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ATP-dependent chromatin remodeling complexes in Drosophila

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Abstract

The regulation of chromatin structure is of fundamental importance for many DNA-based processes in eukaryotes. Activation or repression of gene transcription or DNA replication depends on enzymes which can generate the appropriate chromatin environment. Several of these enzymes utilize the energy of ATP hydrolysis to alter nucleosome structure. In recent years our understanding of the multisubunit complexes within which they function, their mechanisms of action, their regulation and their in-vivo roles has increased. Much of what we have learned has been gleaned from studies in Drosophila melanogaster. Here we will review what we know about the main classes of ATP-dependent chromatin remodelers in Drosophila.

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References

  • Aasland R, Stewart AF (1995) The chromo shadow domain, a second chromo domain in heterochromatin- binding protein 1, HP1. Nucleic Acids Res 23: 3168–3174.

    PubMed  CAS  Google Scholar 

  • Aasland R, Gibson TJ, Stewart AF (1995) The PHD finger: implications for chromatin-mediated transcriptional regulation. Trends Biochem Sci 20: 56–59.

    PubMed  CAS  Google Scholar 

  • Aasland R, Stewart AF, Gibson T (1996) The SANT domain: a putative DNA-binding domain in the SWI-SNF and ADA complexes, the transcriptional co-repressor N-CoR and TFIIIB. Trends Biochem Sci 21: 87–88.

    PubMed  CAS  Google Scholar 

  • Adamkewicz JI, Hansen KE, Prud'homme WA, Davis JL, Thorner J (2001) High affinity interaction of yeast transcriptional regulator, Mot1, with TATA box-binding protein (TBP). J Biol Chem 276: 11883–11894.

    PubMed  CAS  Google Scholar 

  • Alexiadis V, Lusser A, Kadonaga JT (2004) A conserved N-terminal motif in Rad54 is important for chromatin remodeling and homologous strand pairing. J Biol Chem 279: 27824–27829.

    PubMed  CAS  Google Scholar 

  • Armstrong JA, Papoulas O, Daubresse G, Sperling AS, Lis JT, Scott MP, Tamkun JW (2002) The Drosophila BRM complex facilitates global transcription by RNA polymerase II. EMBO J 21: 5245–5254.

    PubMed  CAS  Google Scholar 

  • Armstrong JA, Sperling AS, Deuring R et al. (2005) Genetic screens for enhancers of brahma reveal functional interactions between the BRM chromatin-remodeling complex and the delta-notch signal transduction pathway in Drosophila. Genetics 170: 1761–1774.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Ballestar E, Pile LA, Wassarman DA, Wolffe AP, Wade PA (2001) A Drosophila MBD family member is a transcriptional corepressor associated with specific genes. Eur J Biochem 268: 5397–5406.

    PubMed  CAS  Google Scholar 

  • Bannister AJ, Zegerman P, Partridge JF et al. (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410: 120–124.

    PubMed  CAS  Google Scholar 

  • Becker PB, Hörz W (2002) ATP-dependent nucleosome remodeling. Annu Rev Biochem 71: 247–273.

    PubMed  CAS  Google Scholar 

  • Beisel C, Imhof A, Greene J, Kremmer E, Sauer F (2002) Histone methylation by the Drosophila epigenetic transcriptional regulator Ash1. Nature 419: 857–862.

    PubMed  CAS  Google Scholar 

  • Boerkoel CF, Takashima H, John J et al. (2002) Mutant chromatin remodeling protein SMARCAL1 causes Schimke immuno-osseous dysplasia. Nat Genet 30: 215–220.

    PubMed  CAS  Google Scholar 

  • Bonaldi T, Langst G, Strohner R, Becker PB, Bianchi ME (2002) The DNA chaperone HMGB1 facilitates ACF/CHRAC-dependent nucleosome sliding. EMBO J 21: 6865–6873.

    PubMed  CAS  Google Scholar 

  • Bork P, Koonin EV (1993) An expanding family of helicases within the ‘DEAD/H’ superfamily. Nucleic Acids Res 21: 751–752.

    PubMed  CAS  Google Scholar 

  • Bouazoune K, Brehm A (2005) dMI-2 chromatin binding and remodeling activities are regulated by dCK2 phosphorylation. J Biol Chem 280: 41912–41920.

    PubMed  CAS  Google Scholar 

  • Bouazoune K, Mitterweger A, Langst G et al. (2002) The dMi-2 chromodomains are DNA binding modules important for ATP- dependent nucleosome mobilization. EMBO J 21: 2430–2440.

    PubMed  CAS  Google Scholar 

  • Bowen NJ, Fujita N, Kajita M, Wade PA (2004) Mi-2/NuRD: multiple complexes for many purposes. Biochim Biophys Acta 1677: 52–57.

    PubMed  CAS  Google Scholar 

  • Brackertz M, Boeke J, Zhang R, Renkawitz R (2002) Two highly related p66 proteins comprise a new family of potent transcriptional repressors interacting with MBD2 and MBD3. J Biol Chem 277: 40958–40966.

    PubMed  CAS  Google Scholar 

  • Brackertz M, Gong Z, Leers J, Renkawitz R (2006) p66alpha and p66beta of the Mi-2/NuRD complex mediate MBD2 and histone interaction. Nucleic Acids Res 34: 397–406.

    PubMed  CAS  Google Scholar 

  • Breeden L, Nasmyth K (1987) Cell cycle control of the yeast HO gene: cis- and trans-acting regulators. Cell 48: 389–397.

    PubMed  CAS  Google Scholar 

  • Brehm A, Langst G, Kehle J et al. (2000) dMi-2 and ISWI chromatin remodelling factors have distinct nucleosome binding and mobilization properties. EMBO J 19: 4332–4341.

    PubMed  CAS  Google Scholar 

  • Cairns BR, Kim YJ, Sayre MH, Laurent BC, Kornberg RD (1994) 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.

    PubMed  CAS  Google Scholar 

  • Cardoso C, Couillault C, Mignon-Ravix C et al. (2005) XNP-1/ATR-X acts with RB, HP1 and the NuRD complex during larval development in C. elegans. Dev Biol 278: 49–59.

    PubMed  CAS  Google Scholar 

  • Cernilogar FM, Orlando V (2005) Epigenome programming by Polycomb and Trithorax proteins. Biochem Cell Biol 83: 322–331.

    PubMed  CAS  Google Scholar 

  • Clapier CR, Langst G, Corona DF, Becker PB, Nightingale KP (2001) Critical role for the histone H4 N terminus in nucleosome remodeling by ISWI. Mol Cell Biol 21: 875–883.

    PubMed  CAS  Google Scholar 

  • Collins RT, Treisman JE (2000) Osa-containing Brahma chromatin remodeling complexes are required for the repression of wingless target genes. Genes Dev 14: 3140–3152.

    PubMed  CAS  Google Scholar 

  • Collins RT, Furukawa T, Tanese N, Treisman JE (1999) Osa associates with the Brahma chromatin remodeling complex and promotes the activation of some target genes. EMBO J 18: 7029–7040.

    PubMed  CAS  Google Scholar 

  • Corona DF, Langst G, Clapier CR et al. (1999) ISWI is an ATP-dependent nucleosome remodeling factor. Mol Cell 3: 239–245.

    PubMed  CAS  Google Scholar 

  • Corona DF, Eberharter A, Budde A et al. (2000) Two histone fold proteins, CHRAC-14 and CHRAC-16, are developmentally regulated subunits of chromatin accessibility complex (CHRAC). EMBO J 19: 3049–3059.

    PubMed  CAS  Google Scholar 

  • Corona DF, Clapier CR, Becker PB, Tamkun JW (2002) Modulation of ISWI function by site-specific histone acetylation. EMBO Rep 3: 242–247.

    PubMed  CAS  Google Scholar 

  • Cote J, Quinn J, Workman JL, Peterson CL (1994) Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex. Science 265: 53–60.

    PubMed  CAS  Google Scholar 

  • Czermin B, Melfi R, McCabe D, Seitz V, Imhof A, Pirrotta V (2002) Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111: 185–196.

    PubMed  CAS  Google Scholar 

  • Daubresse G, Deuring R, Moore L et al. (1999) The Drosophila kismet gene is related to chromatin-remodeling factors and is required for both segmentation and segment identity. Development 126: 1175–1187.

    PubMed  CAS  Google Scholar 

  • de la Cruz X, Lois S, Sanchez-Molina S, Martinez-Balbas MA (2005) Do protein motifs read the histone code? Bioessays 27: 164–175.

    PubMed  Google Scholar 

  • Dejardin J, Cavalli G (2005) Epigenetic inheritance of chromatin states mediated by Polycomb and trithorax group proteins in Drosophila. Prog Mol Subcell Biol 38: 31–63.

    PubMed  CAS  Google Scholar 

  • Delmas V, Stokes DG, Perry RP (1993) A mammalian DNA-binding protein that contains a chromodomain and an SNF2/SWI2-like helicase domain. Proc Natl Acad Sci USA 90: 2414–2418.

    PubMed  CAS  Google Scholar 

  • Deuring R, Fanti L, Armstrong JA et al. (2000) 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.

    PubMed  CAS  Google Scholar 

  • Durr H, Korner C, Muller M, Hickmann V, Hopfner KP (2005) X-ray structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase core and its complex with DNA. Cell 121: 363–373.

    PubMed  Google Scholar 

  • Eberharter A, Becker PB (2004) ATP-dependent nucleosome remodelling: factors and functions. J Cell Sci 117: 3707–3711.

    PubMed  CAS  Google Scholar 

  • Eberharter A, Ferrari S, Langst G et al. (2001) Acf1, the largest subunit of CHRAC, regulates ISWI-induced nucleosome remodelling. EMBO J 20: 3781–3788.

    PubMed  CAS  Google Scholar 

  • Eberharter A, Vetter I, Ferreira R, Becker PB (2004) ACF1 improves the effectiveness of nucleosome mobilization by ISWI through PHD-histone contacts. EMBO J 23: 4029–4039.

    PubMed  CAS  Google Scholar 

  • Eisen JA, Sweder KS, Hanawalt PC (1995) Evolution of the SNF2 family of proteins: subfamilies with distinct sequences and functions. Nucleic Acids Res 23: 2715–2723.

    PubMed  CAS  Google Scholar 

  • Eissenberg JC, Wong M, Chrivia JC (2005) Human SRCAP and Drosophila melanogaster DOM are homologs that function in the notch signaling pathway. Mol Cell Biol 25: 6559–6569.

    PubMed  CAS  Google Scholar 

  • Ekwall K (2005) Genome-wide analysis of HDAC function. Trends Genet 21: 608–615.

    PubMed  CAS  Google Scholar 

  • Elfring LK, Daniel C, Papoulas O et al. (1998) Genetic analysis of brahma: the Drosophila homolog of the yeast chromatin remodeling factor SWI2. Genetics 148: 251–265.

    PubMed  CAS  Google Scholar 

  • Feng Q, Zhang Y (2001) The MeCP1 complex represses transcription through preferential binding, remodeling, and deacetylating methylated nucleosomes. Genes Dev 15: 827–832.

    PubMed  CAS  Google Scholar 

  • Feng Q, Cao R, Xia L, Erdjument-Bromage H, Tempst P, Zhang Y (2002) Identification and functional characterization of the p66/p68 components of the MeCP1 complex. Mol Cell Biol 22: 536–546.

    PubMed  CAS  Google Scholar 

  • Fischle W, Wang Y, Jacobs SA, Kim Y, Allis CD, Khorasanizadeh S (2003) Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev 17: 1870–1881.

    PubMed  CAS  Google Scholar 

  • Flanagan JF, Mi LZ, Chruszcz M et al. (2005) Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature 438: 1181–1185.

    PubMed  CAS  Google Scholar 

  • Fujita N, Jaye DL, Kajita M, Geigerman C, Moreno CS, Wade PA (2003) MTA3, a Mi-2/NuRD complex subunit, regulates an invasive growth pathway in breast cancer. Cell 113: 207–219.

    PubMed  CAS  Google Scholar 

  • Fujita N, Jaye DL, Geigerman C et al. (2004) MTA3 and the Mi-2/NuRD complex regulate cell fate during B lymphocyte differentiation. Cell 119: 75–86.

    PubMed  CAS  Google Scholar 

  • Fyodorov DV, Kadonaga JT (2002a) Binding of Acf1 to DNA involves a WAC motif and is important for ACF-mediated chromatin assembly. Mol Cell Biol 22: 6344–6353.

    PubMed  CAS  Google Scholar 

  • Fyodorov DV, Kadonaga JT (2002b) Dynamics of ATP-dependent chromatin assembly by ACF. Nature 418: 897–900.

    PubMed  CAS  Google Scholar 

  • Fyodorov DV, Blower MD, Karpen GH, Kadonaga JT (2004) Acf1 confers unique activities to ACF/CHRAC and promotes the formation rather than disruption of chromatin in vivo. Genes Dev 18: 170–183.

    PubMed  CAS  Google Scholar 

  • Girdham CH, Glover DM (1991) Chromosome tangling and breakage at anaphase result from mutations in lodestar, a Drosophila gene encoding a putative nucleoside triphosphate-binding protein. Genes Dev 5: 1786–1799.

    PubMed  CAS  Google Scholar 

  • Go MJ, Artavanis-Tsakonas S (1998) A genetic screen for novel components of the notch signaling pathway during Drosophila bristle development. Genetics 150: 211–220.

    PubMed  CAS  Google Scholar 

  • Goldman-Levi R, Miller C, Bogoch J, Zak NB (1996) Expanding the Mot1 subfamily: 89B helicase encodes a new Drosophila melanogaster SNF2-related protein which binds to multiple sites on polytene chromosomes. Nucleic Acids Res 24: 3121–3128.

    PubMed  CAS  Google Scholar 

  • Gorbalenya AE, Koonin EV, Donchenko AP, Blinov VM (1989) Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Res 17: 4713–4730.

    PubMed  CAS  Google Scholar 

  • Grune T, Brzeski J, Eberharter A, Clapier CR, Corona DF, Becker PB, Muller CW (2003) Crystal structure and functional analysis of a nucleosome recognition module of the remodeling factor ISWI. Mol Cell 12: 449–460.

    PubMed  Google Scholar 

  • Hamiche A, Kang JG, Dennis C, Xiao H, Wu C (2001) Histone tails modulate nucleosome mobility and regulate ATP-dependent nucleosome sliding by NURF. Proc Natl Acad Sci USA 98: 14316–14321.

    PubMed  CAS  Google Scholar 

  • Hartlepp KF, Fernandez-Tornero C, Eberharter A, Grune T, Muller CW, Becker PB (2005) The histone fold subunits of Drosophila CHRAC facilitate nucleosome sliding through dynamic DNA interactions. Mol Cell Biol 25: 9886–9896.

    PubMed  CAS  Google Scholar 

  • Hassan AH, Prochasson P, Neely KE et al. (2002) Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes. Cell 111: 369–379.

    PubMed  CAS  Google Scholar 

  • Haynes SR, Dollard C, Winston F, Beck S, Trowsdale J, Dawid IB (1992) The bromodomain: a conserved sequence found in human, Drosophila and yeast proteins. Nucleic Acids Res 20: 2603.

    PubMed  CAS  Google Scholar 

  • Heitzler P, Vanolst L, Biryukova I, Ramain P (2003) Enhancer-promoter communication mediated by Chip during Pannier-driven proneural patterning is regulated by Osa. Genes Dev 17: 591–596.

    PubMed  CAS  Google Scholar 

  • Hirose F, Ohshima N, Shiraki M et al. (2001) Ectopic expression of DREF induces DNA synthesis, apoptosis, and unusual morphogenesis in the Drosophila eye imaginal disc: possible interaction with Polycomb and trithorax group proteins. Mol Cell Biol 21: 7231–7242.

    PubMed  CAS  Google Scholar 

  • Hirose F, Ohshima N, Kwon EJ, Yoshida H, Yamaguchi M (2002) Drosophila Mi-2 negatively regulates dDREF by inhibiting its DNA-binding activity. Mol Cell Biol 22: 5182–5193.

    PubMed  CAS  Google Scholar 

  • Hirschhorn JN, Brown SA, Clark CD, Winston F (1992) Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. Genes Dev 6: 2288–2298.

    PubMed  CAS  Google Scholar 

  • Imbalzano AN, Xiao H (2004) Functional properties of ATP-dependent chromatin remodeling enzymes. Adv Protein Chem 67: 157–179.

    PubMed  CAS  Google Scholar 

  • Ito T, Bulger M, Pazin MJ, Kobayashi R, Kadonaga JT (1997) ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 90: 145–155.

    PubMed  CAS  Google Scholar 

  • Ito T, Levenstein ME, Fyodorov DV, Kutach AK, Kobayashi R, Kadonaga JT (1999) ACF consists of two subunits, Acf1 and ISWI, that function cooperatively in the ATP-dependent catalysis of chromatin assembly. Genes Dev 13: 1529–1539.

    PubMed  CAS  Google Scholar 

  • Kal AJ, Mahmoudi T, Zak NB, Verrijzer CP (2000) The Drosophila brahma complex is an essential coactivator for the trithorax group protein zeste. Genes Dev 14: 1058–1071.

    PubMed  CAS  Google Scholar 

  • Kang JG, Hamiche A, Wu C (2002) GAL4 directs nucleosome sliding induced by NURF. EMBO J 21: 1406–1413.

    PubMed  CAS  Google Scholar 

  • Kehle J, Beuchle D, Treuheit S et al. (1998) dMi-2, a hunchback-interacting protein that functions in polycomb repression. Science 282: 1897–1900.

    PubMed  CAS  Google Scholar 

  • Kelley DE, Stokes DG, Perry RP (1999) CHD1 interacts with SSRP1 and depends on both its chromodomain and its ATPase/helicase-like domain for proper association with chromatin. Chromosoma 108: 10–25.

    PubMed  CAS  Google Scholar 

  • Kennison JA, Tamkun JW (1988) Dosage-dependent modifiers of polycomb and antennapedia mutations in Drosophila. Proc Natl Acad Sci USA 85: 8136–8140.

    PubMed  CAS  Google Scholar 

  • Kon C, Cadigan KM, da Silva SL, Nusse R (2005) Developmental roles of the Mi-2/NURD-associated protein p66 in Drosophila. Genetics 169: 2087–2100.

    PubMed  CAS  Google Scholar 

  • Korenjak M, Taylor-Harding B, Binne UK et al. (2004) Native E2F/RBF complexes contain Myb-interacting proteins and repress transcription of developmentally controlled E2F target genes. Cell 119: 181–193.

    PubMed  CAS  Google Scholar 

  • Kruger W, Peterson CL, Sil A et al. (1995) 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.

    PubMed  CAS  Google Scholar 

  • Kukimoto I, Elderkin S, Grimaldi M, Oelgeschlager T, Varga-Weisz PD (2004) The histone-fold protein complex CHRAC-15/17 enhances nucleosome sliding and assembly mediated by ACF. Mol Cell 13: 265–277.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Laherty CD, Yang WM, Sun JM, Davie JR, Seto E, Eisenman RN (1997) Histone deacetylases associated with the mSin3 corepressor mediate mad transcriptional repression. Cell 89: 349–356.

    PubMed  CAS  Google Scholar 

  • Langst G, Becker PB (2001) ISWI induces nucleosome sliding on nicked DNA. Mol Cell 8: 1085–1092.

    PubMed  CAS  Google Scholar 

  • Langst G, Becker PB (2004) Nucleosome remodeling: one mechanism, many phenomena? Biochim Biophys Acta 1677: 58–63.

    PubMed  CAS  Google Scholar 

  • Laurent BC, Treich I, Carlson M (1993) The yeast SNF2/SWI2 protein has DNA-stimulated ATPase activity required for transcriptional activation. Genes Dev 7: 583–591.

    PubMed  CAS  Google Scholar 

  • Lewis PW, Beall EL, Fleischer TC, Georlette D, Link AJ, Botchan MR (2004) Identification of a Drosophila Myb-E2F2/RBF transcriptional repressor complex. Genes Dev 18: 2929–2940.

    PubMed  CAS  Google Scholar 

  • Lusser A, Urwin DL, Kadonaga JT (2005) Distinct activities of CHD1 and ACF in ATP-dependent chromatin assembly. Nat Struct Mol Biol 12: 160–166.

    PubMed  CAS  Google Scholar 

  • Marenda DR, Zraly CB, Feng Y, Egan S, Dingwall AK (2003) The Drosophila SNR1 (SNF5/INI1) subunit directs essential developmental functions of the Brahma chromatin remodeling complex. Mol Cell Biol 23: 289–305.

    PubMed  CAS  Google Scholar 

  • Marenda DR, Zraly CB, Dingwall AK (2004) The Drosophila Brahma (SWI/SNF) chromatin remodeling complex exhibits cell-type specific activation and repression functions. Dev Biol 267: 279–293.

    PubMed  CAS  Google Scholar 

  • Marhold J, Brehm A, Kramer K (2004a) The Drosophila methyl-DNA binding protein MBD2/3 interacts with the NuRD complex via p55 and MI-2. BMC Mol Biol 5: 20.

    PubMed  Google Scholar 

  • Marhold J, Kramer K, Kremmer E, Lyko F (2004b) The Drosophila MBD2/3 protein mediates interactions between the MI-2 chromatin complex and CpT/A-methylated DNA. Development 131: 6033–6039.

    PubMed  CAS  Google Scholar 

  • Martinez-Balbas MA, Tsukiyama T, Gdula D, Wu C (1998) Drosophila NURF-55, a WD repeat protein involved in histone metabolism. Proc Natl Acad Sci USA 95: 132–137.

    PubMed  CAS  Google Scholar 

  • Metivier R, Reid G, Gannon F (2006) Transcription in four dimensions: nuclear receptor-directed initiation of gene expression. EMBO Rep 7: 161–167.

    PubMed  CAS  Google Scholar 

  • Milan M, Pham TT, Cohen SM (2004) Osa modulates the expression of Apterous target genes in the Drosophila wing. Mech Dev 121: 491–497.

    PubMed  CAS  Google Scholar 

  • Mizuguchi G, Tsukiyama T, Wisniewski J, Wu C (1997) Role of nucleosome remodeling factor NURF in transcriptional activation of chromatin. Mol Cell 1: 141–150.

    PubMed  CAS  Google Scholar 

  • Mizuguchi G, Vassilev A, Tsukiyama T, Nakatani Y, Wu C (2001) ATP-dependent nucleosome remodeling and histone hyperacetylation synergistically facilitate transcription of chromatin. J Biol Chem 276: 14773–14783.

    PubMed  CAS  Google Scholar 

  • Mohrmann L, Verrijzer CP (2005) Composition and functional specificity of SWI2/SNF2 class chromatin remodeling complexes. Biochim Biophys Acta 1681: 59–73.

    PubMed  CAS  Google Scholar 

  • Mohrmann L, Langenberg K, Krijgsveld J, Kal AJ, Heck AJ, Verrijzer CP (2004) Differential targeting of two distinct SWI/SNF-related Drosophila chromatin-remodeling complexes. Mol Cell Biol 24: 3077–3088.

    PubMed  CAS  Google Scholar 

  • Moller A, Avila FW, Erickson JW, Jackle H (2005) Drosophila BAP60 is an essential component of the Brahma complex, required for gene activation and repression. J Mol Biol 352: 329–337.

    PubMed  Google Scholar 

  • Moshkin YM, Armstrong JA, Maeda RK et al. (2002) Histone chaperone ASF1 cooperates with the Brahma chromatin-remodelling machinery. Genes Dev 16: 2621–2626.

    PubMed  CAS  Google Scholar 

  • Muller J, Hart CM, Francis NJ et al. (2002) Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111: 197–208.

    PubMed  CAS  Google Scholar 

  • Murawsky CM, Brehm A, Badenhorst P, Lowe N, Becker PB, Travers AA (2001) Tramtrack69 interacts with the dMi-2 subunit of the Drosophila NuRD chromatin remodelling complex. EMBO Rep 2: 1089–1094.

    PubMed  CAS  Google Scholar 

  • Neigeborn L, Carlson M (1984) Genes affecting the regulation of SUC2 gene expression by glucose repression in Saccharomyces cerevisiae. Genetics 108: 845–858.

    PubMed  CAS  Google Scholar 

  • Orphanides G, LeRoy G, Chang CH, Luse DS, Reinberg D (1998) FACT, a factor that facilitates transcript elongation through nucleosomes. Cell 92: 105–116.

    PubMed  CAS  Google Scholar 

  • Orphanides G, Wu WH, Lane WS, Hampsey M, Reinberg D (1999) The chromatin-specific transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins. Nature 400: 284–288.

    PubMed  CAS  Google Scholar 

  • Papoulas O, Beek SJ, Moseley SL et al. (1998) The Drosophila trithorax group proteins BRM, ASH1 and ASH2 are subunits of distinct protein complexes. Development 125: 3955–3966.

    PubMed  CAS  Google Scholar 

  • Paro R, Hogness DS (1991) The Polycomb protein shares a homologous domain with a heterochromatin- associated protein of Drosophila. Proc Natl Acad Sci USA 88: 263–267.

    PubMed  CAS  Google Scholar 

  • Peterson CL, Herskowitz I (1992) Characterization of the yeast SWI1, SWI2, and SWI3 genes, which encode a global activator of transcription. Cell 68: 573–583.

    PubMed  CAS  Google Scholar 

  • Pray-Grant MG, Daniel JA, Schieltz D, Yates JR 3rd, Grant PA (2005) Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation. Nature 433: 434–438.

    PubMed  CAS  Google Scholar 

  • Prelich G, Winston F (1993) Mutations that suppress the deletion of an upstream activating sequence in yeast: involvement of a protein kinase and histone H3 in repressing transcription in vivo. Genetics 135: 665–676.

    PubMed  CAS  Google Scholar 

  • Qian YW, Wang YC, Hollingsworth RE Jr, Jones D, Ling N, Lee EY (1993) A retinoblastoma-binding protein related to a negative regulator of Ras in yeast. Nature 364: 648–652.

    PubMed  CAS  Google Scholar 

  • Rea S, Eisenhaber F, O’Carroll D et al. (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406: 593–599.

    PubMed  CAS  Google Scholar 

  • Reddy BA, Etkin LD (1991) A unique bipartite cysteine-histidine motif defines a subfamily of potential zinc-finger proteins. Nucleic Acids Res 19: 6330.

    PubMed  CAS  Google Scholar 

  • Romeijn RJ, Gorski MM, van Schie MA et al. (2005) Lig4 and rad54 are required for repair of DNA double-strand breaks induced by P-element excision in Drosophila. Genetics 169: 795–806.

    PubMed  CAS  Google Scholar 

  • Schwanbeck R, Xiao H, Wu C (2004) Spatial contacts and nucleosome step movements induced by the NURF chromatin remodeling complex. J Biol Chem 279: 39933–39941.

    PubMed  CAS  Google Scholar 

  • Seelig HP, Moosbrugger I, Ehrfeld H, Fink T, Renz M, Genth E (1995) The major dermatomyositis-specific Mi-2 autoantigen is a presumed helicase involved in transcriptional activation. Arthritis Rheum 38: 1389–1399.

    PubMed  CAS  Google Scholar 

  • Seto ES, Bellen HJ (2004) The ins and outs of Wingless signaling. Trends Cell Biol 14: 45–53.

    PubMed  CAS  Google Scholar 

  • Sims RJ 3rd, Chen CF, Santos-Rosa H, Kouzarides T, Patel SS, Reinberg D (2005) 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.

    PubMed  CAS  Google Scholar 

  • Smith S, Stillman B (1989) Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell 58: 15–25.

    PubMed  CAS  Google Scholar 

  • Smith CL, Horowitz-Scherer R, Flanagan JF, Woodcock CL, Peterson CL (2003) Structural analysis of the yeast SWI/SNF chromatin remodeling complex. Nat Struct Biol 10: 141–145.

    PubMed  CAS  Google Scholar 

  • Srinivasan S, Armstrong JA, Deuring R, Dahlsveen IK, McNeill H, Tamkun JW (2005) The Drosophila trithorax group protein Kismet facilitates an early step in transcriptional elongation by RNA Polymerase II. Development 132: 1623–1635.

    PubMed  CAS  Google Scholar 

  • Stern M, Jensen R, Herskowitz I (1984) Five SWI genes are required for expression of the HO gene in yeast. J Mol Biol 178: 853–868.

    PubMed  CAS  Google Scholar 

  • Stokes DG, Tartof KD, Perry RP (1996) CHD1 is concentrated in interbands and puffed regions of Drosophila polytene chromosomes. Proc Natl Acad Sci USA 93: 7137–7142.

    PubMed  CAS  Google Scholar 

  • Straub T, Dahlsveen IK, Becker PB (2005) Dosage compensation in flies: mechanism, models, mystery. FEBS Lett 579: 3258–3263.

    PubMed  CAS  Google Scholar 

  • Strohner R, Wachsmuth M, Dachauer K et al. (2005) A ‘loop recapture’ mechanism for ACF-dependent nucleosome remodeling. Nat Struct Mol Biol 12: 683–690.

    PubMed  CAS  Google Scholar 

  • Tamkun JW, Deuring R, Scott MP et al. (1992) brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68: 561–572.

    PubMed  CAS  Google Scholar 

  • Therrien M, Morrison DK, Wong AM, Rubin GM (2000) A genetic screen for modifiers of a kinase suppressor of Ras-dependent rough eye phenotype in Drosophila. Genetics 156: 1231–1242.

    PubMed  CAS  Google Scholar 

  • Thoma NH, Czyzewski BK, Alexeev AA, Mazin AV, Kowalczykowski SC, Pavletich NP (2005) Structure of the SWI2/SNF2 chromatin-remodeling domain of eukaryotic Rad54. Nat Struct Mol Biol 12: 350–356.

    PubMed  Google Scholar 

  • Tong JK, Hassig CA, Schnitzler GR, Kingston RE, Schreiber SL (1998) Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex. Nature 395: 917–921.

    PubMed  CAS  Google Scholar 

  • Tsukiyama T, Wu C (1995) ISWI, a member of the SWI2/SNF2 ATPase family, encodes the 140 kDa subunit of the nucleosome remodeling factor. Cell 83: 1011–1020.

    PubMed  CAS  Google Scholar 

  • Tsukiyama T, Daniel C, Tamkun J, Wu C (1995) Purification and properties of an ATP-dependent nucleosome remodeling factor. Cell 83: 1021–1026.

    PubMed  CAS  Google Scholar 

  • Varga-Weisz PD, Wilm M, Bonte E, Dumas K, Mann M, Becker PB (1997) Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II. Nature 388: 598–602.

    PubMed  CAS  Google Scholar 

  • Verheyen EM, Purcell KJ, Fortini ME, Artavanis-Tsakonas S (1996) Analysis of dominant enhancers and suppressors of activated Notch in Drosophila. Genetics 144: 1127–1141.

    PubMed  CAS  Google Scholar 

  • Verreault A, Kaufman PD, Kobayashi R, Stillman B (1998) Nucleosomal DNA regulates the core-histone-binding subunit of the human Hat1 acetyltransferase. Curr Biol 8: 96–108.

    PubMed  CAS  Google Scholar 

  • Wade PA, Jones PL, Vermaak D, Wolffe AP (1998) A multiple subunit Mi-2 histone deacetylase from Xenopus laevis cofractionates with an associated Snf2 superfamily ATPase. Curr Biol 8: 843–846.

    PubMed  CAS  Google Scholar 

  • Wade PA, Gegonne A, Jones PL, Ballestar E, Aubry F, Wolffe AP (1999) Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation. Nat Genet 23: 62–66.

    PubMed  CAS  Google Scholar 

  • Woodage T, Basrai MA, Baxevanis AD, Hieter P, Collins FS (1997) Characterization of the CHD family of proteins. Proc Natl Acad Sci USA 94: 11472–11477.

    PubMed  CAS  Google Scholar 

  • Xi R, Xie T (2005) Stem cell self-renewal controlled by chromatin remodeling factors. Science 310: 1487–1489.

    PubMed  CAS  Google Scholar 

  • Xiao H, Sandaltzopoulos R, Wang HM et al. (2001) Dual functions of largest NURF subunit NURF301 in nucleosome sliding and transcription factor interactions. Mol Cell 8: 531–543.

    PubMed  CAS  Google Scholar 

  • Xue Y, Wong J, Moreno GT, Young MK, Cote J, Wang W (1998) NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol Cell 2: 851–861.

    PubMed  CAS  Google Scholar 

  • Yagi Y, Ip YT (2005) Helicase89B is a Mot1p/BTAF1 homologue that mediates an antimicrobial response in Drosophila. EMBO Rep 6: 1088–1094.

    PubMed  CAS  Google Scholar 

  • Zhang Y, Iratni R, Erdjument-Bromage H, Tempst P, Reinberg D (1997) Histone deacetylases and SAP18, a novel polypeptide, are components of a human Sin3 complex. Cell 89: 357–364.

    PubMed  CAS  Google Scholar 

  • Zhang Y, LeRoy G, Seelig HP, Lane WS, Reinberg D (1998) The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities. Cell 95: 279–289.

    PubMed  CAS  Google Scholar 

  • Zraly CB, Marenda DR, Dingwall AK (2004) SNR1 (INI1/SNF5) mediates important cell growth functions of the Drosophila Brahma (SWI/SNF) chromatin remodeling complex. Genetics 168: 199–214.

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Massachusetts General Hospital, Department of Molecular Biology, Harvard Medical School, Department of Genetics, 185 Cambridge Street, Boston, MA, 02114, USA

    Karim Bouazoune

  2. Institut für Molekularbiologie und Tumorforschung, Philipps-Universität Marburg, Emil-Mannkopff-Str.2, 35055, Marburg, Germany

    Alexander Brehm

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  1. Karim Bouazoune
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  2. Alexander Brehm
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Correspondence to Alexander Brehm.

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Bouazoune, K., Brehm, A. ATP-dependent chromatin remodeling complexes in Drosophila. Chromosome Res 14, 433–449 (2006). https://doi.org/10.1007/s10577-006-1067-0

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