Chromatin remodelling in mammalian differentiation: Lessons from ATP-dependent remodellers

Nature Reviews Genetics

Volumn 7, Issue 6, 2006, Pages 461-473

  De La Serna, Ivana L ^a   Ohkawa, Yasuyuki ^b   Imbalzano, Anthony N ^b  

^a MEDICAL COLLEGE OF OHIO   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE;

ADIPOGENESIS; BONE MARROW CELL; CELL CYCLE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CELL TYPE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; ERYTHROPOIESIS; GENE ACTIVATION; GENE EXPRESSION; GENE REPRESSION; GENE TARGETING; GENETIC LINKAGE; GENETIC RECOMBINATION; GENOME ANALYSIS; MAMMAL; MUSCLE DEVELOPMENT; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; T LYMPHOCYTE; TISSUE SPECIFICITY;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ANIMALS; CELL CYCLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HUMANS;

MAMMALIA;

EID: 33646869229     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg1882     Document Type: Review

References (134)

1. Bork, P. & Koonin, E. V. An expanding family of helicases within the 'DEAD/H' superfamily. Nucleic Acids Res. 21, 751-752 (1993).
2. Henikoff, S. Transcriptional activator components and poxvirus DNA-dependent ATPases comprise a single family. Trends Biochem. Sci. 18, 291-292 (1993).
3. Eisen, J. A., Sweden K. S. & Hanawalt, P. C. Evolution of the SNF2 family of proteins: subfamilies with distinct sequences and functions. Nucleic Acids Res. 23, 2715-2723 (1995).
4. Hassan, A. H. et al. Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes. Cell 111, 369-379 (2002).
5. Boyer, L. A., Latek, R. R. & Peterson, C. L. The SANT domain: a unique histone-tail-binding module? Nature Rev. Mol. Cell Biol. 5, 158-163 (2004).
6. Bannister, A. J. et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410, 120-124 (2001).
7. Lachner, M., O'Carroll, D., Rea, S., Mechtler, K. & Jenuwein, T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410, 116-120 (2001).
8. Flanagan, J. F. et al. Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature 438, 1181-1185 (2005).
9. Sims, R. J. et al. Human but not yeast CHD1 binds directly and selectively to histone H3 methylated at lysine 4 via its tandem chromodomains. J. Biol. Chem. 280, 41789-41792 (2005).
10. de la Cruz, X., Lois, S., Sanchez-Molina, S. & Martinez-Balbas, M. A. Do protein motifs read the histone code? Bioessays 27, 164-175 (2005).
11. Bottomley, M. J. Structures of protein domains that create or recognize histone modifications. EMBO Rep. 5, 464-469 (2004).
12. Smith, C. L. & Peterson, C. L. ATP-dependent chromatin remodeling. Curr. Top. Dev. Biol. 65, 115-148 (2005).
13. Reyes, J. C. et al. Altered control of cellular proliferation in the absence of mammalian brahma (SNF2α). EMBO J. 17, 6979-6991 (1998).
14. Bultman, S. et al. A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol. Cell 6, 1287-1295 (2000).
15. Guidi, C. J. et al. Disruption of Ini1 leads to peri-implantation lethality and tumorigenesis in mice. Mol. Cell. Biol. 21, 3598-3603 (2001).
16. Klochendler-Yeivin, A. et al. The murine SNF5/INI1 chromatin remodeling factor is essential for embryonic development and tumor suppression. EMBO Rep. 1, 500-506 (2000).
17. Roberts, C. W., Galusha, S. A., McMenamin, M. E., Fletcher, C. D. & Orkin, S. H. Haploinsufficiency of Snf5 (integrase interactor 1) predisposes to malignant rhabdoid tumors in mice. Proc. Natl Acad. Sci. USA 97, 13796-13800 (2000).
18. Bultman, S. J., Gebuhr, T. C. & Magnuson, T. 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 Dev. 19, 2849-2861 (2005).
19. Chi, T. H. et al. Sequential roles of Brg, the ATPase subunit of BAF chromatin remodeling complexes, in thymocyte development. Immunity 19, 169-182 (2003).
20. Chi, T. H. et al. Reciprocal regulation of CD4/CD8 expression by SWI/SNF-like BAF complexes. Nature 418, 195-199 (2002). This manuscript, along with references 19 and 21, used mouse models to show that SWI/SNF complexes are involved in both activation and repression of T-cell-specific gene expression, and function at multiple stages of T-cell development.
21. Gebuhr, T. C. et al. The role of Brg1, a catalytic subunit of mammalian chromatin-remodeling complexes, in T cell development. J. Exp. Med. 198, 1937-1949 (2003).
22. Han, S. et al. Peripheral T cells become sensitive to glucocorticoid- and stress-induced apoptosis in transgenic mice overexpressing SRG3. J. Immunol. 167, 805-810 (2001).
23. Williams, C. J. et al. The chromatin remodeler Mi-2β is required for CD4 expression and T cell development. Immunity 20, 719-733 (2004). Through use of a conditional knockout of CHD4, the authors demonstrated that this remodelling enzyme contributed to activation of T-cell-specific gene expression. Previously, this subfamily of enzymes had only been linked to gene repression.
24. Kim, J. K. et al. Srg3, a mouse homolog of yeast SWI3, is essential for early embryogenesis and involved in brain development. Mol. Cell. Biol. 21, 7787-7795 (2001).
25. Gresh, L. et al. The SWI/SNF chromatin-remodeling complex subunit SNF5 is essential for hepatocyte differentiation. EMBO J. 24, 3313-3324 (2005).
26. Lickert, H. et al. Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature 432, 107-112 (2004).
27. Wang, Z. et al. Polybromo protein BAF180 functions in mammalian cardiac chamber maturation. Genes Dev. 18, 3106-3116 (2004).
28. Kowenz-Leutz, E. & Leutz, A. A C/EBP β isoform recruits the SWI/SNF complex to activate myeloid genes. Mol. Cell 4, 735-743 (1999). The first report to identify endogenous mammalian genes regulated by SWI/SNF enzymes. The study also indicated that genes in the same differentiation pathway were differentially regulated by SWI/SNF enzymes.
29. Holstege, F. C. et al. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95, 717-728 (1998).
30. Sudarsanam, P., Iyer, V. R., Brown, P. O. & Winston, F. Whole-genome expression analysis of snf/swi mutants of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 97, 3364-3369 (2000).
31. Joh, T., Hosokawa, Y., Suzuki, R., Takahashi, T. & Seto, M. Establishment of an inducible expression system of chimeric MLL-LTG9 protein and inhibition of Hox a7, Hox b7 and Hox c9 expression by MLL-LTG9 in 32Dcl3 cells. Oncogene 18, 1125-1130 (1999).
32. Schreiner, S. A., Garcia-Cuellar, M. P., Fey, G. H. & Slany, R. K. The leukemogenic fusion of MLL with ENL creates a novel transcriptional transactivator. Leukemia 13, 1525-1533 (1999).
33. Rozenblatt-Rosen, O. et al. The C-terminal SET domains of ALL-1 and TRITHORAX interact with the INI1 and SNR1 proteins, components of the SWI/SNF complex. Proc. Natl Acad. Sci. USA 95, 4152-4157 (1998).
34. Nie, Z. et al. Novel SWI/SNF chromatin-remodeling complexes contain a mixed-lineage leukemia chromosomal translocation partner. Mol. Cell. Biol. 23, 2942-2952 (2003).
35. Armstrong, J. A., Bieker, J. J. & Emerson, B. M. A SWI/SNF-related chromatin remodeling complex, E-RC1, is required for tissue-specific transcriptional regulation by EKLFin vitro. Cell 95, 93-104 (1998).
36. Lee, C. H., Murphy, M. R., Lee, J. S. & Chung, J. H. Targeting a SWI/SNF-related chromatin remodeling complex to the β-globin promoter in erythroid cells. Proc. Natl Acad. Sci. USA 96, 12311-12315 (1999).
37. O'Neill, D. et al. Tissue-specific and developmental stage-specific DNA binding by a mammalian SWI/SNF complex associated with human fetal-to-adult globin gene switching. Proc. Natl Acad. Sci. USA 96, 349-354 (1999).
38. O'Neill, D. W. et al. An ikaros-containing chromatin-remodeling complex in adult-type erythroid cells. Mol. Cell. Biol. 20, 7572-7582 (2000). A complex containing both NuRD and SWI/SNF enzyme subunits was isolated and shown to bind to the β-globin locus with the Ikaros transcription factor, suggesting that multiple classes of ATP-dependent chromatin-remodelling enzyme contribute to globin gene switching during erythropoiesis.
39. Lopez, R. A., Schoetz, S., DeAngelis, K., O'Neill, D. & Bank, A. Multiple hematopoietic defects and delayed globin switching in Ikaros null mice. Proc. Natl Acad. Sci. USA 99, 602-607 (2002).
40. Stopka, T. & Skoultchi, A. I. The ISWI ATPase Snf2h is required for early mouse development. Proc. Natl. Acad. Sci. USA 100, 14097-14102 (2003).
41. Choi, Y. I. et al. Notch1 confers a resistance to glucocorticoid-induced apoptosis on developing thymocytes by down-regulating SRG3 expression. Proc. Natl Acad. Sci. USA 98, 10267-10272 (2001).
42. Bowen, N. J., Fujita, N., Kajita, M. & Wade, P. A. Mi-2/NuRD: multiple complexes for many purposes. Biochim. Biophys. Acta 1677, 52-57 (2004).
43. Winandy, S. Regulation of chromatin structure during thymic T cell development. J. Cell Biochem. 95, 466-477 (2005).
44. Morshead, K. B., Ciccone, D. N., Taverna, S. D., Allis, C. D. & Oettinger, M. A. Antigen receptor loci poised for V(D)J rearrangement are broadly associated with BRG1 and flanked by peaks of histone H3 dimethylated at lysine 4. Proc. Natl Acad. Sci. USA 100, 11577-11582 (2003).
45. Patenge, N., Elkin, S. K. & Oettinger, M. A. ATP-dependent remodeling by SWI/SNF and ISWI proteins stimulates V(D)J cleavage of 5 S arrays. J. Biol. Chem. 279, 35360-35367 (2004).
46. Zhao, K. et al. Rapid and phosphoinositol-dependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell 95, 625-636 (1998). This report provided the first evidence that ATP-dependent chromatin-remodelling enzymes could be regulated by signal-transduction pathways.
47. Cocco, L., Maraldi, N. M. & Manzoli, F. A. New frontiers of inositide-specific phospholipase C in nuclear signalling. Eur. J. Histochem. 48, 83-88 (2004).
48. Martelli, A. M., Manzoli, L. & Cocco, L. Nuclear inositides: facts and perspectives. Pharmacol. Ther. 101, 47-64 (2004).
49. Rando, O. J., Zhao, K., Janmey, P. & Crabtree, G. R. Phosphatidylinositol-dependent actin filament binding by the SWI/SNF-like BAF chromatin remodeling complex. Proc. Natl Acad. Sci. USA 99, 2824-2829 (2002).
50. Alvarez, J. D. et al. The MAR-binding protein SATB1 orchestrates temporal and spatial expression of multiple genes during T-cell development. Genes Dev. 14, 521-535 (2000).
51. Cai, S., Han, H. J. & Kohwi-Shigematsu, T. Tissue-specific nuclear architecture and gene expression regulated by SATB1. Nature Genet. 34, 42-51 (2003).
52. Dickinson, L. A., Joh, T., Kohwi, Y. & Kohwi-Shigematsu, T. A tissue-specific MAR/SAR DNA-binding protein with unusual binding site recognition. Cell 70, 631-645 (1992).
53. Yasui, D., Miyano, M., Cai, S., Varga-Weisz, P. & Kohwi-Shigematsu, T. SATB1 targets chromatin remodelling to regulate genes over long distances. Nature 419, 641-645 (2002). The SATB1 regulatory protein was known to affect gene expression over long distances by manipulation of higher-order chromatin organization. Here, the authors demonstrated that SATB1 function was mediated at least in part through the targeting of multiple ATP-dependent chromatin-remodelling enzymes.
54. Erickson, R. L., Hemati, N., Ross, S. E. & MacDougald, O. A. p300 coactivates the adipogenic transcription factor CCAAT/enhancer-binding protein α. J. Biol. Chem. 276, 16348-16355 (2001).
55. Pedersen, T. A., Kowenz-Leutz, E., Leutz, A. & Nerlov, C. Cooperation between C/EBPαTBP/TFIIB and SWI/SNF recruiting domains is required for adipocyte differentiation. Genes Dev. 15, 3208-3216 (2001). These authors demonstrated that SWI/SNF enzymes facilitated adipogenic differentiation through interaction with an adipogenic activator.
56. Takahashi, N. et al. Overexpression and ribozyme-mediated targeting of transcriptional coactivators CREB-binding protein and p300 revealed their indispensable roles in adipocyte differentiation through the regulation of peroxisome proliferator-activated receptor γ. J. Biol. Chem. 277, 16906-16912 (2002).
57. Salma, N., Xiao, H., Mueller, E. & Imbalzano, A. N. Temporal recruitment of transcription factors and SWI/SNF chromatin-remodeling enzymes during adipogenic induction of the peroxisome proliferator-activated receptor gamma nuclear hormone receptor. Mol. Cell. Biol. 24, 4651-4663 (2004).
58. Soutoglou, E. & Talianidis, I. Coordination of PIC assembly and chromatin remodeling during differentiation-induced gene activation. Science 295, 1901-1904 (2002).
59. Agalioti, T. et al. Ordered recruitment of chromatin modifying and general transcription factors to the IFN-β promoter. Cell 103, 667-678 (2000).
60. Lomvardas, S. & Thanos, D. Nucleosome sliding via TBP DNA binding in vivo. Cell 106, 685-696 (2001).
61. Imbalzano, A. N., Kwon, H., Green, M. R. & Kingston, R. E. Facilitated binding of TATA-binding protein to nucleosomal DNA. Nature 370, 481-485 (1994).
62. Müller, C., Calkhoven, C. F., Sha, X. & Leutz, A. The CCAAT enhancer-binding protein alpha (C/EBPα) requires a SWI/SNF complex for proliferation arrest. J. Biol. Chem. 279, 7353-7358 (2004).
63. Iakova, P., Awad, S. S. & Timchenko, N. A. Aging reduces proliferative capacities of liver by switching pathways of C/EBPα growth arrest. Cell 113, 495-506 (2003).
64. Wang, W. et al. Diversity and specialization of mammalian SWI/SNF complexes. Genes Dev. 10, 2117-2130 (1996). Cloning of the genes encoding subunits of SWI/ SNF complexes revealed gene families and tissue-specific expression of some genes, advancing the concept that chromatin-remodelling enzymes could be modified for specific functions by the inclusion or exclusion of individual enzyme subunits.
65. Olave, I., Wang, W., Xue, Y., Kuo, A. & Crabtree, G. R. Identification of a polymorphic, neuron-specific chromatin remodeling complex. Genes Dev. 16, 2509-2517 (2002).
66. Machida, Y., Murai, K., Miyake, K. & Iijima, S. Expression of chromatin remodeling factors during neural differentiation. J. Biochem. (Tokyo) 129, 43-49 (2001).
67. Reisman, D. N., Sciarrotta, J., Bouldin, T. W., Weissman, B. E. & Funkhouser, W. K. The expression of the SWI/SNF ATPase subunits BRG1 and BRM in normal human tissues. Appl. Immunohistochem. Mol. Morphol. 13, 66-74 (2005).
68. Aihara, T. et al. Cloning and mapping of SMARCA5 encoding hSNF2H, a novel human homologue of Drosophila ISWI. Cytogenet. Cell Genet. 81, 191-193 (1998).
69. Okabe, I. et al. Cloning of human and bovine homologs of SNF2/SWI2: a global activator of transcription in yeast S. cerevisiae. Nucleic Acids Res. 20, 4649-4655 (1992).
70. Lazzaro, M. A. & Picketts, D. J. Cloning and characterization of the murine Imitation Switch (ISWI) genes: differential expression patterns suggest distinct developmental roles for Snf2h and Snf21. J. Neurochem. 77, 1145-1156 (2001).
71. Banting, G. S. et al. CECR2, a protein involved in neurulation, forms a novel chromatin remodeling complex with SNF2L Hum. Mol. Genet. 14, 513-524 (2005).
72. Barak, O. et al. Isolation of human NURF: a regulator of Engrailed gene expression. EMBO J. 22, 6089-6100 (2003).
73. Aigner, S. & Gage, F. H. A small gem with great powers: geminin keeps neural progenitors thriving. Dev. Cell 9, 171-172 (2005).
74. Seo, S. et al. Geminin regulates neuronal differentiation by antagonizing Brg1 activity. Genes Dev. 19, 1723-1734 (2005). The cell-cycle regulator geminin, which was previously implicated in neural-cell-fate acquisition, was shown to function in maintaining the undifferentiated state by antagonizing the pro-differentiation function of the BRG1 subunit of SWI/SNF enzymes during neurogenesis.
75. Seo, S., Richardson, G. A. & Kroll, K. L. The SWI/SNF chromatin remodeling protein Brg1 is required for vertebrate neurogenesis and mediates transactivation of Ngn and NeuroD. Development 132, 105-115 (2005).
76. Hsieh, J. & Gage, F. H. Chromatin remodeling in neural development and plasticity. Curr. Opin. Cell Biol. 17, 664-671 (2005).
77. Battaglioli, E. et al. REST repression of neuronal genes requires components of the hSWI/SNF complex. J. Biol. Chem. 277, 41038-41045 (2002).
78. Watanabe, H. et al. SWI/SNF complex is essential for NRSF-mediated suppression of neuronal genes in human nonsmall cell lung carcinoma cell lines. Oncogene 25, 470-479 (2006).
79. Berkes, C. A. et al. Pbx marks genes for activation by MyoD indicating a role for a homeodomain protein in establishing myogenic potential. Mol. Cell 14, 465-477 (2004).
80. de la Serna, I. L., Carlson, K. A. & Imbalzano, A. N. Mammalian SWI/SNF complexes promote MyoD-mediated muscle differentiation. Nature Genet. 27, 187-190 (2001). This manuscript was the first to demonstrate that interference with SWI/SNF chromatin-remodelling enzyme function not only abrogated gene expression but also inhibited changes in chromatin accessibility at an endogenous, differentiation-specific locus.
81. Roy, K., de la Serna, I. L. & Imbalzano, A. N. The myogenic basic helix-loop-helix family of transcription factors shows similar requirements for SWI/SNF chromatin remodeling enzymes during muscle differentiation in culture. J. Biol. Chem. 277, 33818-33824 (2002).
82. de la Serna, I. L. et al. MyoD targets chromatin remodeling complexes to the myogenin locus prior to forming a stable DNA-bound complex. Mol. Cell. Biol. 25, 3997-4009 (2005). Provides a detailed, mechanistic assessment of the targeting of ATP-dependent chromatin-remodelling enzymes to a muscle-specific promoter.
83. de la Serna, I. L., Roy, K., Carlson, K. A. & Imbalzano, A. N. MyoD can induce cell cycle arrest but not muscle differentiation in the presence of dominant negative SWI/SNF chromatin remodeling enzymes. J. Biol. Chem. 276, 41486-41491 (2001).
84. Simone, C. et al. p38 pathway targets SWI-SNF chromatin-remodeling complex to muscle-specific loci. Nature Genet 36, 738-743 (2004). Showed targeting of SWI/SNF enzymes via the MyoD regulator and indicated that SWI/SNF mediated chromatin remodelling was dependent on the p38 signalling pathway.
85. Blais, A. et al. An initial blueprint for myogenic differentiation. Genes Dev. 19, 553-569 (2005).
86. Cao, Y. et al. Global and gene-specific analyses show distinct roles for Myod and Myog at a common set of promoters. EMBO J. 25, 502-511 (2006).
87. Ohkawa, Y., Marfella, C. G. A. & Imbalzano, A. N. Skeletal muscle specification by Myogenin and Mef2D via the SWI/SNF ATPase Brg1. EMBO J. 25, 490-501 (2006).
88. Knoepfler, P. S. et al. A conserved motif N-terminal to the DNA-binding domains of myogenic bHLH transcription factors mediates cooperative DNA binding with pbx-Meis1/Prep1. Nucleic Acids Res. 27, 3752-3761 (1999).
89. Chaya, D. & Zaret, K. S. Sequential chromatin immunoprecipitation from animal tissues. Methods Enzymol. 376, 361-372 (2004).
90. Strahl, B. D. & Allis, C. D. The language of covalent histone modifications. Nature 403, 41-45 (2000).
91. Pal, S. et al. mSin3A/histone deacetylase 2- and PRMT5-containing Brg1 complex is involved in transcriptional repression of the Myc target gene cad. Mol. Cell. Biol. 23, 7475-7487 (2003).
92. Xu, W. et al. A methylation-mediator complex in hormone signaling. Genes Dev. 18, 144-156 (2004).
93. Breeden, L. & Nasmyth, K. Cell cycle control of the yeast HO gene: cis- and trans-acting regulators. Cell 48, 389-397 (1987).
94. Stern, M., Jensen, R. & Herskowitz, I. Five SWI genes are required for expression of the HO gene in yeast. J. Mol. Biol. 178, 853-868 (1984).
95. Neigeborn, L. & Carlson, M. Genes affecting the regulation of SUC2 gene expression by glucose repression in Saccharomyces cerevisiae. Genetics 108, 845-858 (1984).
96. Kingston, R. E., Bunker, C. A. & Imbalzano, A. N. Repression and activation by multiprotein complexes that alter chromatin structure. Genes Dev. 10, 905-920 (1996).
97. Winston, F. & Carlson, M. Yeast SNF/SWI transcriptional activators and the SPT/SIN chromatin connection. Trends Genet. 8, 387-391 (1992).
98. Kruger, W. & Herskowitz, I. A negative regulator of HO transcription, SIN1 (SPT2), is a nonspecific DNA-binding protein related to HMG1. Mol. Cell. Biol. 11, 4135-4146 (1991).
99. Kruger, W. et al. Amino acid substitutions in the structured domains of histones H3 and H4 partially relieve the requirement of the yeast SWI/SNF complex for transcription. Genes Dev. 9, 2770-2779 (1995).
100. Hirschhorn, J. N., Brown, S. A., Clark, C. D. & Winston, F. Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. Genes Dev. 6, 2288-2298 (1992).
101. Cairns, B. R., Kim, Y. J., Sayre, M. H., Laurent, B. C. & Kornberg, R. D. A multisubunit complex containing the SWI1/ADR6, SWI2/SNF2, SWI3, SNF5, and SNF6 gene products isolated from yeast. Proc. Natl Acad. Sci. USA 91, 1950-1954 (1994).
102. Peterson, C. L., Dingwall, A. & Scott, M. P. Five SWI/SNF gene products are components of a large multisubunit complex required for transcriptional enhancement. Proc. Natl Acad. Sci. USA 91, 2905-2908 (1994).
103. Cote, J., Quinn, J., Workman, J. L. & Peterson, C. L. Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex. Science 265, 53-60 (1994).
104. Kennison, J. A. The Polycomb and trithorax group proteins of Drosophila: trans-regulators of homeotic gene function. Annu. Rev. Genet. 29, 289-303 (1995).
105. Tamkun, J. W. The role of brahma and related proteins in transcription and development. Curr. Opin. Genet. Dev. 5, 473-477 (1995).
106. Tamkun, J. W. et al. brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68, 561-572 (1992).
107. Khavari, P. A., Peterson, C. L., Tamkun, J. W., Mendel, D. B. & Crabtree, G. R. BRG1 contains a conserved domain of the SWI2/SNF2 family necessary for normal mitotic growth and transcription. Nature 366, 170-174 (1993).
108. Muchardt, C. & Yaniv, M. A human homologue of Saccharomyces cerevisiae SNF2/SWI2 and Drosophila brm genes potentiates transcriptional activation by the glucocorticoid receptor. EMBO J. 12, 4279-4290 (1993).
109. Kwon, H., Imbalzano, A. N., Khavari, P. A., Kingston, R. E. & Green, M. R. Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex. Nature 370, 477-481 (1994).
110. Dingwall, A. K. et al. The Drosophila snr1 and brm proteins are related to yeast SWI/SNF proteins and are components of a large protein complex. Mol. Biol. Cell 6, 777-791 (1995).
111. Armstrong, J. A. et al. The Drosophila BRM complex facilitates global transcription by RNA polymerase II. EMBO J. 21, 5245-5254 (2002).
112. Tsukiyama, T., Daniel, C., Tamkun, J. & Wu, C. ISWI, a member of the SWI2/SNF2 ATPase family, encodes the 140 kDa subunit of the nucleosome remodeling factor. Cell 83, 1021-1026 (1995).
113. Goodwin, G. H. Isolation of cDNAs encoding chicken homologues of the yeast SNF2 and Drosophila Brahma proteins. Gene 184, 27-32 (1997).
114. Farrona, S., Hurtado, L., Bowman, J. L. & Reyes, J. C. The Arabidopsis thaliana SNF2 homolog AtBRM controls shoot development and flowering. Development 131, 4965-4975 (2004).
115. Ito, T., Bulger, M., Pazin, M. J., Kobayashi, R. & Kadonaga, J. T. ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 90, 145-155 (1997).
116. Varga-Weisz, P. D. et al. Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II. Nature 388, 598-602 (1997).
117. Badenhorst, P., Voas, M., Rebay, I. & Wu, C. Biological functions of the ISWI chromatin remodeling complex NURF. Genes Dev. 16, 3186-3198 (2002).
118. Badenhorst, P. et al. The Drosophila nucleosome remodeling factor NURF is required for Ecdysteroid signaling and metamorphosis. Genes Dev. 19, 2540-2545 (2005).
119. Deuring, R. et al. The ISWI chromatin-remodeling protein is required for gene expression and the maintenance of higher order chromatin structure in vivo. Mol. Cell 5, 355-365 (2000).
120. Xi, R. & Xie, T. Stem cell self-renewal controlled by chromatin remodeling factors. Science 310, 1487-1489 (2005).
121. Guschin, D. et al. Multiple ISWI ATPase complexes from Xenopus laevis. Functional conservation of an ACF/CHRAC homolog. J. Biol. Chem. 275, 35248-35255 (2000).
122. Bozhenok, L., Wade, P. A. & Varga-Weisz, P. WSTF-ISWI chromatin remodeling complex targets heterochromatic replication foci. EMBO J. 21, 2231-2241 (2002).
123. Collins, N. et al. An ACF1-ISWI chromatin-remodeling complex is required for DNA replication through heterochromatin. Nature Genet. 32, 627-632 (2002).
124. Dirscherl, S. S., Henry, J. J. & Krebs, J. E. Neural and eye-specific defects associated with loss of the Imitation Switch (ISWI) chromatin remodeler in Xenopus laevis. Mech. Dev. 122, 1157-1170 (2005).
125. Kehle, J. et al. dMi-2, a hunchback-interacting protein that functions in polycomb repression. Science 282, 1897-1900 (1998).
126. Ogas, J., Kaufmann, S., Henderson, J. & Somerville, C. PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc. Natl Acad. Sci. USA 96, 13839-13844 (1999).
127. Solari, F. & Ahringer, J. NURD-complex genes antagonise Ras-induced vulval development in Caenorhabditis elegans. Curr. Biol. 10, 223-226 (2000).
128. Wade, P. A., Jones, P. L., Vermaak, D. & Wolffe, A. P. A multiple subunit Mi-2 histone deacetylase from Xenopus laevis cofractionates with an associated Snf2 superfamily ATPase. Curr. Biol. 8, 843-846 (1998).
129. Ahringer, J. NuRD and SIN3 histone deacetylase complexes in development. Trends Genet. 16, 351-356 (2000).
130. von Zelewsky, T. et al. The C. elegans Mi-2 chromatin-remodelling proteins function in vulval cell fate determination. Development 127, 5277-5284 (2000).
131. Unhavaithaya, Y. et al. MEP-1 and a homolog of the NURD complex component Mi-2 act together to maintain germline-soma distinctions in C. elegans. Cell 111, 991-1002 (2002).
132. Shin, T. H. & Mello, C. C. Chromatin regulation during C. elegans germline development. Curr. Opin. Genet. Dev. 13, 455-462 (2003).
133. Hendrich, B., Guy, J., Ramsahoye, B., Wilson, V. A. & Bird, A. Closely related proteins MBD2 and MBD3 play distinctive but interacting roles in mouse development. Genes Dev. 15, 710-723 (2001).
134. Lagger, G. et al. Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. EMBO J. 21, 2672-2681 (2002).