Corto and DSP1 interact and bind to a maintenance element of the Scr Hox gene: understanding the role of Enhancers of trithorax and Polycomb
© Salvaing et al; licensee BioMed Central Ltd. 2006
Received: 13 February 2006
Accepted: 14 April 2006
Published: 14 April 2006
Polycomb-group genes (PcG) encode proteins that maintain homeotic (Hox) gene repression throughout development. Conversely, trithorax-group (trxG) genes encode positive factors required for maintenance of long term Hox gene activation. Both kinds of factors bind chromatin regions called maintenance elements (ME). Our previous work has shown that corto, which codes for a chromodomain protein, and dsp1, which codes for an HMGB protein, belong to a class of genes called the Enhancers of trithorax and Polycomb (ETP) that interact with both PcG and trxG. Moreover, dsp1 interacts with the Hox gene Scr, the DSP1 protein is present on a Scr ME in S2 cells but not in embryos. To understand better the role of ETP, we addressed genetic and molecular interactions between corto and dsp1.
We show that Corto and DSP1 proteins co-localize at 91 sites on polytene chromosomes and co-immunoprecipitate in embryos. They interact directly through the DSP1 HMG-boxes and the amino-part of Corto, which contains a chromodomain. In order to search for a common target, we performed a genetic interaction analysis. We observed that corto mutants suppressed dsp1 1 sex comb phenotypes and enhanced Antp Scx phenotypes, suggesting that corto and dsp1 are simultaneously involved in the regulation of Scr. Using chromatin immunoprecipitation of the Scr ME, we found that Corto was present on this ME both in Drosophila S2 cells and in embryos, whereas DSP1 was present only in S2 cells.
Our results reveal that the proteins Corto and DSP1 are differently recruited to a Scr ME depending on whether the ME is active, as seen in S2 cells, or inactive, as in most embryonic cells. The presence of a given combination of ETPs on an ME would control the recruitment of either PcG or TrxG complexes, propagating the silenced or active state.
Many transcription factors are expressed only transiently during development. After they have disappeared, the patterns of gene expression they have induced must be inherited by daughter cells. In eukaryotes, two groups of proteins, the Polycomb-group (PcG) and the Trithorax-group (TrxG), fulfil this memory function. Their existence was first revealed in Drosophila melanogaster where homeotic gene (Hox) expression is established in early embryos by the transient Gap and Pair-Rule transcription factors and controlled by PcG and TrxG proteins during the rest of development [1–3]. The PcG and TrxG proteins combine into several heteromeric complexes that bind chromatin. PcG complexes maintain Hox gene silencing whereas TrxG complexes counteract the action of PcG complexes (reviewed in ). These proteins regulate many other genes such as engrailed [5, 6], ph , fork head  and the iroquois-complex .
In Drosophila, at least two PcG complexes called PRC2 and PRC1 (Polycomb Repressive Complex) and two TrxG complexes (TAC 1 and BRM) have been biochemically purified (reviewed in ). The PRC1 complex contains the PcG proteins Polycomb (PC), Polyhomeotic (PH), Posterior Sex Combs (PSC) and dRING1, and additional polypeptides such as the DNA binding protein Zeste [11, 12]. The PRC2 complex contains the PcG proteins Extra Sex Combs (ESC), SU(Z)12 and Enhancer of Zeste (E(Z)), a histone methyltransferase that methylates lysine 27 of histone H3 (H3K27me3), and the histone binding protein p55 [13, 14]. PC is also found in another complex that contains the DNA binding protein Pipsqueak , ESC and E(Z) are found in a larger complex that contains Polycomb-like (PCL), the histone deacetylase RPD3 and p55 , and E(Z) is found in a complex that contains the deacetylase SIR2 . The TrxG complex TAC1 contains CBP, a member of the CBP/p300 histone acetyl tranferase (HAT) family, the anti-phosphatase SBF1, and the TrxG protein TRX, which is homologous to mammalian MLL/ALL and methylates histone H3 on lysine 4 (H3K4me) [18–20]. Lastly, the BRM complex contains the TrxG proteins BRM, Osa and Moira. It is related to the yeast SWI/SNF ATP-dependent chromatin remodeling complex, sharing four polypeptides with it, among which is the ATPase BRM . It also contains BAP111, an HMGB protein that binds nonspecifically in the minor groove of the double-helix, thus bending the DNA [22, 23].
In Drosophila, the PcG and TrxG proteins bind overlapping sequences called Polycomb/Trithorax Response Elements (PRE/TREs) (reviewed in ). Two PRE/TREs (Fab-7 and the Hedgehog PRE/TRE) have been demonstrated to be true maintenance elements (ME), i. e. to control the maintenance of activation or repression of target loci through cell division [24, 25]. A major issue is to understand how PcG and TrxG complexes are specifically recruited to ME. On the one hand, the specific recruitment of these complexes could be achieved by recognition of posttranslationally modified histone tails. For example, PC recognizes K27 methylation of H3 via its chromodomain. Hence, PRC1 may be recruited to chromatin by the recognition of the H3K27me3 mark laid down by PRC2 through E(Z) . Furthermore, the methyl-transferase activity of E(Z) is required for correct repression of Hox genes, suggesting that this histone modification is actually related to gene regulation . On the other hand, DNA binding proteins such as Zeste, GAF (GAGA factor), PHO (Pleiohomeotic), the HMG-box protein DSP1 (Dorsal Switch Protein 1) and Pipsqueak, which are present at some ME, also seem to be involved in the specific recruitment of PcG and TrxG [15, 27–31]. Indeed, their various combinations and associations with co-factors could make complex binding more specific.
In a large screen to identify modifiers of trxG mutations, 6 genes previously identified as PcG genes (Asx, E(z), E(Pc), Psc, Scm and Su(z)2) were isolated as enhancers of trxG phenotypes . The authors suggested that the corresponding genes be renamed "Enhancers of trithorax and Polycomb" (ETP) to account for their role both in repression and activation of Hox genes. Further studies identified other ETP proteins, among which is GAF [29, 33], or PHO, which directly binds a PC-containing complex as well as the BRM complex . The chromodomain protein Corto [35, 36] and the HMGB protein DSP1  also behave as ETP. Indeed, a loss-of-function allele of corto enhances the macrochaete phenotype of the trxG gene osa as well as the Polycomb phenotype of the PcG genes mxc, Pc, Pcl, ph and the ETP genes E(z) and Scm [35, 38]. On the other hand, a dsp1 null allele enhances the haltere to wing transformation of several trxG mutants ash1, brm, osa, trx), whereas male hemizygotes for this allele exhibit transformation of the A4 segment into a more posterior one, which is a Polycomb phenotype . Thus, dsp1 also behaves like an ETP. To date, little information regarding the mode of action of ETP has become available. No ETP has yet been found in TrxG complexes. Some of them belong to PcG complexes (such as E(Z), PSC and SCM) but most of them (such as ASX, Corto, GAF and SU(Z)2) have not been found in PcG complexes to date. However, in embryonic extracts, Corto co-immunoprecipitates with ESC and PC, while SU(Z)2 and GAF co-immunoprecipitate with PC, suggesting that these ETPs can transiently interact with PcG complexes [29, 36, 39]. How ETPs promote either the activation or the repression of a defined target gene is an open question.
To understand better the role of ETP, we analyzed the interaction between Corto and DSP1. We show that both proteins co-localize at 91 sites on Oregon-R polytene chromosomes. These include 84B, which corresponds to the distal part of the ANTP-complex. In addition, Corto and DSP1 co-immunoprecipitate in embryonic extracts and directly interact through the HMG-boxes of DSP1. Moreover, we show that the corto and dsp1 genes interact and that corto, like dsp1, is directly involved in the regulation of the Hox gene Scr. Chromatin immunoprecipitation experiments indicate that Corto, like DSP1, localizes on a 10 kb-XbaI ME of the Scr cis-regulatory sequences. On the basis of our results, we propose that both proteins interact on chromatin to regulate a subset of common targets including Scr.
DSP1 and Corto co-localize on polytene chromosomes
To examine whether DSP1 plays a role in Corto recruitment, we looked at the localization of Corto in the dsp1 1 homozygote mutant strain, which is devoid of DSP1 protein . No modification of Corto binding sites was observed in this strain, indicating that the DNA-binding protein DSP1 is dispensable for Corto recruitment to chromatin (Figure 1D–E).
DSP1 and Corto are parts of a common complex in embryos and interact directly
The reverse experiment, i. e. migration and transfer of the GST-Corto fusion proteins incubated with radiolabeled DSP1, gave no conclusive results owing to the difficulty in renaturing Corto. We showed previously that the only noticeable domain of the 550 amino acid Corto protein is a chromodomain located in the NH2-terminal half (aminoacids 107 to 203) . In order to characterize the Corto domains interacting with DSP1, we performed GST pull-down experiments using full-length or truncated forms of Corto fused to GST and radiolabeled full-length DSP1. The results are shown in Figure 4B. DSP1 was retained by the full-length Corto protein, corroborating the far-western results with DSP1. Moreover, DSP1 was retained by a GST fusion protein containing the NH2-terminal half of Corto (GST-C1/324), but was not detectably retained on the COOH-terminal half (GSTC325/550 and GST-C440/550). Interestingly, DSP1 was not retained on the Corto chromodomain (GST-C127/203).
Taken together, these results indicate that, in vitro, DSP1 and Corto directly interact through either the HMG-box A or the HMG-box B of DSP1 on the one hand, and the amino-terminal half of Corto on the other.
corto and dsp1 interact genetically and participate in Sex comb reduced (Scr)regulation
Genetic interactions between dsp1 and corto
average sex comb teeth on the T1 leg
A6 to A5 (%)
dsp1 1 /Y ; +/+
+/Y; corto 420 /+
+/Y; corto 07128 /+
dsp1 1 /Y; corto 420 /+
dsp1 1 /Y; corto 07128 /+
Genetic interactions between corto and Scr
T2 to T1 (%)
Antp Scx /+
Antp Scx /corto 420
Antp Scx /corto 07128
Antp Scx /corto L1
Corto and DSP1 bind the same region within the 10-kb XbaI fragment of the Scrregulatory sequences
We report in the present work that the two ETPs corto and dsp1 interact genetically and that the proteins they encode (i) directly interact in vitro, (ii) co-immunoprecipitate in embryos and (iii) co-localize on 91 sites in salivary gland polytene chromosomes. These results suggest that the proteins are simultaneously involved in the regulation of several target genes. DSP1 can bind Corto through one of the two HMG-boxes that also mediate DNA binding. It has been suggested that during nucleoprotein complex formation, the HMG-box B of HMGB bends DNA whereas the HMG-box A mediates interaction with transcription factors, thus promoting their contact with targets . DSP1 seems to follow that scheme to enhance the binding of transcription factors as Dorsal or Bicoid to DNA [42, 43]. What therefore could be the role of the DSP1-Corto interaction in the regulation of common targets? First, DSP1 could bring Corto to the chromatin, where it could further interact with other partners. These partners could be PcG factors or GAF, which have previously been shown to interact with Corto . Nevertheless, this hypothesis is unlikely since we observed no modification of Corto binding to polytene chromosomes in the dsp1 1 strain. Second, DSP1 could inhibit the interaction between Corto and PcG factors or GAF, thus preventing the silencing of targets that bind both proteins. Third, Corto could modify the DNA bending ability of DSP1 and thus modulate its interaction with other factors, for example TrxG complexes. Indeed, the dsp1 gene was previously shown to interact with the TrxG genes trx and brm  Our results do not allow us to discriminate between these last two, non-exclusive possibilities.
We also report that the Hox gene Scr is a common target of Corto and DSP1. Both proteins bind a 10-kb XbaI fragment located 37-kb upstream of the Scr transcription start. Genetic studies have shown that this fragment is required for Scr function in the embryo and in the imaginal disc [44–46]. In embryos, it restricts the expression of a Scr-lacZ fusion gene to the labial and prothoracic segments , whereas in larvae it is required for Scr expression in the first leg imaginal disc and for Scr silencing in the second and third leg imaginal discs . Interestingly, the function of the 10-kb XbaI fragment is sensitive to a subset of PcG and TrxG mutations  and has been genetically characterized as an upstream maintenance element of Scr . At the end of embryogenesis, the Scr expression domain is restricted to the labial and prothoracic segments. In consequence, the mean state of this ME in the whole embryo would be silenced. We can thus assume that the global situation in embryos mimics that of the T2 and T3 leg imaginal discs. Conversely, since Scr is expressed in S2 cells (data not shown), we propose that the situation in S2 cells rather mimics that of T1 leg imaginal disc cells. Hence, Corto, which is present on the Scr ME whether active (S2 cells) or silenced (embryos), could be present on this ME in all three leg imaginal discs. On the other hand, DSP1, which is present on the ME in S2 cells but not in embryos, could bind the ME only in cells where this element is active, hence in T1 leg imaginal disc cells. We thus propose that both Corto and DSP1 proteins localize on this Scr ME in the first leg imaginal disc.
Some trxG mutants as well as the dsp1 null mutant exhibit a reduced sex comb and our previous work has shown that dsp1 interacts with certain trxG genes and regulates Scr expression in T1 discs [2, 37]. HMGB, the vertebrate homologue of DSP1, has been reported to activate and stabilize the TFIID-TFIIA-promoter complex in vitro  and some TrxG factors have been shown to interact with the RNA polymerase II complex, thus facilitating transcriptional elongation [49, 50]. This leads us to propose that in the T1 leg imaginal disc, DSP1 facilitates the interaction between a TrxG complex and the transcription machinery, thus maintaining Scr activation. Moreover, Corto has been shown to interact with PcG complexes . The binding of Corto to DSP1 could then impede the interaction between Corto and PcG complexes, thus limiting their recruitment. Therefore, the interaction between the two proteins on the ME would lead to a level of Scr transcription compatible with T1 identity. Conversely, in the T2 and T3 leg imaginal discs, since DSP1 does not bind the ME, Corto would be able to interact with PcG complexes, thus enhancing the silencing of Scr.
In summary, we have shown that the two ETPs Corto and DSP1 directly interact and are simultaneously found on a Scr ME when active, whereas Corto alone is found on the same ME when inactive. Our data suggest that different combinations of ETP favor the recruitment of either PcG or TrxG complexes, participating in the maintenance of the silenced or active state of ME.
Drosophila strains and genetics
Flies were raised on standard medium at 25°C except for the dsp1 strain, which was maintained at 22°C. All mutations and chromosome aberrations used are described in Flybase . Oregon-R or w 1118 were used as wild-type reference strains. dsp1 1 is a null allele of dsp1, which is maintained as a homozygous strain . corto 420 , corto 07128 and corto L1 are loss-of-function alleles: a deficiency, a P-element insertion and an uncharacterized mutation obtained by EMS mutagenesis, respectively. These alleles were balanced over TM3.
Localization of proteins on polytene chromosomes
Co-immunostaining of Oregon-R or dsp1 1 polytene chromosomes was performed as previously described using rabbit affinity purified anti-DSP1 (1:150) and rat anti-Corto (1:40) as primary antibodies . Secondary antibodies (Alexa Fluor® 594 goat anti-rabbit IgG and Alexa Fluor® 488 goat anti-rat IgG, Molecular Probes) were used at a 1:1000 dilution. To determine the precise localization of Corto and DSP1, immunostainings were performed separately on squashes of Oregon-R chromosomes using rabbit affinity-purified anti-DSP1 (1:150) or rabbit anti-Corto (1:40) as described .
Embryos (0–14 hour-old w 1118 , 2 g) were crushed in 4 ml of 50 mM Tris pH 7.5, 150 mM NaCl, 1% NP40, 0.1% SDS, 1 mM PMSF supplemented with protease inhibitors (Roche). After sonication and high-speed centrifugation, the extracts were pre-cleared with protein A-agarose beads and incubated overnight at 4°C with 10 μg of anti-DSP1 affinity-purified antibodies or 10 μl of rabbit serum. Following extensive washing, the beads were resuspended in Laemmli buffer and analyzed by SDS-PAGE and western blotting.
Far-western and GST pull-down assays
Most of the vectors expressing full-length or truncated forms of MBP-DSP1 or GST-Corto fusion proteins have been described previously [36, 37]. pGEX-C1/324 was obtained by digestion of pEG-Corto with EcoRI and PvuII and sub-cloning the resulting 1-kb fragment into pGEX4T-1. pGEX-C325/550 was obtained by PCR amplification of a 0.7 kb DNA fragment from pBS-Corto using oligonucleotides 5'-CCG GAA TTC CGG GCT GCG GCC CAG GCC TCG ATA GCC-3' and 5'-CCG CTC GAG CGG CAC GTT GTA GCA GGA GAT CTG CGG-3', digestion with EcoRI and XhoI, and sub-cloning into pGEX4T-1. In vitro synthesis of radiolabeled proteins was performed using the TNT® coupled reticulocyte lysate system (Promega) and 35S methionine. Far-western and GST pull-down assays were performed as previously described [36, 37].
Immunoprecipitation of crosslinked chromatin (XChIP) and semi-quantitative PCR analysis
Formaldehyde cross-linking of Drosophila S2 cell or 0–14 hour-old w 1118 embryo chromatin and chromatin immunoprecipitation were performed as described . Immunoprecipitation of purified chromatin was performed either with rabbit Corto antibodies (1:20), affinity-purified DSP1 antibodies (5 μg) or rabbit serum (1:20) in 250 μl final volumes. One percent of the co-immunoprecipitated DNA was used for the PCR reactions. Nine primer pairs amplifying 500–700 bp fragments in the cis-regulatory sequences of Scr (NCBI accession number: NT_033777) were designed: SL forward 5'-AAA TCG GAC TGC TGC AAT TGA AGG-3', reverse 5'-AAT CCA AAA TGT TAC CCG GTG GCC-3', S1 forward 5'-GCA TCA AAA ACG AGT TAA GG-3', reverse 5'-ATA AAT CTT AGC TGC CTG CG-3', S2 forward 5'-CGC AGG CAG CTA AGA TTT ATG G-3', reverse 5'-CCG TTT GGG ATA AAC TTG GG-3', S3 forward 5'-GTT CCC AAG TTT ATC CCA AAC G-3', reverse 5'-GCT GAG GAG AAA GCT TCT GG-3', S4 forward 5'-CCA GAA GCT TTC TCC TCA GC-3', reverse 5'-CGG TAG CTG ATT TCG GAA AG-3', S5 forward 5'-CTT TCC GAA ATC AGC TAC CG-3', reverse 5'-TAT TTC CTC TCG AAC CCA CG-3', S6 forward 5'-GAG AGG AAA TAT GCA CTG GC-3', reverse 5'-GAA CGG ATC CAA ACC AAA CC-3', S7 forward 5'-AAA AGC TCT GAA AGT GTT AAG TGG C-3', reverse 5'-AAT GGC CCG AAT GAA GAA GC-3', and SR forward 5'-TCT ATC GTT CGG TTC AAT GGC TCC-3', reverse 5'-TTG GAA AAT GCC CAG CAG ACA TCC-3'. The PCR schemes were as follows: 94°C for 3 min; 94°C for 1 min, 57°C (S3, S6), 58°C (S4), 59°C (S1), 60°C (SL, S2, S5, S7, SR) for one min, 35 times, 72°C for one min; 72°C for 10 min. PCR samples were taken at the 29th, 31st, 33rd and 35th cycles to ensure that quantifications were performed in the linear range. PCR gels were photographed with a Biorad Geldoc system and quantified using ImageJ software (NIH). The results were normalized against the mock immunoprecipitation and presented as percentages of input DNA.
The authors wish to thank Valérie Ribeiro, Nicole Salmon and Andrée Soulas for excellent technical assistance, and Sébastien Bloyer, Jean-Michel Gibert and Neel Randsholt for fruitful discussions and careful reading of the manuscript. JS was supported by fellowships from the Ministère de la Recherche and from Association pour la Recherche contre le Cancer. This work was supported in part by Ligue Locale 41 contre le Cancer and Fondation pour la Recherche Médicale to DL and MD.
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