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Genes Dev. Mar 1, 2001; 15(5): 619–626.
PMCID: PMC312638

In vivo chromatin remodeling by yeast ISWI homologs Isw1p and Isw2p


Isw1p and Isw2p are budding yeast homologs of the Drosophila ISWI chromatin-remodeling ATPase. Using indirect-end-label and chromatin immunoprecipitation analysis, we show both independent and cooperative Isw1p- and Isw2p-mediated positioning of short nucleosome arrays in gene-regulatory elements at a variety of transcription units in vivo. We present evidence that both yeast ISWI complexes regulate developmental responses to starvation and that for Isw2p, recruitment by different DNA-binding proteins controls meiosis and haploid invasive growth.

Keywords: Yeast, chromatin, transcription, Isw1p, Isw2p, chromatin-remodeling ATPase

Eukaryotic genomes are packaged into chromatin, a nucleoprotein complex with a hierarchy of condensed structures. Transcription, replication, recombination, and repair of DNA require enzymes and trans-acting factors to gain access to DNA in chromatin, and the facilitation of this by remodeling chromatin structure has emerged as an important theme in the regulation of these processes. A range of recent genetic and biochemical experiments have identified mechanisms that act to remodel the primary repeating unit of chromatin, the nucleosome core particle that consists of 146 bp of DNA wrapped around two copies of each histone protein H2A, H2B, H3 and H4. These mechanisms fall into two main categories. The first class involves covalent modification of histone protein N-terminal tails, typically by acetylation, methylation, and phosphorylation. The second class appears to use ATP hydrolysis to alter the conformation or location of the nucleosome. These two mechanisms are not mutually exclusive, and both may interact in regulating chromatin fluidity (Xue et al. 1998; for review, see Cairns 1998; Kingston and Narlikar 1999).

ATP-dependent chromatin remodeling is catalyzed by a variety of multi-subunit protein complexes that all contain members of a superfamily of ATPase enzymes conserved throughout the Eukaryota. The various ATP-dependent chromatin-remodeling complexes can be grouped into three main families (SWI/SNF-, ISWI- and Mi-2/CHD-like) on the basis of the primary structure of their ATPase subunits and in vitro biochemical activities (for review, see Kingston and Narlikar 1999; Brehm et al. 2000). Although the ISWI-like complexes have undergone extensive biochemical analysis, relatively little is known of their physiological role. In Drosophila, the ISWI ATPase purifies as a component of three compositionally and functionally distinct chromatin-remodeling complexes termed NURF, ACF, and CHRAC. Immunolocalization of ISWI in Drosophila cells suggests that one or more of these complexes is abundantly distributed over both mitotic and polytene chromosomes. Analysis of null alleles suggests that ISWI activity is essential for development and is required for normal X chromosome structure. The ISWI protein appears to localize to nontranscribed regions of polytene chromosomes but is also required for engrailed and ultrabithorax expression, suggesting participation in both gene repression and activation processes (Deuring et al. 2000). A Xenopus ISWI activity has recently been implicated in the chromatin remodeling that takes place when somatic nuclei are transplanted into oocytes (Kikyo et al. 2000). Budding yeast contains two ISWI homologs: Isw1p, which purifies in a complex with three other proteins, and Isw2p, which purifies separately with one other protein. Both complexes show ATP-dependent nucleosome spacing activities in vitro, and the Isw1p complex also shows in vitro nucleosome disruption activity similar to NURF (Tsukiyama et al. 1999). Although disruption of both ISW1 and ISW2 genes has very little phenotypic effect in vegetatively growing yeast (Tsukiyama et al. 1999), a recent transcriptome analysis suggests that both Isw1p and Isw2p are involved in gene activation and repression (Hughes et al. 2000). Diploid isw2 homozygotes also appear to be unable to undergo premeiotic DNA replication, suggesting that Isw2p activity might be required for activation of meiosis/sporulation-specific genes (Trachtulcova et al. 2000). Nevertheless, it remains unclear how the nucleosome remodeling activity of the ISWI proteins manifests in real chromatin.

We therefore decided to look for ISWI-dependent chromatin structures directly in vivo. Nucleosome position at a specific locus can be inferred by comparing micrococcal nuclease (MNase) cleavage patterns in digests of chromatin with those obtained for purified DNA (Livingstone-Zatchej and Thoma 1999). We have been using indirect-end-label analysis for rapid MNase digestion of chromatin in whole yeast cells, previously employed to study SWI/SNF nucleosome-remodeling activity in vivo (Kent and Mellor 1995; Wu and Winston 1997), to screen panels of yeast loci for changes in chromatin structure in strains deficient in various chromatin-remodeling activities. The indirect-end-label methodology allows relatively large regions of chromatin to be visualized in terms of nucleosome footprints in MNase digestion patterns, allowing identification of target regions for chromatin modulators and providing information on mechanistics, targeting, and remodeling factor abundance. Here we show that during vegetative growth in rich media, both Isw1p- and Isw2p-dependent chromatin structures are common in yeast regulatory DNA.

Results and Discussion

We took two approaches in our search for Isw1/2p-dependent chromatin structures. Initially we analyzed a panel of seven yeast loci including DRS2 and GDH3, which were picked at random from Chromosome I (Avedano et al. 1997; Chen et al. 1999), and HIS3, MET16, MET17, PHO5, and PHO3, which were chosen because their chromatin structure has been characterized previously (Struhl 1983; Almer et al. 1986; Kent et al. 1994; O'Connell et al. 1995; Svaren and Hörz 1997). During these experiments, an isw1/2 mutant transcriptome became available (Hughes et al. 2000). We therefore also analyzed the FIG1 gene (Erdman et al. 1998), which is induced in isw1 mutant yeast, and the INO1 gene (Jackson and Lopes 1996), which is induced in isw2 yeast, with the prediction that we might observe Isw1p- and Isw2p-dependent changes in chromatin, respectively.

Chromatin structures were examined by comparing MNase cleavage patterns in isw1 isw2 double mutants and isogenic wild-type strains during exponential vegetative growth in rich medium. No changes in MNase cleavage pattern were detected at PHO5 or HIS3 (Fig. (Fig.1A;1A; data not shown). Figure Figure1A1A shows that both repressed and activated chromatin structures at PHO5 (Svaren and Hörz 1997) occur normally in the absence of Isw1p and Isw2p. However, at DRS2, FIG1, GDH3, INO1, MET16, MET17, and PHO3, we observed changes in chromatin MNase cleavage patterns in isw1 isw2 yeast, which localized to potential regulatory DNA in both promoters and 5′ ORF regions (Fig. (Fig.1;1; data not shown). These results suggest that yeast ISWI factors act widely throughout the yeast genome. The loci with ISWI-dependent MNase cleavage patterns were then analyzed further in isw1 and isw2 single mutants to determine the contribution of each ISWI complex.

Figure 1
Isw1p- and Isw2p-dependent changes in MNase accessibility in yeast chromatin mapped by indirect-end-label analysis. All chromatin digestions were performed with MNase at concentrations of 75, 150, and 300 units/mL. Naked DNA controls are marked “DNA.” ...

Isw1p- and Isw2p-dependent chromatin structures

At the loci we sampled, we found three types of contribution from Isw1p and Isw2p; examples of each are presented in Figure Figure1.1. The DRS2 locus showed a chromatin structure that altered only in cells lacking Isw1p, that is, where the MNase cleavage pattern in the isw1 single mutant is identical to the isw1 isw2 pattern but the isw2 pattern is identical to wild type (Fig. (Fig.1B).1B). Chromatin structures at the GDH3 promoter and within the 5′ ORF of MET16 were similarly Isw1p dependent (data not shown). The INO1 and PHO3 promoters, however, showed chromatin structures that altered only in the absence of Isw2p, that is, where MNase cleavage patterns in the isw2 single mutant are identical to the isw1 isw2 pattern but isw1 patterns are identical to wild type (Fig. (Fig.1C,D).1C,D). These results therefore suggest that the Isw1p and Isw2p complexes can function independent of each other. However, analysis of MNase cleavage patterns at the FIG1 and MET17 loci revealed regions of chromatin that appear to require the action of both Isw1p and Isw2p together, that is, where neither single-mutant MNase cleavage pattern is identical to the isw1 isw2 double-mutant pattern (Fig. (Fig.1E,F).1E,F). Figure Figure1E1E illustrates the Isw1p-dependent MNase cleavage patterns within the 5′ ORF of FIG1 and an Isw2p-dependent cleavage site within the promoter, close to the Dra I site at −279 bp. At the MET17 locus (Fig. (Fig.1F),1F), the ISWI-dependent region of MNase cleavage is located not within the regulatory DNA of MET17 but over a solo Ty1 retroposon δ element (a sequence equivalent to a retroviral long terminal repeat) termed YLRCδ18. At this locus, the isw1 pattern is essentially the same as the wild-type structure, and the isw2 pattern only shows one cleavage site characteristic of the isw1 isw2 double mutant. This result suggests that both Isw1p and Isw2p act on chromatin in this region, although Isw2p alone is sufficient for the wild-type structure as far as we can detect with MNase. To test whether the ISWI-dependent chromatin structure that we observe at YLRCδ18 might be a general feature of Ty1δ elements, we picked a full-length Ty1 retroposon, YARCTy1-1, at random from the yeast genome and analyzed the MNase cleavage pattern of its 5′ δ in wild-type and isw1 isw2 strains. Figure Figure1G1G shows that an ISWI-dependent change in MNase accessibility also occurs within this δ element. Therefore, it appears likely that Isw1p and Isw2p together affect δ element chromatin.

Drosophila ISWI- and both yeast Isw1p- and Isw2p-containing complexes show similar ATP-dependent transdisplacement activity toward in vitro assembled nucleosomes (Hamiche et al. 1999; Längst et al. 1999; Tsukiyama et al. 1999). The in vivo ISWI-dependent chromatin structures we observe are all consistent with this observed activity: In all cases, MNase cleavage sites characteristic of deproteinized DNA are protected in wild-type and isw1/2 mutant chromatin, implying the presence of nucleosomes in both states. However, chromatin-specific cleavage sites in wild-type and isw1/2 yeast differ in relative position (typically by 50–100 bp), suggesting that two to three nucleosomes at each of these loci adopt alternative translational positions in the absence of Isw1p and/or Isw2p (Fig. (Fig.2).2).

Figure 2
Inferred nucleosome positions at (A) DRS2, (B) PHO3, and (C) the solo Ty δ element at MET17. MNase cleavage sites are plotted relative to the nearest ORF for naked DNA (DNA) and chromatin in wild-type (WT) and isw mutant yeast. Nucleosomes are ...

To test whether Isw1p and Isw2p are acting directly on the nucleosomal templates we have analyzed, we next performed chromatin immunoprecipitation (ChIP) experiments with strains expressing tagged Isw1p and Isw2p. Chromatin structures at FIG1 and INO1 are identical to wild type in the Isw1p–myc- and Isw2p-myc-tagged strains, respectively (data not shown), indicating that both tagged proteins are functional. ChIP samples were analyzed with PCR primers designed to amplify the regions associated with the ISWI-dependent chromatin structures shown in Figure Figure1.1. Figure Figure3A3A shows anti-myc–tag specific ChIP of regions of Isw1p-dependent chromatin in the Isw1p–-myc strain and similarly specific ChIP of regions of Isw2p-dependent chromatin in the Isw2p-myc strain. Loci such as FIG1 and the Ty δ element at MET17 that show chromatin structures that are dependent on both Isw1p and Isw2p show ChIP of DNA in both marked strains. We note here that ChIP with Isw1p–-myc recovers about fourfold less DNA than an equal input of Isw2p-myc chromatin. Although this could be a consequence of differential myc tag accessibility, it might also suggest that Isw1p and Isw2p work in different ways, with Isw1p being associated with DNA more transiently.

Figure 3
(A) ChIP of DNA in regions of Isw1p- and/or Isw2p-dependent chromatin in yeast strains expressing Isw1/2p with C-terminal myc tags and analyzed by PCR. TOT lanes contain input chromatin and dilutions at 1:10 and 1:20. IP and NoAb lanes contain ChIP samples ...

The results presented above suggest that the chromatin structures we observe are a direct consequence of the action of Isw1p and/or Isw2p and that in vivo Isw1p and Isw2p both use their transdisplacement activity to move nucleosomes into specific positions. Given that the chromatin structures we have described all occur in potential regulatory DNA, we next asked whether the changes are a cause or consequence of changes in gene expression.

ISWI-dependent gene expression

Under identical growth conditions to those used to analyze chromatin structure, the isw mutant chromatin structures at INO1, PHO3, and Ty1 elements all correlate with a relative increase in expression: Figure Figure3B3B shows that basal levels of INO1 RNA are raised in isw2 and isw1 isw2 mutant yeast relative to wild type. Figure Figure3C3C shows that acid phosphatase activity in isw2 yeast is fivefold higher than in the wild-type and isw1 strains during growth in rich media. The activity of a PHO5 promoter-lacZ fusion reporter plasmid under identical growth conditions shows no increase in activity in isw2 yeast. Taken together with the repressed chromatin structures observed at PHO5 in Figure Figure1A,1A, this result suggests that the increased acid phosphatase activity in isw2 yeast is likely to derive from de-repression of PHO3. Interestingly, the pool of Ty1 transcript is more abundant only in the isw1 isw2 double mutant, which adds further support to the conclusion that both Isw1p and Isw2p function together at Ty1 δ chromatin. In contrast to INO1, PHO3, and Ty1 elements, the expression levels of DRS2 and FIG1 are not substantially perturbed in any of the isw mutants. The fact that DRS2 and FIG1 expression remains constant despite changes in chromatin structure suggests that the ISWI-dependent chromatin structures at these loci are a direct product of ISWI function rather than an indirect consequence of gene activation or repression. We also analyzed MNase cleavage patterns at INO1 during basal expression in rich media and after 23-fold induction on transfer into starvation/sporulation media (Fig. (Fig.3D).3D). On induction, a single MNase cleavage site normally present at −180 bp becomes protected, suggesting that transcription from INO1 is accompanied by a small change in chromatin structure. However, this change in MNase cleavage pattern is completely different from what we observe in the absence of Isw2p (Fig. (Fig.1C).1C). Thus, INO1 transcription per se does not produce the isw2 mutant chromatin structure.

The Isw1p- and Isw2p-dependent chromatin structures we observe suggest that remodeling activity is localized to short arrays of two or three nucleosomes rather than affecting general nucleosome position or large chromosomal domains. This result argues that Isw1p and Isw2p activity is targeted to particular DNA regions by one or more trans-acting factors. Drosophila ISWI, as part of the NURF complex, cooperates with GAGA factor to disrupt nucleosomes on the hsp70 promoter in vitro (Tsukiyama and Wu 1995). However, no GAGA-like factor appears to exist in Saccharomyces cerevisiae. We therefore analyzed DNA sequences underlying and flanking the ISWI-dependent regions of yeast chromatin for putative recognition sequences of DNA-binding proteins. Possible candidates included Cbf1p, Fkh1/2p, Pho2p, Ste12p, Thi2p, and Ume6p. The simplest model, in which a DNA-bound factor acts as a tether for either Isw1p or Isw2p, would predict that absence of either DNA-binding protein or remodeling ATPase will produce an identical alteration in chromatin structure. Of the DNA-binding proteins we tested, the absence of Ume6p produced exactly that result at the INO1 locus. A Ume6p-binding motif at INO1, termed URS1, is required for repression of the gene during vegetative growth (Jackson and Lopes 1996), a similar phenotype to isw2 yeast. Figure Figure4A4A shows that MNase cleavage pattern at INO1 in ume6 mutant yeast is identical to the isw2 pattern shown in Figure Figure1C.1C. A similar result was also obtained very recently at the REC104 promoter by Goldmark et al. (2000), who implicate Ume6p in the recruitment of Isw2p to early meiotic genes in yeast. However, MNase cleavage at PHO3, which is also Isw2p dependent, shows a wild-type pattern in the absence of Ume6p (Fig. (Fig.4B).4B). This result is recapitulated in a ChIP analysis (Fig. (Fig.4C,D):4C,D): ChIP of INO1 promoter DNA with Isw2p is abolished in ume6 mutant yeast, whereas ChIP of the PHO3 promoter is not. We conclude that Ume6p acts to recruit Isw2p to DNA at INO1 but not at PHO3. Ume6p is therefore not the only recruitment factor for Isw2p.

Figure 4
(A) Indirect-end-label analysis of MNase chromatin cleavage patterns at INO1 showing a chromatin structure that is Ume6p dependent. Analysis as described in Figure Figure1.1. A Ume6p-binding motif, termed URS1, is present at −193 bp. The ...

It has been shown previously that diploid isw2 yeast are unable to undergo meiosis (Trachtulkova et al. 2000), and recent work has confirmed that Isw2p functions to regulate early meiotic genes (Goldmark et al. 2000). Meiosis in yeast is a response to starvation. Several of the genes we have studied or that show changes in expression in isw mutant transcriptome analysis (Hughes et al. 2000) are not solely involved in meiosis but are regulated more widely by starvation. For instance, INO1 is induced in the absence of inositol and choline, and PHO3 by starvation for thiamine (Rogers et al 1982). We therefore looked for defects in other aspects of the starvation response in isw mutants. Figure Figure4E4E shows that both isw1 and isw2 mutant yeast exhibit enhanced haploid invasive growth (HIG) on rich media (Roberts and Fink 1994). Invading cells lacking Isw1p show an elongated morphology and polar budding, while the absence of Isw2p results in aberrant cell morphology (J. Mellor, unpubl.). The absence of Ume6p does not result in morphological changes or enhanced HIG (Fig. (Fig.4E;4E; data not shown), again suggesting that another recruitment factor exists for Isw2p. We conclude that the ISWI complexes in yeast regulate the developmental responses of yeast to starvation.

Materials and methods

Strains and media

For analysis of Isw1p- and Isw2p-dependent chromatin structures, two sets of isogenic strains were used: YTT166/W1588–4C (ISW1, ISW2), YTT186 (isw1::ADE2), YTT196 (isw2::LEU2), and YTT199 (isw1::ADE2, isw2::LEU2) were a gift from Toshio Tsukiyama (Tsukiyama et al. 1999). CEN.PK2-1D (ISW1, ISW2) and CEN.KR9-6C (isw1::KanMX) are EUROSCARF strains. CEN.RP2 (isw2::URA3) and CEN.RP1+2 (isw1::KanMX isw2::URA3), which are isogenic to CEN PK2-1D, were a generous gift from Raymond Poot and Patrick Varga-Weiss. For analysis of Ume6p-dependent chromatin, we used EUROSCARF strains YO3566 (ume6::KanMX) and its isogenic wild-type parent BY4741. Deletion of UME6 and C-terminal tagging of Isw1p and Isw2p with c-myc epitopes in the CEN.PK2 background was performed by gene replacement (Longtine et al. 1998). Primers are available from the authors. Rich media (YPD) contained 1% (w/v) Bactopeptone, 1% (w/v) yeast extract, and 2% (w/v) D-glucose, and yeast were grown at 29°C. Liquid cultures were harvested within a range of cell densities determined to represent mid-log/prediauxic shift phase. Haploid invasive growth was assayed as described by Roberts and Fink (1994) after growth of cells on YPD agar plates for 48 h.

In vivo chromatin analysis

Chromatin was digested with MNase in permeabilized yeast cells according to the general method of Kent et al. (1993) and Wu and Winston (1997), using the rapid sphaeroplasting modification described by Kent and Mellor (1995). Chromatin samples, each containing DNA from 2.0 × 108 cells, were digested with 75, 150, and 300 U/mL of MNase for 3 min at 37°C. Equivalent amounts of purified genomic DNA were digested with 10 U/mL MNase at 22°C for 40 sec to provide “naked” DNA controls. Further samples of purified DNA were cleaved with restriction enzymes and pooled in various combinations to provide marker digests. MNase-treated samples and marker mixes were digested to completion with appropriate restriction enzymes and analyzed by indirect-end-labeling (Wu 1980), as described by Kent et al. (1994). Experiments were repeated at least twice and in both isogenic strain backgrounds.


Probes were derived from DNA fragments amplified by PCR from yeast genomic DNA. PCR products were cleaved with appropriate restriction enzymes and gel purified before radiolabeling by random priming. Hybridization and washing of Southern and Northern blots was carried out in aqueous buffer as described by Kent et al. (1994).

Interpretation of MNase digests

Molecular weights of MNase cleavage products were assigned using One-Dscan (Scanalytics) based on the mobility of marker bands. Given the specificity of MNase for nucleosomal linker DNA, protection of a MNase cleavage site normally observed in purified DNA and replacement by two flanking chromatin-specific cleavage sites ~150 bp apart is taken to imply the presence of a translationally positioned nucleosome.

Northern analysis

RNA was isolated from 2 × 108 cell aliquots of cultures, grown under identical conditions to those used for chromatin analysis, using the RNeasy midi kit (QIAGEN), and processed according to the manufacturer's protocols. INO1 and FIG1 transcript was measured using RNA from YTT strains, and Ty 1 and DRS2 transcript using CEN.PK2 strains. Indirect-end-labels were used as probes where appropriate. The Ty 1 probe was a gift from Jef Boeke.

Enzymatic assays

Cells were assayed for acid phosphatase activity as described by Svaren et al. (1994). β-galactosidase activity was assayed as described by Hirst et al. (1994). The values for the assays are plotted as averages of three independent experiments each performed in duplicate. The PHO5-lacZ plasmid was made by PCR amplification of the region of PHO5 from the PmlI site at −250 bp to +258 bp, at which place a HindIII site was introduced. This fragment was fused in frame to lacZ introduced into pRS426 containing the PHO5 upstream sequences on an EcoRI (−2667 bp) to PmlI (−250 bp) fragment.

ChIP assays

ChIP was performed as described by Meluh and Broach (1999). Cultures were fixed in 1% formaldehyde for 2 h at room temperature. Chromatin from 3.0 × 108 cell equivalents was incubated for 15 h with (IP) or without (NoAb) anti-myc monoclonal antibody from clone 9E10 (Sigma) at a 1:200 dilution. NoAb and IP samples were resuspended in 40 μL for Isw1p–-myc analysis and in 150 μL for Isw2p-myc analysis. With primer pairs amplifying 300 bp, 5 μL aliqouts of DNA were analyzed by PCR. DNA from input chromatin (TOT) represents 0.5% of total with 1:10 and 1:20 dilutions. Products were fractionated on 1.5% agarose gels containing ethidium bromide and photographed in negative. Primer pairs amplify the following regions: INO1: −200 to +100 bp; PHO3: −120 to +180 bp; Ty δ at MET17: −1100 to −800; FIG1: −200 to +100; DRS2: +230 to +530.


We are grateful to Toshio Tsukiyama, Patrick Varga-Weiss, Raymond Poot, and Colin Goding for providing yeast strains and advice; Stephen Lee for photography; Nick Proudfoot for constructive criticism; and Anitha Nair for excellent technical help. This work was supported by The Wellcome Trust.

The publication costs of this article were defrayed in part by payment of page charges. This article must therefore be hereby marked “advertisement” in accordance with 18 USC section 1734 solely to indicate this fact.


E-MAIL ku.ca.xo.loiblom@tnekan; FAX 44-1-865-275297.

Article and publication are at www.genesdev.org/cgi/doi/10.1101/gad.190301.


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