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Previous Article | Next Article 
Molecular and Cellular Biology, October 2003, p. 6759-6768, Vol. 23, No. 19
0270-7306/03/$08.00+0 DOI: 10.1128/MCB.23.19.6759-6768.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.
Jing-Yi Huang,3 Gary LeRoy,1,2 Sherrie Hu,1,2 Yuh-Hwa Wang,2 Robert J. Donnelly,4, William S. Lane,5 Sheng-Chung Lee,3 and Danny Reinberg1,2*
Howard Hughes Medical Institute,2 Division of Nucleic Acids Enzymology,4 Department of Biochemistry, University of Medicine and Dentistry of New JerseyRobert Wood Johnson Medical School, Piscataway, New Jersey 08854,3 Institute of Molecular Medicine, National Taiwan University, Taipei, Taiwan,5 Molecular Resource Facility, New Jersey Medical School, University of Medicine and Dentistry of New Jersey, Newark, New Jersey 07103,1 Microchemistry and Proteomics Analysis Facility, Harvard University, Cambridge, Massachusetts 021386
Received 17 April 2003/ Returned for modification 15 May 2003/ Accepted 17 June 2003
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ABSTRACT |
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INTRODUCTION |
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The dynamic state of chromatin is the result of factors that perturb the state of chromatin in conjunction with factors that assemble or reposition components of chromatin. Two main families of proteins perturb chromatin: (i) enzymes that covalently modify the N-terminal tail of the histones (17, 29) and (ii) ATP-dependent chromatin remodeling complexes, which utilize the energy of ATP hydrolysis to mobilize nucleosomes or to otherwise alter chromatin structure (24, 26). These protein complexes render DNA more accessible to the binding of transcriptional regulatory factors. In addition, several factors that assemble or reposition nucleosomes have been identified and classified according to whether or not their function is coupled to DNA replication. Chromatin assembly occurs primarily during the S phase of the cell cycle, when DNA replication takes place and histone polypeptides are newly synthesized. However, outside of the S phase, chromatin assembly also occurs, although to a much lesser extent. DNA repair, histone turnover, and transcription are examples of processes during which chromatin can be temporarily altered (14, 23).
The model of nucleosome assembly proposes that histone chaperones deposit H3/H4 tetramers onto DNA in a reaction that seems to be the rate-limiting step, followed by the deposition of H2A/H2B dimers. Once histone chaperones deposit histones onto the DNA, chromatin spacing complexes mobilize the nucleosomes to produce a regularly spaced nucleosomal array. Several different chromatin spacing factors have been identified in various species (23). All of these factors share an ATPase-containing subunit, which belongs to the ISWI family. ISWI was initially identified in Drosophila melanogaster, in three different "chromatin-remodeling" complexes: ACF (10), CHRAC (25), and NURF (22). A new complex containing components of NURF, as well as TRF-2 (for TBP-related factor 2), has been identified recently (9). It has been proposed that this complex may be involved in core promoter selectivity of a subset of Drosophila genes. In yeast, there are two ISWI homologues—ISWI1 and ISWI2—each of which is a part of distinct chromatin-remodeling complexes (21). In Xenopus laevis, five ISWI complexes have been identified, one of which is the homologue of ACF (7). In humans, there are two known ISWI homologues: hSNF2H and hSNF2L. hSNF2H is part of several different chromatin-remodeling complexes, including ACF and BAZ-like complexes (2, 3, 11), CHRAC (16), NoRC (20), RSF (12), and an hSNF2H complex containing components of the cohesin and NuRD complexes (8). In contrast, hSNF2L-containing chromatin-remodeling complexes have not yet been identified. Importantly, although all of these factors share the ISWI subunit, not all of them have the ability to assemble nucleosomes.
We have previously described RSF, which is composed of two subunits, hSNF2H and p325 (Rsf-1), a protein encoded by an as-yet-uncharacterized novel gene(s). RSF was isolated from HeLa cells as an activity that allows the formation of competent RNA polymerase II transcription initiation complexes on chromatin templates as a result of its ability to mobilize nucleosomes (12). Later on, we discovered that RSF could assemble chromatin in vitro in an energy-dependent manner (13). However, in contrast to the other chromatin assembly and spacing factors, RSF-mediated chromatin assembly was found to be independent of histone chaperones (13). We describe here the isolation of a cDNA encoding Rsf-1, the largest subunit of RSF. Using complex generated with recombinant RSF, we have fully reconstituted the chromatin assembly reaction and analyzed the function of each individual subunit in the chromatin assembly reaction in vitro.
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MATERIALS AND METHODS |
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Peptide sequencing of Rsf-1 by ion trap mass spectrometry. Rsf-1 was isolated by sodium dodecyl sulfate (SDS)-polyacrylamide gel electrophoresis and then subjected to reduction, carboxyamidomethylation, and digestion with trypsin. Peptides were analyzed by microcapillary reversed-phase high-pressure liquid chromatography nanoelectrospray tandem mass spectrometry on an LCQ DECA XP quadrupole ion trap mass spectrometer (ThermoFinnigan). A normalized collision energy of 30% and with an isolation width of 2.5 Da was used, with recurring ions dynamically excluded. Preliminary mapping of peptide sequences was accomplished with the SEQUEST algorithm.
Cloning of Rsf-1 and production of the corresponding protein in baculovirus. Peptide sequences from Rsf-1 obtained by ion trap mass spectrometry identified multiple expressed sequence tag (ESTs) from the NCBI EST database. Two clones (accession numbers 545521 and 626008) were used to screen a HeLa cell (Clontech) and a human heart (Novagen) cDNA library according to the suppliers' instructions. We obtained four overlapping cDNAs that were used to construct the full-length cDNA. The Flag peptide sequence was inserted at the 5' end, in frame, by using the PCR. In order to produce baculoviruses, the full-length Rsf-1 gene was subcloned into pVL1393 vector (Pharmingen), and the recombinant viruses were generated by using BaculoGold DNA (Pharmingen).
Northern blot. Northern blots were carried out by using multiple-tissue Northern blots according to the supplier's instructions (Clontech). The Rsf-1 probe extended from nucleotides 1750 to 4018. The ß-actin probe used was provided by the supplier.
Alkaline phosphatase treatment. Native RSF (0.5 µg) was treated with 1 U of alkaline phosphatase (Roche) for 30 min at 37°C. The reaction was stopped with SDS sample buffer, and the proteins were resolved on an SDS-polyacrylamide gel and then silver stained.
Immunofluorescence microscopy. HeLa cells grown on coverslips were fixed with 1% paraformaldehyde for 30 min, washed with phosphate-buffered saline (PBS), and permeabilized with 0.1% Triton X-100. Cells were stained by sequential incubation with antibodies to the proteins of interest (first antibodies) and secondary fluorescence-labeled antibodies and then visualized with a TCS (Leica) confocal imaging system.
Interphasic and mitotic nuclear extracts. HeLa cells at 70% confluency were treated (mitotic extract) or not treated (interphasic extract) with 100 ng of nocodazole/ml for 20 h. Mitotic HeLa cells became deattached from the plate; therefore, nontreated cells were washed several times with PBS in order to eliminate mitotic cells. The medium of the treated cells, on the other hand, was collected, and the plate was washed several times to recover all mitotic cells. After a wash with PBS, the cells were resuspended in hypotonic buffer (20 mM HEPES [pH 7.8], 5 mM potassium acetate, 0.5 mM MgCl2) and Dounce homogenized 25 times. The solution was centrifuged at 4,500 rpm for 3 min, and the pellet was resuspended in the same buffer containing 1 M NaCl, followed by incubation for 1.5 h at 4°C. The suspension was centrifuged at 14,000 rpm for 20 min, and the supernatant (nuclear extract) was directly used for immunoprecipitation assays.
Protein purification. HeLa cell core histones were purified as described previously (15). Native RSF was purified from HeLa nuclear pellet as described previously (12). Recombinant Flag-tagged HBXAP and Rsf-1 were expressed from baculovirus in Sf9 cells. Briefly, Sf9 cells were infected at a multiplicity of infection of 10 for 48 h. The cells were then pelleted, washed twice with cold PBS buffer, resuspended in lysis buffer (20 mM Tris-HCl [pH 7.9], 0.6 M NaCl, 4 mM MgCl2, 0.4 mM EDTA, 2 mM dithiothreitol, 20 mM ß-glycerophosphate, 20% glycerol, 0.4 mM phenylmethylsulfonyl fluoride, 1 mM benzamidine-HCl, 4 µg of leupeptin/ml, 2 µg of aprotinin/ml), and subjected to freeze-thaw disruption. The insoluble material was removed by centrifugation at 11,000 rpm (SLA-600TC rotor; Sorvall) for 10 min at 4°C, and the supernatant was incubated with anti-FLAG M2-agarose beads for 4 h at 4°C. The beads were washed with lysis buffer, and the bound proteins were eluted with 0.2 mg of Flag peptide/ml dissolved in lysis buffer. Recombinant RSF was expressed from baculovirus in Sf9 cells coinfected with Flag-tagged Rsf-1 and hSNF2H baculoviruses at a multiplicity of infection of 10. Recombinant RSF was purified with M2-agarose beads as described above, and the M2 column eluate was further purified by gel filtration chromatography. Recombinant hSNF2H was expressed from baculovirus in Sf9 cells and purified by chromatography on DEAE-52 resin. The protein was eluted from the DEAE-52 column with a linear ammonium sulfate gradient between 50 and 500 mM.
Immunoprecipitation. Immunoprecipitations were performed as described previously, with several washes with a salt concentration of 500 mM KCl plus 0.05% NP-40 (13).
DNA-binding assays. A radiolabeled 206-bp DNA fragment was incubated for 15 min at 30°C with recombinant RSF, recombinant hSNF2H, or recombinant Rsf-1 at the indicated molar ratio, in buffer consisting of 10 mM HEPES (pH 7.5), 60 mM KCl, 0.5 µg of bovine serum albumin, 0.5 mM EGTA, 10% glycerol, 1 mM dithiothreitol, and 0.2 mM phenylmethylsulfonyl fluoride. The reaction was loaded onto nitrocellulose membranes which were air dried and washed three times with TE buffer (10 mM Tris [pH 7.9], 0.1 mM EDTA). The 32P that remained on the membrane after the washing step was quantified by using a scintillation counter.
Electron microscopy. hSNF2H or Rsf-1 were incubated with 3-kb EcoRI-linearized plasmid in the presence or absence of HeLa-purified core histones in the chromatin assembly buffer. The incubation was performed for 30 min at 30°C. For the characterization of the DNA-protein complexes, the reaction was incubated with antibodies against the RSF subunit hSNF2h. After the first antibody incubation, the reaction was fixed with glutaraldehyde and purified by gel filtration (1 ml, A5 M resin; Bio-Rad). The reaction was incubated with secondary antibodies conjugated with 10-nm gold particles and then fixed with glutaraldehyde, purified, and prepared for electron miscroscopy. The protein-DNA complexes were mixed in a buffer containing 2 mM spermidine, adsorbed to glow-charged carbon-coated grids, washed with a water-graded-ethanol series, and rotary shadow cast with tungsten. Samples were examined with a Philips 420 electron microscope. Micrographs are shown in reverse contrast. A Cohu charge-coupled device camera attached to a Macintosh computer programmed with NIH IMAGE software was used to form the images. The percentage results presented were obtained by counting at least 100 DNA molecules per experiment.
ATPase. The ATPase assay was performed as described previously (28).
Chromatin assembly and analysis. The chromatin assembly reactions and micrococcal nuclease digestions were performed as previously described (13)
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RESULTS |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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11-kb species, an 7-kb mRNA, and an 5.6-kb mRNA, which are probably alternatively spliced species since all of them hybridized with a probe to p325. p325 mRNA is expressed at different levels in the tissues analyzed; a high level of expression was observed in the heart, skeletal muscle, kidney, and placenta, whereas very low levels existed in other tissues such as the brain and colon (Fig. 1C). During our studies on the RSF-p325 subunit a new cDNA, HBXAP (XAP-8), was deposited in the GenBank database (accession number NM016578 [gi 10835261]). HBXAP cDNA is similar to the one encoding RSF-p325 except that 252 amino acids found at the N terminus of p325 are missing (Fig. 1A). HBXAP was identified in a two-hybrid screen for proteins that interact with the transcriptional activator pX, which is encoded by the hepatitis B virus (HBV) (18). Functional assays demonstrated that HBXAP stimulated HBV transcription in a pX-dependent manner (18). Later, a larger version of HBXAP was deposited in the GenBank database (accession number AF380176 [gi 14211815]), and this species corresponded exactly to the RSF-p325 gene sequence.
Western blot analyses with monoclonal antibodies generated against the full-length RSF-p325 protein demonstrated that the cDNA clone we isolated encodes the full-length open reading frame of RSF-p325 (Fig. 3B). As mentioned above, the predicted molecular mass of p325 is 164 kDa, but it migrates above the 200-kDa marker and below the histone acetyltransferase p300 (which has a predicted molecular mass of 332 kDa) on SDS-polyacrylamide gels. This slower migration of p325 is due to its highly acidic charge and also to phosphorylation, since treatment of the protein with phosphatase resulted in the generation of a species that migrated faster than untreated p325 on SDS-polyacrylamide gels (Fig. 1D). This faster-migrating species was not a result of proteolysis since antibodies recognizing the N and C termini of p325 were reactive with this new species (data not shown). Moreover, the smallest subunit of RSF, hSNF2H, did not change its migration upon phosphatase treatment (data not shown). It is worth mentioning that the phosphorylation state of p325 does not affect the chromatin assembly reaction. RSF treated with alkaline phosphatase is able to assemble chromatin with a specific activity similar to that of the phosphorylated form (data not shown). To avoid confusion between the name of the protein and its molecular mass and to follow the nomenclature that has been used for other chromatin-remodeling factor subunits, we named p325 Rsf-1.
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Recombinant RSF. To understand the functional importance of each subunit of RSF, baculoviruses encoding each of the RSF subunits were used to infect Sf9 cells individually or together (coinfection). The procedure used to purify each of the polypeptides resulted in highly purified proteins (see Materials and Methods and Fig. 3A and B).
To test whether the recombinant RSF complex has activity, we analyzed its ability to carry out ATP hydrolysis and chromatin assembly in vitro. The nucleosome-stimulated ATPase activity of the recombinant complex, isolated by coinfection of viruses carrying individual subunits, was comparable to that of native RSF (Fig. 3C). Also, there was no apparent difference in chromatin assembly activity between recombinant and native RSF as gauged by micrococcal nuclease digestion of assembled chromatin (Fig. 3D). Moreover, the specific activity of the native and recombinant RSF complexes was similar in both assays (data not shown). From these experiments, we conclude that recombinant RSF is functionally equivalent to the native complex, at least with respect to its ATPase and chromatin assembly activities.
Function of the individual RSF components Rsf-1 and hSNF2H. We first assessed the individual subunits for their role in generating the ATPase activity of the RSF complex. As shown previously, hSNF2H alone showed a strong ATPase activity (Fig. 4A, lanes 2 to 4), which is nucleosome dependent (data not shown). On the other hand, Rsf-1 did not display ATPase activity (Fig. 4A, lanes 5 and 6). Moreover, Rsf-1 did not affect the hSNF2H-dependent ATPase activity (Fig. 4A, lanes 7 and 8). This suggests that the ATPase activity of hSNF2H is independent of Rsf-1. This result agrees with findings for the Drosophila ISWI protein, in which Acf-1 was unable to stimulate the ATPase activity of ISWI under several different conditions (6).
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We previously proposed that the binding of RSF to core histones through Rsf-1 is followed by the binding of the RSF-histone complex to the DNA (13). Therefore, we investigated whether the individual subunits of RSF could bind to DNA. Two types of experiments were performed. First, we analyzed the association of hSNF2H and Rsf-1 to DNA by electron microscopy, mixing recombinant hSNF2H or Rsf-1 along with DNA in the presence or absence of core histones. When hSNF2H was analyzed in the presence or absence of core histones, we observed ca. 30% (in the presence of histones), and the majority (in the absence of histones) of the DNA molecules contained a single large protein complex (Fig. 5A, upper panels). The large protein complex observed on the DNA was composed of hSNF2H, as demonstrated by probing the reaction with gold-conjugated antibodies to hSNF2H (Fig. 5A, upper panels). This result suggested that hSNF2H is able to interact with DNA regardless of the presence of core histones. The analysis of Rsf-1 showed the formation of similar large protein complexes in ca. 20% of the DNA molecules when the reaction was carried out in the presence of core histones (Fig. 5A, bottom panel). In contrast, when the reaction was carried out in the absence of core histones, the large protein complex bound to the DNA was not observed (data not shown).
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Taken together, these experiments suggest that each subunit of RSF has a defined role in chromatin assembly; Rsf-1 is the histone chaperone of the complex probably allowing nucleosome formation, while hSNF2H provides the energy for the nucleosome spacing activity.
Rsf-1 versus HBXAP. As mentioned above, while we were cloning the full-length cDNA encoding Rsf-1, a new cDNA, HBXAP was identified with a sequence identical to that of Rsf-1, except that it lacked 252 amino acids found at the N terminus of Rsf-1 (18). That report showed that HBXAP physically associates with HBV-pX and facilitates pX-dependent stimulation of HBV transcription. Therefore, we were interested in studying HBXAP in the context of the RSF complex.
For this series of experiments, we cloned and expressed Flag-tagged HBXAP in baculovirus-infected Sf9 cells and used these cells as our source for purification of recombinant HBXAP (Fig. 6A). We first tested the ability of HBXAP to associate with hSNF2H. As a control, we used Flag-tagged Rsf-1, which, as expected, showed interaction with hSNF2H by immunoprecipitation (Fig. 6B, lane 4). In contrast, we found that HBXAP, which lacks only 252 amino acids at the N-terminal region of Rsf-1, was unable to interact with hSNF2H (Fig. 6B, lanes 5 and data not shown).
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Taken together, these results suggest that the failure of HBXAP to assemble chromatin is due to the inability of HBXAP to interact with hSNF2H. This conclusion suggests that the activities of each of the RSF subunits (that is, the ability of Rsf-1 to interact with core histones and the ATPase activity of hSNF2H) are tightly coupled during chromatin assembly.
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DISCUSSION |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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The largest subunit of RSF, Rsf-1, turned out to be a larger version of the recently identified protein HBXAP. Northern blot analyses revealed the existence of several species of Rsf-1 and HBXAP mRNAs (19) (Fig. 1C). Consequently, it is likely that a family of Rsf-1/HBXAP proteins exists.
HBXAP is involved in pX-dependent activation of HBV transcription (18) and also displayed a transcriptional repressive activity in vitro when targeted to a reporter gene by fusion to the Gal4 DNA-binding domain (19). The RSF complex, on the other hand, was initially identified as a chromatin-remodeling complex and, due to its ability to mobilize nucleosomes in vitro, allows the binding of transcriptional activators to their target sites. As a result, competent RNA polymerase II preinitiation complexes can be formed on chromatin templates (12). The apparent discrepancy between the roles of HBXAP and Rsf-1 may be due to the inability of HBXAP to interact with hSNF2H and, therefore, with chromatin remodeling complexes. Consistent with this is our observation that HBXAP is unable to support chromatin assembly in vitro. Taken together, these results suggest that Rsf-1 and HBXAP have distinct functions in the cell. In order to analyze further Rsf-1 and HBXAP, we developed antibodies against the N-terminal region of Rsf-1 that is missing in HBXAP. We used these antibodies for localization studies in HeLa cells with immunofluorescence analyses, but we could not observe any differences when the resultant immunofluorescence patterns were compared to those generated with antibodies that recognize both Rsf-1 and HBXAP (data not shown).
It is possible that the histone chaperone activity of Rsf-1 is, in part, a consequence of its acidic properties and the presence of glutamic and aspartic acid stretches at the C-terminal region. We searched for sequence homology with other histone chaperone proteins, such as CAF-1 and NAP-1, but we were unable to find any clear similarities. Homology searches between Rsf-1 and other subunits of the ISWI chromatin remodeling complexes, such as Acf-1 (as well as the BAZ family of proteins) and NURF-301, yielded no matches. A search for homologues in other species showed a candidate in Drosophila, the CG8677 gene product.
Regarding the hSNF2H and Rsf-1 association, we have found that almost all hSNF2H found in the HeLa nuclear pellet fraction is associated with Rsf-1 (data not shown). In contrast, the hSNF2H found in the nuclear extract fraction is associated with several forms of ACF and BAZ-containing complexes. With respect to Rsf-1, we have not found Rsf-1 that is not associated with hSNF2H (data not shown), suggesting that Rsf-1 exists in the cell as RSF.
RSF and other members of the ISWI family of chromatin remodeling factors are abundant in HeLa cells. We found that there are similar amounts of RSF and ACF in HeLa cells (11). An obvious question, then, is why does the cell need so much of and so many kinds of these factors? One likely explanation is that each complex has a specific function and that its activity is modulated by the other components of the complexes. Unfortunately, most of the biochemical analyses carried out thus far showed that the complexes have similar properties (for example, ATPase, chromatin assembly, and chromatin remodeling). Therefore, the development of specific assays will be necessary for the analysis of each of these complexes. As an example, RNA interference has been used recently for the analysis of the function of ACF in vivo. The experiments suggest that ACF has a role in DNA replication of heterochromatin at pericentromeric regions, allowing DNA replication to proceed through highly condensed chromatin regions (5).
Consequently, one of the challenges of future investigations is to decipher the mechanism of action of these factors within the cell, as well as to discover the functional differences between the various chromatin-remodeling factors.
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ACKNOWLEDGMENTS |
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This work was supported by a grant from the National Institutes of Health (GM37120) and by the Howard Hughes Medical Institute.
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FOOTNOTES |
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Present address: Institut Curie, Section de Recherche, UMR218, 75231 Paris Cedex 05, France.
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