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Centre for Functional Genomics, Institute of Molecular BioSciences, Massey University, Private Bag 11222, Palmerston North, New Zealand,1 Institute of Fundamental Sciences, Massey University, Private Bag 11222, Palmerston North, New Zealand2
Received 23 March 2005/ Returned for modification 6 June 2005/ Accepted 18 July 2005
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ABSTRACT |
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INTRODUCTION |
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Dosage compensation in Drosophila requires the ribonucleoprotein male-specific lethal (MSL) complex (1). The complex binds to hundreds of sites along the male X chromosome (17, 26). The core protein components are MSL1, MSL2, MSL3, MLE, and MOF. Loss-of-function mutations in any of the genes encoding these proteins lead to male-specific lethality, due to a failure in dosage compensatation (5, 20). A sixth protein, JIL1, preferentially associates with the male X chromosome and has been shown to coimmunoprecipitate with components of the MSL complex (21). Loss-of-function jil1 mutations are, however, lethal to both sexes, indicating a vital role for JIL1 in addition to X chromosome dosage compensation. The two noncoding RNA components of the complex, roX1 and roX2, share little sequence similarity but are genetically redundant and appear to be functionally interchangeable (32). The MSL complex does not assemble in females as one protein component, MSL2, is absent (4, 24, 47).
MSL1 plays a central role in assembly of the MSL complex (41). The amino-terminal domain of MSL1 binds to MSL2 (8, 41). We previously suggested that the interaction between MSL1 and MSL2 was via predicted amphipathic coiled-coil 
-helical regions that are found within the interacting domains (41). In addition, the carboxyl-terminal domain of MSL1 binds to both MSL3 and MOF (41). Subsequent studies have shown that MOF and MSL3 bind to adjacent regions in the MSL1 carboxyl-terminal domain (34). Further, formation of the MSL1/MSL3/MOF complex leads to a significant increase in the histone acetylase activity of MOF (34), which preferentially acetylates histone H4 at lysine 16 (2, 43). Both MSL3 and MOF have been shown to bind RNA nonspecifically in vitro and thus may have a role in incorporation of roX RNAs into the complex (3). Incorporation of MLE into the complex is presumably via interaction with the roX RNA, as MLE contains an RNA binding domain but does not appear to interact with any of the other protein components of the complex (8).
While progress has been made in understanding MSL complex assembly, how the complex specifically binds to hundreds of sites on the male X chromosome and then upregulates transcription so precisely remains poorly understood. One model for X chromosome binding is that the first step involves recognition of approximately 30 "high-affinity" or "chromatin entry" sites on the X chromosome by the MSL1/MSL2 dimeric complex (22). Additional binding to the high-affinity sites within the roX1 and roX2 genes requires MLE. Subsequently, the other components bind, and the complex then spreads along the chromosome to hundreds of other sites. One of the key observations that support this model is that the MSL1/MSL2 complex binds to the high-affinity sites in the absence of MSL3, MLE, or MOF (17, 27). MSL1 and MSL2, however, do not contain any of the well-characterized DNA binding domains (36, 47). We previously found that a deletion mutant of MSL1 that lacked the first 84 amino acids (aa) bound to MSL2, MSL3, and MOF but failed to bind to the X chromosome (41). This result suggested an important role for the amino-terminal region in X chromosome binding. Here, we show that a conserved basic segment at the amino terminus of MSL1 is essential for binding to the high-affinity sites on the X chromosome in the absence of endogenous MSL1. We also find that the adjacent region of MSL1 mediates MSL1 self-association. Lastly, we confirm the importance of the predicted coiled-coil region of MSL1 in binding to MSL2 and that this interaction is essential for binding of the amino-terminal region of MSL1 to the X chromosome.
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MATERIALS AND METHODS |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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The 0.8-kb NotI/XbaI fragment containing the HA tag was inserted into the NotI/XbaI sites of P transformation vector pCaSpeR-hs. Subsequently, this construct was used as a template for PCR to make the truncated and site-directed mutants. The sequences of the primers used to make these constructs and amplification conditions are available on request. The respective PCR fragments were digested with NotI/XbaI and inserted into pCaSpeR-hs. To make the MSL2 N terminus, PCR primers containing FLAG tag were designed. The PCR fragments were digested with EcoRI/XbaI and cloned to pCaSpeR-hs. All constructs were confirmed by DNA sequencing.
Multiple sequence alignments of MSL1 amino acid sequences were performed using Clustal W and then refined manually. Accession numbers for the sequences used are available upon request.
Fly crosses and transgenesis. Flies were grown at 25°C on standard cornmeal-yeast-sugar-molasses medium. To create homozygous msl1L60 female larvae that express MSL2 and MSL1NHA, P[MSL1NHA w+] y w; Bc/msl1L60 males were crossed to w; msl1L60; P[H83M2-6I w+] females. For other msl1 constructs, we first selected recombinants carrying the transgene and msl1L60. Recombinant y w/Y; P[MSL1NHAmut w+] msl1L60/Bc males were crossed to w; msl1L60; P[H83M2-6I w+] females. Homozygous msl1L60 female larvae were distinguished from their heterozygous siblings by the absence of the dominant black cell marker.
To make transgenic flies, plasmids were purified by CsCl-ethidium bromide gradient centrifugation and microinjected together with 
2,3 helper plasmid into y w embryos by standard procedures (40). Transgenics were identified due to expression of the white marker gene.
Immunofluorescent chromosome staining, immunoprecipitation, and Western blotting. Polytene chromosome squashes and immunostaining procedures were as described by Lyman et al. (27). Transgenic larvae were grown at 25°C. Primary rat anti-HA (Roche), rabbit anti-MSL2, and anti-MOF antibodies were used at a dilution of 1:50. Fluorescein isothiocyanate-conjugated rabbit anti-rat (Sigma) and Alexa Fluor-594-conjugated donkey anti-rabbit (Molecular Probes) secondary antibodies were used at a dilution of 1:600 and 1:1,000, respectively. DNA was counterstained with 4',6'-diamidino-2-phenylindole (DAPI).
To confirm protein expression of transgenic flies, adult flies were heat shocked at 37°C for 1 h, and then recovery took place at 25°C for 4 h. A protein extract was prepared, and Western blots were performed as described previously (41). For immunoprecipitation, approximately 50 heat-treated flies were homogenized in 1 ml of lysis buffer (50 mM Tris-HCl [pH 7.5], 300 mM NaCl, 2 mM EDTA, 1% NP-40) containing protease inhibitor (Roche). The homogenate was incubated for 30 min on ice and then centrifuged at 12,000 x g for 10 min at 4°C to remove debris. Protein concentration was determined by the Bradford method with a protein assay kit (Bio-Rad). A total of 0.7 mg of protein extracts was incubated with 25 µl of anti-HA affinity beads (Roche) at 4°C for 4 h with constant rocking. The beads were washed three times with washing buffer (20 mM Tris-HCl [pH 7.5], 150 mM NaCl, 2 mM EDTA, 1% NP-40). Bound proteins were mixed with sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) loading buffer, and Western blot analysis was performed.
In vitro transcription and translation; immunoprecipitation pulldown. DNA templates for in vitro transcription and translation were prepared from pCaSpeR-hs templates by PCR as described previously (41). Coupled in vitro transcription-translation reactions were performed with the TNT system (Promega) according to the manufacturer's instructions. For immunoprecipitation reactions, approximately 0.7 mg protein extract from transgenic flies that express MSL2NFLAG was incubated with anti-FLAG affinity beads (Sigma), and the beads were then washed extensively. A total of 4 µl of [35S]methionine-labeled in vitro-translated proteins was then mixed with the prebound beads in 200 µl of binding buffer (20 mM Tris-HCl [pH 7.5], 150 mM NaCl, 2 mM EDTA, 1% NP-40) containing protease inhibitor at 4°C for 4 h. The beads were washed four times with a high-salt binding buffer (containing 500 mM NaCl) and then once with standard binding buffer. Bound proteins were analyzed on 10% SDS-PAGE gels, followed by autoradiography.
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RESULTS |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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30 high-affinity sites. This is because the amino-terminal domain does not interact with MOF and MSL3, both of which are needed for the MSL1/MSL2 complex to bind to sites on the X chromosome other than the high-affinity sites (17, 37). However, we found that the HA-tagged amino-terminal domain of MSL1 (MSL1NHA) bound to hundreds of sites on the male X chromosome (Fig. 2C and D). Identical results were obtained if MSL1NHA expression was controlled by either the strongly heat-inducible hsp70 promoter (Fig. 2C and D) or the constitutive armadillo promoter (Fig. 2E). Further, we found that with the hsp70 construct, basal-level expression at 25°C was sufficient to detect X chromosome binding of MSL1NHA (Fig. 2D). Heat shock treatment to overexpress MSL1NHA did not lead to a significant increase in binding to the autosomes (Fig. 2C), nor did it disrupt X chromosome binding by other components of the MSL complex (data not shown). Since heat treatment was not necessary to detect X chromosome binding of MSL1NHA, all additional experiments in this study were performed with larvae raised at 25°C without heat shock. Surprisingly, daily heat-shock treatment of the progeny of an MSL1NHA line had little effect on male viability (85 male and 119 female progeny obtained), indicating that binding of MSL1NHA to the X chromosome did not significantly disrupt MSL complex activity. In contrast, we previously found that overexpression of a truncated version of MSL1 missing the first 84 amino acids that did not bind to the X chromosome was lethal to males (41). 84HA, which is identical to MSL1NHA but lacks the first 84 amino acids, did not bind to the male X chromosome (Fig. 2F). The lack of binding could be because the 84HA protein lacks a nuclear localization sequence. However, staining of whole salivary glands showed that 84HA was localized to the nucleus (Fig. 2H and I). Thus, the first 84 amino acids of MSL1 appear to play an essential role in X chromosome binding.
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84HA does not bind to the male X chromosome, we made three additional smaller deletion mutants to identify the region important for X chromosome binding. Like 84HA, 74HA did not bind to the male X chromosome (Fig. 4A). 50HA, however, bound very weakly to the male X chromosome in approximately 50% of the nuclei examined (Fig. 4B). In the other 50% of nuclei, no staining of the X chromosome with the anti-HA antibody could be detected above background levels. In contrast, 26HA bound more strongly to the X chromosome but with less intensity than MSL1NHA (Fig. 4C).
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26HA could bind to the X chromosome in a msl1 null mutant background. We found that there was no binding of 26HA to the X chromosomes in homozygous msl1L60 female larvae that expressed MSL2 (Fig. 5A). This demonstrates that the first 26 amino acids of MSL1 are essential for binding to the high-affinity sites. As discussed above, this region contains several well-conserved basic and aromatic amino acid residues. To test the importance of some of these conserved amino acids in X chromosome binding, we made two mutant versions of MSL1NHA. In mut_bas1, three of the conserved basic amino acids, lysine 3, arginine 4, and lysine 6, were all replaced by alanine. In a wild-type genetic background, this mutant version of MSL1NHA bound to hundreds of sites on the male X chromosome (data not shown). However, in the absence of endogenous MSL1, binding was restricted to only five of the high-affinity sites (Fig. 5B). Two of these sites mapped to the location of the roX genes, roX1 at 3F and roX2 at 10C. In the second mutation, mut_bas2, two of the conserved aromatic amino acids (phenylalanine 5 and tryptophan 7) were changed to alanine. This mutation did not appear to disrupt binding to the high-affinity sites in msl1L60 null female larvae that expressed MSL2 (Fig. 5C). However, mut_bas2 bound to significantly more autosomal sites than MSL1NHA. Thus, it appears that three of the conserved basic amino acids are essential for binding to most of the high-affinity sites. In addition, two of the conserved aromatic amino acids appear to be important for distinguishing X from autosomes, that is, the specificity of binding.
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26HA bound to these sites but 74HA did not indicated that the region between amino acids 26 and 74 is important for association with the MSL complex. This region is particularly rich in the amino acids glycine, proline, asparagine, and histidine in all Drosophila MSL1 proteins (Fig. 1). Glycine-rich domains are a common feature of many proteins including RNA binding proteins and can mediate protein-protein interaction (7, 11). The glycine-rich domain of the Drosophila Sex-lethal RNA binding protein, which is the master regulator of dosage compensation (38), promotes self-association (10). We therefore tested if the MSL1 glycine-rich domain would facilitate MSL1 self-association. We found that MSL1 coimmunoprecipitated from whole-fly protein extracts with MSL1NHA and 26HA but not 84HA, 74HA, or 50HA (Fig. 6A). There was a small variation in immunoprecipitation efficiency of the HA-tagged proteins, which were also detected with the MSL1 antibody (Fig. 6A). However, this was not sufficient to account for the lack of coimmunoprecipitation of MSL1 with the more truncated versions of MSL1NHA. MSL2 was not required for MSL1 self-association, as protein extracts were prepared from adult females, which normally do not make MSL2 protein. 26HA did not coimmunoprecipitate with MSL3 (Fig. 6B), showing the specificity of the interaction of 26HA with MSL1 (Fig. 6A, lane 10). Deletion of the first 84 amino acids did not, however, disrupt interaction with MSL2 (Fig. 6C), confirming previous studies (8, 41). Thus, MSL1NHA appears to interact with the native MSL complex via MSL1 self-association.
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-helix at the amino terminus of MSL2 to form a coiled-coil structure (41). Likely orthologs of MSL1 and MSL2 have been identified from invertebrate and vertebrate genome sequences (29). Amino acid sequence alignments of MSL1 and MSL2 orthologs showed a high degree of conservation of the predicted -helical regions (Fig. 7A and B). Inspection of the alignments showed that both MSL1 and MSL2 proteins contained a highly conserved region that is largely apolar and precedes the coiled coil. For MSL1, a glutamine-rich spacer separated the apolar and coiled-coil regions. Alanine substitution mutations were made in the apolar, glutamine-rich, and leucine zipper-like regions of MSL1 to investigate the relative importance of these regions in dimerization with MSL2 (Fig. 7C).
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Dimerization of coiled-coil proteins is driven by interaction between apolar side chains in the a and d positions of the -helix. The binding is enhanced by ionic interactions between charged amino acids in the e and g positions. Consequently we made alanine-substitution mutations in the a, d, e, and g positions in the leucine zipper-like motif that follows the glutamine-rich region. We found that all of the mutant versions of MSL1NHA coimmunoprecipitated with MSL2NFLAG (Fig. 7D, lanes 11, 13, 15, and 17). However, there appeared to be significantly less coimmunoprecipitation of two of the mutations, mut_cc1 and mut_cc2, with MSL2NFLAG (Fig. 7D, lanes 11 and 13). The efficiency of immunoprecipitation of MSL2NFLAG was similar for all four coiled coil mutant preparations (Fig. 7E, lanes 11, 13, 15, and 17). These results suggest that the mut_cc1 and mut_cc2 alanine substitution mutations have weakened the interaction between MSL1 and MSL2.
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DISCUSSION |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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30 high-affinity sites on the male X chromosome. Consistent with this possibility, we found that replacement of three of the conserved basic amino acids at positions 3, 4, and 6 by alanine eliminated binding of the amino-terminal region of MSL1 to all but five of the high-affinity X chromosome binding sites. Two of the five sites mapped to the location of the roX genes (roX1 at 3F and roX2 at 10C). It is possible that binding to these sites could be via association with the RNA components of the complex rather than via DNA recognition. Two conserved aromatic amino acids in the basic region appear to be important for binding specificity, as alanine substitution led to increased binding to the autosomes. Aromatic and nonpolar amino acids in the basic domain of bZIP protein C/EBP are important for DNA recognition and binding specificity, respectively (33). Investigating these possibilities will require in vitro binding studies with DNA sequences from the three high-affinity sites that have been identified. It is also possible that the amino terminus of MSL1 could bind RNA, as several proteins bind to RNA via basic-rich motifs (30). If so, the MSL1/MSL2 complex would associate with the nascent RNA of genes transcribed within the high-affinity sites. However, binding of MSL1 to the X chromosome is not disrupted by RNaseA treatment (6). This suggests that it is more likely that the MSL1/MSL2 heteromeric complex recognizes DNA sequences within the high-affinity sites.
Role of the conserved apolar region of MSL1 in binding to MSL2.
bZIP and basic helix-loop-helix proteins bind to DNA as dimers with bZIP dimers, forming coiled coil structures. Coiled coil domains contain a heptad repeat of the form (a-b-c-d-e-f-g)n, where positions a and d are commonly occupied by apolar residues (16). Oligomerization then occurs through the formation of a multistranded, -helical coiled coil in which a and d residues become internalized and hence shielded from the aqueous environment. We previously proposed that the short heptad substructures observed in the sequences of both MSL1 and MSL2 (residues 128 to 143 and 25 to 40, respectively) could provide a simple means by which chain dimerization could be effected in vivo (41). Here, we identified highly conserved apolar regions that lay immediately N terminal to the heptad motif in both chains (residues 113 to 121 and 5 to 14, respectively). Alanine substitution of four amino acids in the MSL1 apolar region eliminated binding to MSL2 in vitro and in vivo. A possible explanation for the critical importance of the MSL1 apolar region is that this acts as a trigger motif that facilitates coiled-coil formation. In the case of long heptad-containing regions, trigger motifs are sometimes used in the sequence to provide a short length of highly stable coiled coil that acts as a nucleating point for subsequent coiled-coil formation (23, 44). For short lengths of coiled coil, however, other features may play an important role in either stabilizing or facilitating the formation of coiled-coil structure (13). If the apolar region of MSL1 does serve as a trigger for dimerization, then the first turn of the -helix would be expected to be important in zipping together the two proteins. Consistent with this suggestion, we found alanine substitution of the first two apolar amino acids in the a position and of the charged amino acids in the e and g positions of the first heptad decreased binding to MSL2 in vitro. It should also be noted that the RING finger domain of MSL2, which immediately follows the short heptad motif, is also important for binding to MSL1 (8).
Significance of MSL1 self-association mediated by the glycine-rich motif.
Remarkably we found that the amino-terminal domain of MSL1 lacking the basic motif (26HA) bound to all sites on the male X chromosome. This appears to be because 26HA binds to full-length MSL1 incorporated into the complete MSL complex. We found that a glycine-rich region between the basic and coiled-coil motifs facilitated MSL1 self-association in vitro and binding to the MSL complex in vivo. The glycine-rich and leucine zipper-like motifs appear to function independently, as MSL1 self-association does not require MSL2 and deletion of the glycine-rich motif (e.g., 84HA) does not disrupt binding to MSL2. However, binding to the MSL complex in vivo does require interaction with MSL2, as a mutation (mut_apo) that disrupted binding of MSL1 to MSL2 in vitro also eliminated binding to the male X chromosome, despite containing a complete glycine-rich motif. An explanation for these observations is that the MSL1NHA:MSL2 heterodimer binds to sites on the X chromosome immediately adjacent to sites occupied by the endogenous MSL complex and that the binding is stabilized by association of MSL1NHA with MSL1 in the complex. The 18D10 high-affinity site appears to consist of a cluster of sites of intermediate or weak affinity for the MSL complex (35). It is likely that stable binding to the X chromosome involves some cooperativity between MSL complexes bound to adjacent sites of differing affinity. MSL1 self-association may then be important in cooperative binding of MSL complexes to the male X chromosome, but testing this proposal will require evaluation of a series of alanine substitution mutations within the glycine-rich region. Alternatively, our results do not preclude the possibility that MSL1NHA is recruited to the male X chromosome by interaction with both MSL2 and MSL1 in prebound MSL complex. Interaction with MSL1 in the complex must also be necessary, as 84HA does not bind to MSL1 or male X chromosome, yet binds to MSL2.
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ACKNOWLEDGMENTS |
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This work was supported by a Massey University postdoctoral fellowship to F.L.
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FOOTNOTES |
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REFERENCES |
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