Forcales, S. V., Hill, D. A., Imbalzano, A. N., Latella, L., & Puri, P. L. (2004). p38 pathway targets SWI-SNF chromatin-remodeling complex to muscle-specific loci. Nat Genet, 36, 738–743.

    Article  PubMed  CAS  Google Scholar 

  53. Oh, J., Sohn, D. H., Ko, M., Chung, H., Jeon, S. H., & Seong, R. H. (2008). BAF60a interacts with p53 to recruit the SWI/SNF complex. J Biol Chem, 283, 11924–11934.

    Article  PubMed  CAS  Google Scholar 

  54. Lee S, Kim DH, Goo YH, Lee YC, Lee SK, Lee JW (2009) Crucial roles for interactions between Mll3/4 and Ini1 in Nuclear Receptor Transactivation. Molecular Endocrinology

  55. Bultman, S., Gebuhr, T., Yee, D., et al. (2000). A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Molecular Cell, 6, 1287–1295.

    Article  PubMed  CAS  Google Scholar 

  56. Guidi, C. J., Sands, A. T., Zambrowicz, B. P., et al. (2001). Disruption of Ini1 leads to peri-implantation lethality and tumorigenesis in mice. Mol Cell Biol, 21, 3598–3603.

    Article  PubMed  CAS  Google Scholar 

  57. Klochendler-Yeivin, A., Fiette, L., Barra, J., Muchardt, C., Babinet, C., & Yaniv, M. (2000). The murine SNF5/INI1 chromatin remodeling factor is essential for embryonic development and tumor suppression. European Molecular Biology Organization Reports, 1, 500–506.

    PubMed  CAS  Google Scholar 

  58. Roberts, C. W., Galusha, S. A., McMenamin, M. E., Fletcher, C. D., & Orkin, S. H. (2000). Haploinsufficiency of Snf5 (integrase interactor 1) predisposes to malignant rhabdoid tumors in mice. Proc Natl Acad Sci USA, 97, 13796–13800.

    Article  PubMed  CAS  Google Scholar 

  59. Lickert, H., Takeuchi, J. K., Von Both, I., et al. (2004). Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature, 432, 107–112.

    Article  PubMed  CAS  Google Scholar 

  60. Gao, X., Tate, P., Hu, P., Tjian, R., Skarnes, W. C., & Wang, Z. (2008). ES cell pluripotency and germ-layer formation require the SWI/SNF chromatin remodeling component BAF250a. Proc Natl Acad Sci USA, 105, 6656–6661.

    Article  PubMed  Google Scholar 

  61. Muchardt, C., Bourachot, B., Reyes, J. C., & Yaniv, M. (1998). ras transformation is associated with decreased expression of the brm/SNF2alpha ATPase from the mammalian SWI-SNF complex. European Molecular Biology Organization Journal, 17, 223–231.

    CAS  Google Scholar 

  62. Bultman, S. J., Gebuhr, T. C., Pan, H., Svoboda, P., Schultz, R. M., & Magnuson, T. (2006). Maternal BRG1 regulates zygotic genome activation in the mouse. Genes Dev, 20, 1744–1754.

    Article  PubMed  CAS  Google Scholar 

  63. Dauvillier, S., Ott, M. O., Renard, J. P., & Legouy, E. (2001). BRM (SNF2alpha) expression is concomitant to the onset of vasculogenesis in early mouse postimplantation development. Mech Dev, 101, 221–225.

    Article  PubMed  CAS  Google Scholar 

  64. Kaeser MD, Aslanian A, Dong MQ, Yates JR, Emerson BM (2008) Brd7, a novel PBAF-specific SWI/SNF subunit, is required for target gene activation and repression in embryonic stem cells. Journal of Biological Chemistry

  65. Ho, L., Ronan, J. L., Wu, J., et al. (2009). An embryonic stem cell chromatin remodeling complex, esBAF, is essential for embryonic stem cell self-renewal and pluripotency. Proc Natl Acad Sci USA, 106, 5181–5186.

    Article  PubMed  Google Scholar 

  66. Fazzio, T. G., Huff, J. T., & Panning, B. (2008). An RNAi screen of chromatin proteins identifies Tip60-p400 as a regulator of embryonic stem cell identity. Cell, 134, 162–174.

    Article  PubMed  CAS  Google Scholar 

  67. Liang, J., Wan, M., Zhang, Y., et al. (2008). Nanog and Oct4 associate with unique transcriptional repression complexes in embryonic stem cells. Nat Cell Biol, 10, 731–739.

    Article  PubMed  CAS  Google Scholar 

  68. Ho, L., Jothi, R., Ronan, J. L., Cui, K., Zhao, K., & Crabtree, G. R. (2009). An embryonic stem cell chromatin remodeling complex, esBAF, is an essential component of the core pluripotency transcriptional network. Proc Natl Acad Sci USA, 106, 5187–5191.

    Article  PubMed  Google Scholar 

  69. Kidder, B. L., Palmer, S., & Knott, J. G. (2009). SWI/SNF-Brg1 regulates self-renewal and occupies core pluripotency-related genes in embryonic stem cells. Stem Cells, 27, 317–328.

    Article  PubMed  CAS  Google Scholar 

  70. Nagl, N. G., Jr., Wang, X., Patsialou, A., Van Scoy, M., & Moran, E. (2007). Distinct mammalian SWI/SNF chromatin remodeling complexes with opposing roles in cell-cycle control. European Molecular Biology Organization Journal, 26, 752–763.

    CAS  Google Scholar 

  71. Yan, Z., Wang, Z., Sharova, L., et al. (2008). BAF250B-associated SWI/SNF chromatin-remodeling complex is required to maintain undifferentiated mouse embryonic stem cells. Stem Cells, 26, 1155–1165.

    Article  PubMed  CAS  Google Scholar 

  72. Schaniel C, Ang YS, Ratnakumar K, et al (2009) Smarcc1/Baf155 couples self-renewal gene repression with changes in chromatin structure in mouse embryonic stem cells. Stem Cells

  73. Boyer, L. A., Latek, R. R., & Peterson, C. L. (2004). The SANT domain: a unique histone-tail-binding module? Nature Reviews. Molecular Cell Biology, 5, 158–163.

    Article  PubMed  CAS  Google Scholar 

  74. LeRoy, G., Orphanides, G., Lane, W. S., & Reinberg, D. (1998). Requirement of RSF and FACT for transcription of chromatin templates in vitro. Science, 282, 1900–1904.

    Article  PubMed  CAS  Google Scholar 

  75. Bozhenok, L., Wade, P. A., & Varga-Weisz, P. (2002). WSTF-ISWI chromatin remodeling complex targets heterochromatic replication foci. European Molecular Biology Organization Journal, 21, 2231–2241.

    CAS  Google Scholar 

  76. Strohner, R., Nemeth, A., Jansa, P., et al. (2001). NoRC—a novel member of mammalian ISWI-containing chromatin remodeling machines. European Molecular Biology Organization Journal, 20, 4892–4900.

    CAS  Google Scholar 

  77. Poot, R. A., Dellaire, G., Hulsmann, B. B., et al. (2000). HuCHRAC, a human ISWI chromatin remodelling complex contains hACF1 and two novel histone-fold proteins. European Molecular Biology Organization Journal, 19, 3377–3387.

    CAS  Google Scholar 

  78. Bochar, D. A., Savard, J., Wang, W., et al. (2000). A family of chromatin remodeling factors related to Williams syndrome transcription factor. Proc Natl Acad Sci USA, 97, 1038–1043.

    Article  PubMed  CAS  Google Scholar 

  79. He, X., Fan, H. Y., Garlick, J. D., & Kingston, R. E. (2008). Diverse regulation of SNF2h chromatin remodeling by noncatalytic subunits. Biochemist, 47, 7025–7033.

    Article  CAS  Google Scholar 

  80. Collins, N., Poot, R. A., Kukimoto, I., Garcia-Jimenez, C., Dellaire, G., & Varga-Weisz, P. D. (2002). An ACF1-ISWI chromatin-remodeling complex is required for DNA replication through heterochromatin. Nat Genet, 32, 627–632.

    Article  PubMed  CAS  Google Scholar 

  81. Cavellan, E., Asp, P., Percipalle, P., & Farrants, A. K. (2006). The WSTF-SNF2h chromatin remodeling complex interacts with several nuclear proteins in transcription. J Biol Chem, 281, 16264–16271.

    Article  PubMed  CAS  Google Scholar 

  82. Santoro, R., & Grummt, I. (2005). Epigenetic mechanism of rRNA gene silencing: temporal order of NoRC-mediated histone modification, chromatin remodeling, and DNA methylation. Mol Cell Biol, 25, 2539–2546.

    Article  PubMed  CAS  Google Scholar 

  83. Stopka, T., & Skoultchi, A. I. (2003). The ISWI ATPase Snf2h is required for early mouse development. Proc Natl Acad Sci USA, 100, 14097–14102.

    Article  PubMed  CAS  Google Scholar 

  84. Assou, S., Cerecedo, D., Tondeur, S., et al. (2009). A gene expression signature shared by human mature oocytes and embryonic stem cells. BMC Genomics, 10, 10.

    Article  PubMed  CAS  Google Scholar 

  85. Banting, G. S., Barak, O., Ames, T. M., et al. (2005). CECR2, a protein involved in neurulation, forms a novel chromatin remodeling complex with SNF2L. Hum Mol Genet, 14, 513–524.

    Article  PubMed  CAS  Google Scholar 

  86. Barak, O., Lazzaro, M. A., Lane, W. S., Speicher, D. W., Picketts, D. J., & Shiekhattar, R. (2003). Isolation of human NURF: a regulator of Engrailed gene expression. European Molecular Biology Organization Journal, 22, 6089–6100.

    CAS  Google Scholar 

  87. Badenhorst, P., Voas, M., Rebay, I., & Wu, C. (2002). Biological functions of the ISWI chromatin remodeling complex NURF. Genes Dev, 16, 3186–3198.

    Article  PubMed  CAS  Google Scholar 

  88. Badenhorst, P., Xiao, H., Cherbas, L., et al. (2005). The Drosophila nucleosome remodeling factor NURF is required for Ecdysteroid signaling and metamorphosis. Genes Dev, 19, 2540–2545.

    Article  PubMed  CAS  Google Scholar 

  89. Wysocka, J., Swigut, T., Xiao, H., et al. (2006). A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature, 442, 86–90.

    PubMed  CAS  Google Scholar 

  90. Landry, J., Sharov, A. A., Piao, Y., et al. (2008). Essential role of chromatin remodeling protein Bptf in early mouse embryos and embryonic stem cells. PLoS Genetics, 4, e1000241.

    Article  PubMed  CAS  Google Scholar 

  91. Marfella, C. G., & Imbalzano, A. N. (2007). The Chd family of chromatin remodelers. Mutat Res, 618, 30–40.

    PubMed  CAS  Google Scholar 

  92. Flanagan, J. F., Mi, L. Z., Chruszcz, M., et al. (2005). Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature, 438, 1181–1185.

    Article  PubMed  CAS  Google Scholar 

  93. Sims, R. J., 3rd, Millhouse, S., Chen, C. F., et al. (2007). Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Molecular Cell, 28, 665–676.

    Article  PubMed  CAS  Google Scholar 

  94. Gaspar-Maia, A., Alajem, A., Polesso, F., et al. (2009). Chd1 regulates open chromatin and pluripotency of embryonic stem cells. Nature, 460, 863–868.

    PubMed  CAS  Google Scholar 

  95. Konev, A. Y., Tribus, M., Park, S. Y., et al. (2007). CHD1 motor protein is required for deposition of histone variant H3.3 into chromatin in vivo. Science, 317, 1087–1090.

    Article  PubMed  CAS  Google Scholar 

  96. McKittrick, E., Gafken, P. R., Ahmad, K., & Henikoff, S. (2004). Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc Natl Acad Sci USA, 101, 1525–1530.

    Article  PubMed  CAS  Google Scholar 

  97. Hall, J. A., & Georgel, P. T. (2007). CHD proteins: a diverse family with strong ties. Biochem Cell Biol, 85, 463–476.

    Article  PubMed  CAS  Google Scholar 

  98. Denslow, S. A., & Wade, P. A. (2007). The human Mi-2/NuRD complex and gene regulation. Oncogene, 26, 5433–5438.

    Article  PubMed  CAS  Google Scholar 

  99. Gao, H., Lukin, K., Ramirez, J., Fields, S., Lopez, D., & Hagman, J. (2009). Opposing effects of SWI/SNF and Mi-2/NuRD chromatin remodeling complexes on epigenetic reprogramming by EBF and Pax5. Proc Natl Acad Sci USA, 106, 11258–11263.

    Article  PubMed  Google Scholar 

  100. Ramirez-Carrozzi, V. R., Nazarian, A. A., Li, C. C., et al. (2006). Selective and antagonistic functions of SWI/SNF and Mi-2beta nucleosome remodeling complexes during an inflammatory response. Genes Dev, 20, 282–296.

    Article  PubMed  CAS  Google Scholar 

  101. Wade, P. A., Gegonne, A., Jones, P. L., Ballestar, E., Aubry, F., & Wolffe, A. P. (1999). Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation. Nat Genet, 23, 62–66.

    PubMed  CAS  Google Scholar 

  102. Yoshida, T., Hazan, I., Zhang, J., et al. (2008). The role of the chromatin remodeler Mi-2beta in hematopoietic stem cell self-renewal and multilineage differentiation. Genes Dev, 22, 1174–1189.

    Article  PubMed  CAS  Google Scholar 

  103. Williams, C. J., Naito, T., Arco, P. G., et al. (2004). The chromatin remodeler Mi-2beta is required for CD4 expression and T cell development. Immunity, 20, 719–733.

    Article  PubMed  CAS  Google Scholar 

  104. Hendrich, B., Guy, J., Ramsahoye, B., Wilson, V. A., & Bird, A. (2001). Closely related proteins MBD2 and MBD3 play distinctive but interacting roles in mouse development. Genes Dev, 15, 710–723.

    Article  PubMed  CAS  Google Scholar 

  105. Kaji, K., Caballero, I. M., MacLeod, R., Nichols, J., Wilson, V. A., & Hendrich, B. (2006). The NuRD component Mbd3 is required for pluripotency of embryonic stem cells. Nat Cell Biol, 8, 285–292.

    Article  PubMed  CAS  Google Scholar 

  106. Zhu, D., Fang, J., Li, Y., & Zhang, J. (2009). Mbd3, a component of NuRD/Mi-2 complex, helps maintain pluripotency of mouse embryonic stem cells by repressing trophectoderm differentiation. PLoS ONE, 4, e7684.

    Article  PubMed  CAS  Google Scholar 

  107. Allen, M. D., Religa, T. L., Freund, S. M., & Bycroft, M. (2007). Solution structure of the BRK domains from CHD7. J Mol Biol, 371, 1135–1140.

    Article  PubMed  CAS  Google Scholar 

  108. Bosman, E. A., Penn, A. C., Ambrose, J. C., Kettleborough, R., Stemple, D. L., & Steel, K. P. (2005). Multiple mutations in mouse Chd7 provide models for CHARGE syndrome. Hum Mol Genet, 14, 3463–3476.

    Article  PubMed  CAS  Google Scholar 

  109. Vissers, L. E., van Ravenswaaij, C. M., Admiraal, R., et al. (2004). Mutations in a new member of the chromodomain gene family cause CHARGE syndrome. Nat Genet, 36, 955–957.

    Article  PubMed  CAS  Google Scholar 

  110. Lalani, S. R., Safiullah, A. M., Fernbach, S. D., et al. (2006). Spectrum of CHD7 mutations in 110 individuals with CHARGE syndrome and genotype-phenotype correlation. Am J Hum Genet, 78, 303–314.

    Article  PubMed  CAS  Google Scholar 

  111. Schnetz, M. P., Bartels, C. F., Shastri, K., et al. (2009). Genomic distribution of CHD7 on chromatin tracks H3K4 methylation patterns. Genome Res, 19, 590–601.

    Article  PubMed  CAS  Google Scholar 

  112. Kobor, M. S., Venkatasubrahmanyam, S., Meneghini, M. D., et al. (2004). A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biology, 2, E131.

    Article  PubMed  Google Scholar 

  113. Kusch, T., Florens, L., Macdonald, W. H., et al. (2004). Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science, 306, 2084–2087.

    Article  PubMed  CAS  Google Scholar 

  114. Ueda, T., Watanabe-Fukunaga, R., Ogawa, H., et al. (2007). Critical role of the p400/mDomino chromatin-remodeling ATPase in embryonic hematopoiesis. Genes Cells, 12, 581–592.

    Article  PubMed  CAS  Google Scholar 

  115. Hu, Y., Fisher, J. B., Koprowski, S., McAllister, D., Kim, M. S., & Lough, J. (2009). Homozygous disruption of the Tip60 gene causes early embryonic lethality. Dev Dyn, 238, 2912–2921.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ivana L. de la Serna.

Additional information

Financial Support

ILD was supported by the National Institute of Environmental Health Sciences; Grant number: 5K22ES12981, Ohio Cancer Research Associates, American Cancer Society, Ohio Division

Rights and permissions

Reprints and permissions

About this article

Cite this article

Saladi, S.V., de la Serna, I.L. ATP Dependent Chromatin Remodeling Enzymes in Embryonic Stem Cells. Stem Cell Rev and Rep 6, 62–73 (2010). https://doi.org/10.1007/s12015-010-9120-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12015-010-9120-y

Keywords

Navigation