Site-specific acetylation of ISWI by GCN5
© Ferreira et al; licensee BioMed Central Ltd. 2007
Received: 10 April 2007
Accepted: 30 August 2007
Published: 30 August 2007
The tight organisation of eukaryotic genomes as chromatin hinders the interaction of many DNA-binding regulators. The local accessibility of DNA is regulated by many chromatin modifying enzymes, among them the nucleosome remodelling factors. These enzymes couple the hydrolysis of ATP to disruption of histone-DNA interactions, which may lead to partial or complete disassembly of nucleosomes or their sliding on DNA. The diversity of nucleosome remodelling factors is reflected by a multitude of ATPase complexes with distinct subunit composition.
We found further diversification of remodelling factors by posttranslational modification. The histone acetyltransferase GCN5 can acetylate the Drosophila remodelling ATPase ISWI at a single, conserved lysine, K753, in vivo and in vitro. The target sequence is strikingly similar to the N-terminus of histone H3, where the corresponding lysine, H3K14, can also be acetylated by GCN5. The acetylated form of ISWI represents a minor species presumably associated with the nucleosome remodelling factor NURF.
Acetylation of histone H3 and ISWI by GCN5 is explained by the sequence similarity between the histone and ISWI around the acetylation site. The common motif RKT/SxGx(Kac)xPR/K differs from the previously suggested GCN5/PCAF recognition motif GKxxP. This raises the possibility of co-regulation of a nucleosome remodelling factor and its nucleosome substrate through acetylation of related epitopes and suggests a direct crosstalk between two distinct nucleosome modification principles.
Disruption of DNA-histone interactions by nucleosome remodelling ATPases may lead to a variety of transitions of chromatin structure, such as the partial or complete disassembly of nucleosomes, the exchange of histones, or the sliding of intact histone octamers on DNA [1–4]. In many cases their activity is focused on local disruption of the nucleosomal fibre through recruitment of DNA-binding regulators to promote access of factors further downstream in the cascade of events that leads to promoter opening . However, genome-wide processes like replication, DNA damage responses or homologous recombination require chromatin to be dynamic on a global scale. In addition to generating local access to nucleosomal DNA, nucleosome disruption may also have profound consequences for the folding of the nucleosomal fibre into higher order structures [5, 6].
One largely unresolved issue to date is how the activity of chromatin remodelling enzymes is regulated. Established regulatory principles that govern, for example, metabolic enzymes also apply to nucleosome remodelling ATPases, but our knowledge is still anecdotal. The expression of nucleosome remodelling ATPases may be selective. For example, the fact that the mammalian ISWI isoform SNF2H is abundant in proliferating cells, whereas the related SNF2L is enriched in terminally differentiated neurons points to functional diversification of related remodelling enzymes and specialized roles in proliferation/differentiation control . Such a role has also been suggested for the SWI2/SNF2-type ATPase hBRM by the early finding that its expression is down-regulated when cells receive a mitogenic stimulus or during ras-mediated oncogenic transformation, whereas its forced expression partially reverses transformation .
A further regulatory strategy involves post-translational modifications of enzymes, such as their phosphorylation. Phosphorylation of hBRM and BRG-1 during mitosis correlates with dissociation of these remodellers from the chromosomes during condensation . Muchardt and colleagues also showed that acetylation of hBRM correlates with a reduced inhibition of cell growth . The possibility of regulating nucleosome remodelling ATPases by lysine acetylation is intriguing given that properties of their substrates, the histones, are most prominently modulated by acetylation at their exposed N-termini .
Here we describe another example of potential regulation of a remodelling ATPase by acetylation. We found that Drosophila ISWI, the founding member of a family of nucleosome remodelling ATPases, was preferentially acetylated by GCN5 at a single lysine within a amino acid sequence of high similarity to the N-terminus of histone H3. This acetylated lysine corresponds to lysine 14 in histone H3 (H3K14), a known target for GCN5, suggesting that this acetyltransferase may affect the chromatin structure by two distinct strategies: by acetylation of the nucleosomes and by modification of a nucleosome remodelling enzyme.
ISWI is acetylated in vivo
Histone acetyltransferases with substrate preference for the histone H3 N-terminus acetylate ISWI in vitro
GCN5 acetylates ISWI at lysine 753
A peptide corresponding to aa 1–19 of histone H3 is acetylated rather well by GCN5 and p300 in a standard HAT reaction, but less by MOF (Figure 4B, left panel). By direct comparison, a peptide spanning the corresponding 19 aa of ISWI (Figure 4A) is well acetylated by GCN5, but not at all by MOF (Figure 4B, right panel). Maldi-TOF mass spectrometry and nano-electrospray sequencing documented that the peptide was mono-acetylated (Figure 4C) exclusively at K753 (Figure 4D). In order to test for the contribution of K753 to ISWI acetylation in the context of the entire protein we expressed recombinant ISWI derivatives that had either K748 or K753 or both lysines replaced by alanines (A) or arginines (R). Equivalent protein amounts (Figure 4E, lower panel) were used as substrate for GCN5-dependent acetylation reactions. The ISWI derivative bearing the K748A mutation was acetylated as the wildtype protein, whereas replacement of lysine 753 by alanine (K753A) led to a significantly reduced acetylation (Figure 4E, compare lanes 4, 5). Collectively the data identify K753 of ISWI, which appears related by sequence context to H3K14, as the major target of acetylation by GCN5 in vitro.
We were not able to evaluate the effect of acetylation on ISWI ATPase activity due to the small fraction of ISWI modified in these in vitro reactions. However, replacement of either lysine 753 or lysine 748 (which corresponds to lysine 9 in H3) by arginine or alanine did not affect the ATPase activity in response to DNA or nucleosomes (Figure 4F).
ISWI is acetylated at K753 by GCN5 in vivo
Acetylated ISWI may reside in the NURF complex, but not in CHRAC/ACF
So far ISWI is known to reside in two kinds of nucleosome remodelling complexes in Drosophila: CHRAC/ACF, which are characterised by the ACF1 subunit, and NURF, which contains NURF301 as a defining feature . In order to explore whether ISWIK753ac was preferentially associated with one of these complexes we ablated the signature subunits ACF1 and NURF301 by RNA interference in SL2 cells (Figure 6A) and found that the ISWIK753ac epitope was significantly reduced in the absence of NURF301, but remained unperturbed if ACF1 was knocked down (Figure 6B). In agreement with the notion that ISWIK753ac is not a subunit of CHRAC/ACF we found that the expression pattern of the acetylated ISWI form was unperturbed in acf1 null flies (data not shown). ISWIK753ac staining was unperturbed in flies heterozygous for the NURF301 allele [E(bx)ry122] . Homozygous mutants are lethal, but survive until the end of the larval stage due to maternal contribution of NURF301 and were not analysed. Immunoprecipitation of NURF301 from extracts of SL2 cells and 8–12 hr embryos co-precipitated acetylated ISWI, which was not the case if ACF1 was precipitated (Figure 6C, D). We conclude that in SL2 cells ISWI may be acetylated in the context of NURF but is not acetylated in association with ACF1. The data do not exclude the existence of additional complexes harbouring the modification.
Many acetyltransferases were first identified following their histone acetylation function and hence named histone acetyltransferases (HATs). However, most of them have now been shown to acetylate non-histone proteins as well, and these modifications can have profound effects on the structure and function . For example, the effects of acetylation on the tumour suppressor protein p53 have been heavily studied . The current work, together with the earlier observation that the effect of the BRM ATPase on cell proliferation can be regulated by acetylation  highlight the potential for direct regulatory cross-talk between different chromatin modifying principles .
The fact that ISWI can be acetylated in vitro and in tissue culture cells by GCN5, which is also known to target the H3 N-terminus, is explained by the sequence similarity between the histone and ISWI around the K753 acetylation site. The common motif RKT/SxGx(Kac)xPR/K differs from the previously suggested GCN5/PCAF recognition motif GKxxP . This raises the possibility of specific co-regulation of a nucleosome remodelling factor and its nucleosome substrate through acetylation of related epitopes. Strikingly, the related motif DK GKG KK RP also occurs in the C-terminus of hBRM, overlapping with potential acetylation sites . Acetylation at one or more C-terminal lysines of BRM correlates with reduced interference with cell cycle progression in mammalian cells and mutation of several of these lysines into arginines impairs BRM function. The data suggest that site-specific acetylation of the ATPase by, for example P/CAF, may adversely affect its function, possibly by interfering with targeting interactions .
The fact that the acetylated ISWI epitope is conserved during evolution suggests functional significance. However, so far we were unable to document an effect of acetylation on the catalytic properties or protein interactions of ISWI, due to the small proportion of ISWI either acetylated in vitro or naturally present in vivo. Lysine 753 of ISWI resides in the HAND domain, a fold of unknown function situated between the ATPase domain and the C-terminal SANT/SLIDE domains that mediate nucleosome interactions . Exploring the role of the HAND domain in ISWI may lead to novel approaches towards evaluating the impact of K753 acetylation. Applying the K753ac-specific antibody to developmental stages of Drosophila revealed that the acetylation of ISWI is a developmentally regulated process, which occurs during oogenesis and early embryogenesis, but is absent from later developmental stages (CC and PBB, unpublished observations). We also obtained preliminary support for the idea that the acetylation of ISWI marks a functionally distinct subpopulation: the acetylated epitope was dramatically enriched on the condensed metaphase chromosomes in early embryos (CC and PBB, unpublished observations). A causal role between the acetylation and the unusual ability of the ATPase to interact with compact chromatin remains to be explored.
The ATPase ISWI is the catalytic moiety of several nucleosome remodelling complexes. Better known and characterized are the factors CHRAC, ACF and NURF (for review, see . The available data suggest that the acetylated form of ISWI may mark a subpopulation of the NURF complex. NURF is involved in the transcription of selected sets of Drosophila genes [18, 23] but flies mutant for the large, defining NURF301 subunit also show defects of chromosome structure . Assessment of which of these functions may be modulated by ISWI acetylation requires a genetic approach.
The acetylation of the amino terminus of histone H3 is an important determinant of active chromatin, but chromatin structure can also be modulated by other modifications of the histone 'tail', notable its methylation or phosphorylation. Whether the analogy between the ISWI and the H3 N-terminus can also be extended to include phosphorylation and methylation remains an interesting aspect for future research.
We identified and characterised a site-specific acetylation of the remodelling ATPase ISWI by GCN5. The modification occurs predominantly in the context of the remodelling factor NURF, however, due to the fact that the acetylation marks a minor subpopulation of the remodeller a functional evaluation of the modification has not yet been achieved.
Recombinant DNA technology
pGEX-4T-3 and pProEx-Htb vectors for expression of GST-ISWI and (His6)-ISWI deletion mutants, respectively have been described earlier [15, 16]. pFastBacHTa-FLAG-ISWI WT was generated by inserting the NcoI-KpnI fragment from pMYB4-FLAG-ISWI WT  into pFastBacHTa vector ("Bac-to-Bac" expression system, Invitrogen). pMYB4-FLAG-ISWIK748A, -ISWIK753A, -ISWIKK748/753AA and -ISWIKK748/753RR were generated using the QuickChange site-directed mutagenesis kit (Stratagene) with primers listed in the supplemental materials and moved as NcoI-KpnI fragments into the pFastBacHTa vector.
Primers used for site-directed mutagenesis
Generation of ISWIK748A:
Generation of ISWIK753A:
Generation of ISWIK748R:
Generation of ISWIK753R
Primers used for PCR to generate dsRNA fragments for RNA interference
ISWI sequences 1–499:
GCN5 sequences 1–525:
ACF1 sequences 1–560
NURF301 sequences 1–521
GST sequences 1–527;
The following antibodies were kind gifts: αISWI (J. Tamkun, UC St. Cruz), αp55 (C. Wu, NIH, Bethesda), αGCN5 (Jerry Workman, Stowers Institute for Medical Research) αNURF301 (Andreas Hochheimer). The monoclonal αACF1 antibody was raised in rats. Its specificity was confirmed using the acf1 null fly strain  (C. Chioda et al, manuscript in preparation). We employed two different pan-acetyl-lysine antibodies for immunoprecipitation  and Western blotting (Cell Signalling Technology # 9441). The αISWIK753ac was raised against ISWI peptide TVGYKacVPKNT (aa 749–758) where K753 was acetylated. The antibody is available from Abcam (ab10748). As control antibody we used rabbit IgG (sc-2027, Santa Cruz Biotechnology). The αH3S10p antibody was from Upstate (RR002, catalog # 05–598).
Cell culture, RNA interference and immunostaining
Drosophila SF4 cells (an SL2 clone sorted for diploidy and adherence) were provided by D. Arndt-Jovin (Göttingen). SF4, Kc and SL2 cells were maintained at 26°C in Schneider's Drosophila medium (Invitrogen) supplemented with 10% fetal calf serum (FCS), antibiotics and glutamine. When needed, trichostatine A (TSA) was added at a final concentration of 200 ng/ml to the medium for 17 hrs before harvesting the cells. RNAi experiments were performed as described . The primers used to generate the double-stranded RNA are listed in the supplemental materials. Briefly, 1–2 × 106 SL2 cells were seeded into 6-wells plates in 1 ml of medium without FCS just before adding 10 μg of dsRNA. Plates were then placed onto a shaking platform for 10 min and then for 50 min at 26°C. 2 ml of medium complemented with FCS were then added to the cells and incubated at 26°C. Cells were collected 10 or 12 days after dsRNA treatment. Protein extractions for Western blot analysis after RNAi, 1–2 × 106 cells were pelleted and lysed in 50 μl of urea buffer (8 M urea, 5% SDS, 200 mM Tris-Cl pH 6.8, 0.1 mM EDTA, 100 mM DTT) and incubated at 65°C for 15 min. Immunostainings were performed as described . For immunostaining following RNAi, cells were collected 12 days after dsRNA treatment. After fixation, permeabilisation and blocking, cells were incubated for 1 hr with antibody against ISWI, diluted 1:600 in blocking solution (2% BSA and 5% goat serum in PBS), or aISWIK753ac, diluted 1:300. After washes, cells were incubated for 1 hr with Cy3-conjugated secondary antibody (Jackson Immunoresearch Laboratories) diluted in blocking buffer. Cells were washed four times in PBS. DNA was counterstained with 1 μg/ml bisbenzimide (Hoechst 33258). Slides were mounted using 1.5% n-propyl gallate, 50% glycerol in PBS. Images were acquired using a Zeiss Axiophot microscope coupled to a Retiga Exi CCD Camera (Qimaging, Burnaby, Canada). Images were cropped and levels adjusted in Photoshop.
Total cell extracts were prepared as described  from 4 × 107 Drosophila cells. All steps were performed at 4°C. Cells were washed with PBS, resuspended in 1 volume of lysis buffer (50 mM Tris-Cl pH 8.0, 300 mM NaCl, 10 mM MgCl2, 0.4% NP40 and proteases inhibitors) and incubated for 15 min. The supernatant was cleared by centrifugation and mixed with 1 volume of dilution buffer (50 mM Tris-Cl pH 8.0, 0.4% NP40). Diluted extracts were pre-cleared with protein A/protein G Sepharose beads (Amersham Biosciences) and incubated with αISWI, αAcLysine or irrelevant antibodies, and immunoprecipitated with protein A/protein G Sepharose beads. Following extensive washing with a 1:1 mix of lysis and dilution buffer, beads were resuspended in Laemmli buffer and proteins were analyzed by Western blot analysis.
Western Blot Analysis
Immunoprecipitated proteins were separated by SDS-PAGE, electro-transferred onto PVDF or nitrocellulose membranes and detected using an ECL kit (Amersham Biosciences) according to the manufacturer's instructions.
In vivo labeling
Drosophila cells were treated with 0.5 mCi/ml [3H]-acetic acid (TRK12, Amersham Biosciences) and 10 mM sodium butyrate (NaB) for 3 hrs at 26°C. Whole cell extracts and immunoprecipitations were performed using standard procedures, except that all buffers were complemented with 5 mM sodium butyrate. Immunoprecipitated proteins were analyzed by Western blot or by autoradiography.
FLAG-ISWI mutants were expressed and purified from baculovirus vectors in Sf9 cells as described . Expression of proteins in E. coli and purification was according to the following published procedures: FLAG-ISWI and HIS6-ISWI deletion mutants ; GST-ISWI deletion mutants ; GST-hGCN5 and FLAG-p300 ; MOF .
In vitro acetylation assays
200 ng of FLAG-ISWI, 200 ng of His- or GST-ISWI deletion mutants, 2 μg of histone octamers or 200 ng of bacterially expressed histone H3 were incubated for 30 min at 26°C, in 20 μl final volume with 0.25 mCi of [3H]-acetyl-CoA (4.1 Ci/mmol, TRK688, Amersham Biosciences), 50 to 100 ng of GST-hGCN5, HA-MOF or FLAG-p300 in HAT buffer (10 mM Tris-Cl pH 7.8, 0.1 mM EDTA, complemented with 1 mM PMSF, 1 mM DTT and 10 mM NaB). Reaction mixtures were analyzed by SDS-PAGE. The gel was Coomassie stained, destained, treated with Amplify (Amersham Biosciences) for 30 min, dried and autoradiographed. 1 μg each of an H3 peptide (aa 1–19) or an ISWI peptide (aa 740–759) were acetylated under the same conditions. A 10 μl aliquot of each reaction was spotted onto p81 filters (Whatman), which were washed three times with 50 mM NaCarbonate pH 9.2 and counted in a scintillation counter.
Sequence alignment was performed using ClustalW software, using default parameters.
MALDI-TOF analysis of acetylated ISWI peptide. The in vitro acetylated peptides were purified on C18 reversed phase ZipTip mini-columns (Millipore) according to the manufacturer's protocol. In short the peptide was washed 3 times with 0.1% TFA, eluted with 1 μl of matrix solution [saturated a-cyanohydroxy-cinammic acid (Sigma) dissolved in 50% ACN (v/v)/0.3% TFA (v/v)] directly onto the target plate. The peptide-matrix co-crystal was analyzed in a Voyager DE STR spectrometer according to the manufacturer's instructions. Peptide mass fingerprints covered the mass range between 700–3500 amu, with the low mass gate set at 500 amu. The accelerating voltage was set to 20 kV, the grid to 66% and the delay time to 100 nsec. ESI-analysis. The ISWI peptide DQEIYYFRKTVGYKVPKNTEC plus a C-terminal cysteine (aa 740–759, M-H+ = 2580,27 amu) was digested with V8 protease. The resulting peptide IYYFRKTVGYKVPKNTE (M-H+ = 2106.14 amu) was de-salted, concentrated using a C18 reversed phase minicolumn (Eppendorf) and eluted in 0.5 μl 50% Methanol, 0.1% FA into medium size nano-spray needles (Protana, Odense, Denmark). ESI mass spectra were recorded on an Applied Biosystems QStar XL hybrid quadrupole time of flight mass spectrometer, equipped with a Protana nano-spray ion source in the static nano-spray mode according to the manufacturer's instructions. The needles were adjusted in front of the orifice and the spray voltage was set between 950 and 1100 V. Product ion scans were acquired for 4–5 min containing approximately 200–300 scans.
The ATPase assays were performed as described previously .
We thank I. Vetter for expert technical assistance and the following former and present lab members for reagents and advice: A. Akhtar, K. Bouazoune, V. Morales, C. Regnard, H. Würl. We also thank M. Heck, J. Tamkun, C. Wu, A. Hochheimer and J. Workman (Stowers Institute) for antibodies. This work was supported by Deutsche Forschungsgemeinschaft through SFB 594 (TP A6) and by the European Union via HPRN-CT-2000-00078 and the Network of Excellence FP6-503433.
- Smith CL, Peterson CL: ATP-dependent chromatin remodeling. Curr Top Dev Biol 2005, 65: 115-148.View ArticlePubMedGoogle Scholar
- Becker PB, Horz W: ATP-dependent nucleosome remodeling. Annu Rev Biochem 2002, 71: 247-273. 10.1146/annurev.biochem.71.110601.135400View ArticlePubMedGoogle Scholar
- Saha A, Wittmeyer J, Cairns BR: Chromatin remodelling: the industrial revolution of DNA around histones. Nat Rev Mol Cell Biol 2006,7(6):437-447. 10.1038/nrm1945View ArticlePubMedGoogle Scholar
- Workman JL: Nucleosome displacement in transcription. Genes Dev 2006,20(15):2009-2017. 10.1101/gad.1435706View ArticlePubMedGoogle Scholar
- Woodcock CL, Dimitrov S: Higher-order structure of chromatin and chromosomes. Curr Opin Genet Dev 2001,11(2):130-135. 10.1016/S0959-437X(00)00169-6View ArticlePubMedGoogle Scholar
- Varga-Weisz PD, Becker PB: Regulation of higher-order chromatin structures by nucleosome-remodelling factors. Curr Opin Genet Dev 2006,16(2):151-156. 10.1016/j.gde.2006.02.006View ArticlePubMedGoogle Scholar
- de la Serna IL, Ohkawa Y, Imbalzano AN: Chromatin remodelling in mammalian differentiation: lessons from ATP-dependent remodellers. Nat Rev Genet 2006,7(6):461-473. 10.1038/nrg1882View ArticlePubMedGoogle Scholar
- Muchardt C, Bourachot B, Reyes JC, Yaniv M: ras transformation is associated with decreased expression of the brm/SNF2alpha ATPase from the mammalian SWI-SNF complex. Embo J 1998,17(1):223-231. 10.1093/emboj/17.1.223PubMed CentralView ArticlePubMedGoogle Scholar
- Muchardt C, Reyes JC, Bourachot B, Leguoy E, Yaniv M: The hbrm and BRG-1 proteins, components of the human SNF/SWI complex, are phosphorylated and excluded from the condensed chromosomes during mitosis. Embo J 1996,15(13):3394-3402.PubMed CentralPubMedGoogle Scholar
- Bourachot B, Yaniv M, Muchardt C: Growth inhibition by the mammalian SWI-SNF subunit Brm is regulated by acetylation. Embo J 2003,22(24):6505-6515. 10.1093/emboj/cdg621PubMed CentralView ArticlePubMedGoogle Scholar
- Kouzarides T: Acetylation: a regulatory modification to rival phosphorylation? EMBO J 2000,19(6):1176-1179. 10.1093/emboj/19.6.1176PubMed CentralView ArticlePubMedGoogle Scholar
- Wang L, Mizzen C, Ying C, Candau R, Barlev N, Brownell J, Allis CD, Berger SL: Histone acetyltransferase activity is conserved between yeast and human GCN5 and is required for complementation of growth and transcriptional activation. Mol Cell Biol 1997,17(1):519-527.PubMed CentralView ArticlePubMedGoogle Scholar
- Akhtar A, Becker PB: Activation of transcription through histone H4 acetylation by MOF, an acetyltransferase essential for dosage compensation in Drosophila. Mol Cell 2000,5(2):367-375. 10.1016/S1097-2765(00)80431-1View ArticlePubMedGoogle Scholar
- Ogryzko VV, Schiltz RL, Russanova V, Howard BH, Nakatani Y: The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 1996,87(5):953-959. 10.1016/S0092-8674(00)82001-2View ArticlePubMedGoogle Scholar
- Grüne T, Brzeski J, Eberharter A, Clapier CR, Corona DF, Becker PB, Müller CW: Crystal structure and functional analysis of a nucleosome recognition module of the remodeling factor ISWI. Mol Cell 2003,12(2):449-460. 10.1016/S1097-2765(03)00273-9View ArticlePubMedGoogle Scholar
- Eberharter A, Vetter I, Ferreira R, Becker PB: ACF1 improves the effectiveness of nucleosome mobilization by ISWI through PHD-histone contacts. Embo J 2004,23(20):4029-4039. 10.1038/sj.emboj.7600382PubMed CentralView ArticlePubMedGoogle Scholar
- Corona DF, Tamkun JW: Multiple roles for ISWI in transcription, chromosome organization and DNA replication. Biochim Biophys Acta 2004,1677(1-3):113-119.View ArticlePubMedGoogle Scholar
- Badenhorst P, Xiao H, Cherbas L, Kwon SY, Voas M, Rebay I, Cherbas P, Wu C: The Drosophila nucleosome remodeling factor NURF is required for Ecdysteroid signaling and metamorphosis. Genes Dev 2005,19(21):2540-2545. 10.1101/gad.1342605PubMed CentralView ArticlePubMedGoogle Scholar
- Roth SY, Denu JM, Allis CD: Histone Acetyltransferases. Annu Rev Biochem 2001, 70: 81-120. 10.1146/annurev.biochem.70.1.81View ArticlePubMedGoogle Scholar
- Brooks CL, Gu W: Ubiquitination, phosphorylation and acetylation: the molecular basis for p53 regulation. Curr Opin Cell Biol 2003,15(2):164-171. 10.1016/S0955-0674(03)00003-6View ArticlePubMedGoogle Scholar
- Eberharter A, Ferreira R, Becker P: Dynamic chromatin: concerted nucleosome remodelling and acetylation. Biol Chem 2005,386(8):745-751. 10.1515/BC.2005.087View ArticlePubMedGoogle Scholar
- Längst G, Becker PB: Nucleosome mobilization and positioning by ISWI-containing chromatin remodeling factors. J Cell Science 2001, 114: 2561-2568.PubMedGoogle Scholar
- Badenhorst P, Voas M, Rebay I, Wu C: Biological functions of the ISWI chromatin remodeling complex NURF. Genes Dev 2002,16(24):3186-3198. 10.1101/gad.1032202PubMed CentralView ArticlePubMedGoogle Scholar
- Corona DFV, Längst G, Clapier CR, Bonte EJ, Ferrari S, Tamkun JW, Becker PB: ISWI is an ATP-dependent nucleosome remodeling factor. Molecular Cell 1999, 3: 239-245. 10.1016/S1097-2765(00)80314-7View ArticlePubMedGoogle Scholar
- Fyodorov DV, Blower MD, Karpen GH, Kadonaga JT: Acf1 confers unique activities to ACF/CHRAC and promotes the formation rather than disruption of chromatin in vivo. Genes Dev 2004,18(2):170-183. 10.1101/gad.1139604PubMed CentralView ArticlePubMedGoogle Scholar
- Hebbes TR, Turner CH, Thorne AW, Crane-Robinson C: A "minimal epitope" anti-protein antibody that recognises a single modified amino acid. Mol Immunol 1989,26(9):865-873. 10.1016/0161-5890(89)90143-0View ArticlePubMedGoogle Scholar
- Maiato H, Sunkel CE, Earnshaw WC: Dissecting mitosis by RNAi in Drosophila tissue culture cells. Biol Proced Online 2003, 5: 153-161. 10.1251/bpo57PubMed CentralView ArticlePubMedGoogle Scholar
- Morales V, Straub T, Neumann MF, Mengus G, Akhtar A, Becker PB: Functional integration of the histone acetyltransferase MOF into the dosage compensation complex. Embo J 2004,23(11):2258-2268. 10.1038/sj.emboj.7600235PubMed CentralView ArticlePubMedGoogle Scholar
- Ferreira R, Magnaghi-Jaulin L, Robin P, Harel-Bellan A, Trouche D: The three members of the pocket proteins family share the ability to repress E2F activity through recruitment of a histone deacetylase. Proc Natl Acad Sci U S A 1998,95(18):10493-10498. 10.1073/pnas.95.18.10493PubMed CentralView ArticlePubMedGoogle Scholar
- Eberharter A, Ferrari S, Langst G, Straub T, Imhof A, Varga-Weisz P, Wilm M, Becker PB: Acf1, the largest subunit of CHRAC, regulates ISWI-induced nucleosome remodelling. EMBO J 2001,20(14):3781-3788. 10.1093/emboj/20.14.3781PubMed CentralView ArticlePubMedGoogle Scholar
- Imhof A, Yang X, Ogryzko VV, Nakatani Y, Wolffe AP, Ge H: Acetylation of general transcription factors by histone acetyltransferases. Current Biology 1997, 7: 689-692. 10.1016/S0960-9822(06)00296-XView ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.