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Genomics. Author manuscript; available in PMC Feb 1, 2010.
Published in final edited form as:
Genomics. Feb 2009; 93(2): 152–158.
Published online Nov 8, 2008. doi:  10.1016/j.ygeno.2008.09.013
PMCID: PMC2668202
NIHMSID: NIHMS95192

YY1's longer DNA-binding motifs

Abstract

The DNA-binding sites of YY1 located within two newly identified downstream genes of YY1, Peg3 (GGCGCCATnTT) and Xist (CCGCCATnTT), are longer than the known motif of YY1 (CGCCATnTT). Gel shift assays indicated that these DNA-binding sites are previously unnoticed, longer motifs of YY1. Independent DNA-binding motif studies further confirmed that YY1 recognizes a longer sequence (GCCGCCATTTTG) as its consensus motif. This longer motif exhibited higher affinity to the YY1 protein than the known motif. Another DNA-binding motif study was also performed using a protein containing three amino acid substitutions in the first zinc finger unit of YY1, mimicking the zinc finger domain of Pho (a drosophila homologue of YY1). The substitutions caused the weakening of DNA-binding specificity at both 5′- and 3′-sides of the longer motif, yielding a much shorter sequence (GCCAT) as a consensus motif. This indicates that the intact first finger unit is required for recognition of the longer motif of YY1. Also, this shortening suggests that the DNA recognition by YY1 is mediated through the concerted, but not modular, contribution by its four zinc finger units.

Keywords: YY1, DNA-binding motifs, Peg3, Xist

Introduction

The mammalian transcription factor YY1 is a ubiquitously expressed, multifunctional protein that can function as an activator, repressor, or initiator binding protein [1-4]. YY1 controls the transcription of a large number of genes and also interacts with various protein partners, including coactivators, corepressors, and other transcription factors. Recent studies reported that YY1 is involved in many important processes, such as embryonic development, cell cycle progression, oncogenesis, genomic imprinting, and X chromosome inactivation [5-9].

YY1 contains four C2H2-type zinc finger units at its C-terminal region, and the structure of YY1 bound to one of its binding sites, the P5 initiator of the AAV (Adeno-Associated Virus), was revealed by X-ray crystallography [10]. The DNA-binding motifs of YY1 were determined through PCR-based selection of randomized sequences with both bacterially expressed and partially purified endogenous proteins of YY1 [11, 12]. The consensus motif derived from each study is similar to the confirmed binding sites of YY1 that are located within several promoters [13, 14]. We also identified multiple YY1 binding sites that are located within the critical regions of the Peg3 and Xist imprinted domains [7, 15]. Interestingly, these binding sites turn out to be longer than the previously known DNA-binding motifs of YY1.

In the current study, we have further characterized the longer DNA-binding motifs of YY1 located within Peg3 and Xist in terms of their functional significance and affinity to the YY1 protein. According to DNA-binding motif studies, these longer motifs are indeed previously unrecognized DNA-binding sites of YY1 and the extension of the YY1 motifs appears to increase their binding affinity to the YY1 protein. Also, the first finger unit of the YY1 protein is responsible for recognizing the extended portion of the longer motifs.

Results

Identification of the longer DNA-binding motifs of YY1 in the Peg3 and Xist domains

The imprinting control regions of Peg3 and Xist contain unusual tandem arrays of YY1 binding sites, which are well conserved among different mammalian species. These conserved YY1 binding sites are slightly longer than the known consensus motif of YY1: GGCGCCATnTT for Peg3 and CCGCCATnTT for Xist vs. CGCCATnTT for the known consensus (n means any base). To further characterize the significance of these longer sites, we analyzed the genomic sequences of the first intron of Peg3 in 6 different species of mammals: human, chimp, mouse, cow, rhesus and dog. As shown in Fig.1A, 9 to 14 YY1 binding sites are localized within a 4-kb interval in the genome of each species. One motif (GGCGCCATnTT) appears to be the dominant form within each species. This motif corresponds to 30% of the YY1 binding sites in human, rhesus and chimp, and about 70% in mouse, cow and dog. Even some of the other variant YY1 binding sites appear to have been derived from this dominant motif since they contain one base change at the CpG dinucleotide site, either as TpG or CpA. In particular, 4 to 5 binding sites from human, chimp and rhesus show this type of mutational change. The change of CpG to either TpG or CpA in mammalian genomes frequently occurs due to the DNA methylation and subsequent deamination of the cytosine base. This is consistent with the fact that the Peg3 is an imprinted gene, one allele of which is always repressed by DNA methylation.

Figure 1Figure 1
Evolutionary conservation of multiple YY1 binding sites in the Peg3 and Xist regions

We also analyzed the longer form of YY1 motifs found in Xist using the genomic sequences derived from 5 mammalian species, including human, mouse, cow, horse and rabbit. As shown in Fig.1B, 3 to 10 binding sites of YY1 are found in the 700-bp genomic region of the second promoter of Xist. About half of the total YY1 binding sites derived from the five species correspond to one type of motif (CCGCCATnTT). Notably, all of the three YY1 binding sites in mouse Xist are the same motif (CCGCCATnTT) and two sites contain an additional G at their 5′-ends (GCCGCCATnTT). In sum, the genomic regions of Peg3 and Xist both contain evolutionarily conserved YY1 motifs that are slightly longer than the known consensus motif.

Higher levels of DNA-binding affinity by the longer motifs of YY1

Several studies have already performed independent DNA-binding motif analyses using PCR-based selection schemes with randomized oligonucleotides. However, these studies did not yield sequence information beyond the CpG site of the binding motif (CGCCATnTT) due to the following reason. A CpG nucleotide was accidentally included as part of the non-randomized vector region, and yet all of the selected sequences used this CpG site as part of their YY1 binding sites. Thus, the sequence information beyond the CpG site could not be derived in these studies [11, 16]. To circumvent this problem, we have used a slightly modified randomized oligonucleotide: CGT(N)7CC(N)7ACG. Thymine and adenine bases were inserted into the left and right border regions, respectively, between the flanking vector regions and the middle randomized portion of the oligonucleotide. We have also positioned two prefixed cytosine bases, CC, in the middle of the randomized portion since the core DNA-binding motif of YY1 contains two cytosines (CCAT). This scheme was designed to ensure a potential YY1 binding site to be localized in the middle of the oligonucleotide, which would eventually allow us to determine consensus bases at the positions beyond the CpG dinucleotide.

We performed six rounds of selection using this oligonucleotide with a GST-YY1 fusion protein that contains the 4 zinc finger units of YY1 protein. The bound oligonucleotides were eluted, subcloned and sequenced as shown in Fig.2A. As expected, 24 out of 40 sequences contain the exact same sequence as the known consensus motif (CGCCATnTT), while the remaining sequences have one to three base differences from this motif. We counted base preference at each position from both sides of the fixed CC bases (Fig.2B). Tabulation of these preferences indeed derived a longer DNA sequence, GCCGCCATTTTG, as the major DNA-binding motif of YY1. An independent analysis using the sequence logos program also confirmed this consensus motif (Fig.2B). This new 12-bp-long motif has two (GC) and one (G) additional bases at its 5′- and 3′ ends, respectively, than the known 9-bp-long consensus motif of YY1. This confirms that the YY1 protein indeed recognizes sequences longer than the previously known 9-bp-long consensus motif. Careful examination of the selected sequences also revealed that the two longer motifs of YY1 found in Peg3 and Xist were indeed included in this pool of selected sequences.

Figure 2
DNA-binding motifs of YY1

We performed a series of gel shift assays to further characterize the functional significance of the longer YY1 motifs (Fig.3). We prepared 5 different duplex probes containing slight base differences at their 5′- and 3′-ends. The GCC probe corresponds to the longer consensus motif (GCCGCCATnTTG) whereas the GGC probe has one base difference at the 2nd position (C->G), representing the YY1 motif in Peg3. The GCC-A probe has a base difference at the 12th position (G->A); the ACC probe at the 1st position (G->A) to represent the motif from Xist; and the AAC probe at the 1st and 2nd positions (GC->AA) to represent the 9-bp-long consensus motif. According to the results from competition assays, the GCC probe showed the highest levels of binding affinity to the YY1 protein; the GGC, GCC-A, and ACC probes exhibited the second highest levels; and finally the AAC probe showed the lowest levels among the five probes. The relative binding affinity of the GCC vs. GGC, ACC, and AAC probes was further demonstrated by reciprocal competition assays (Fig.3C). These assays reconfirmed higher affinity of the GCC probe compared to the three probes. These probes differ by the two bases (GC) at their 5′-ends. Therefore, the two extended bases (GC) on the 5′-end appear to increase the binding affinity of the YY1 protein to its target DNAs. The GGC and ACC probes representing the YY1 motif of Peg3 and Xist, respectively, also turn out to be stronger binding sites than the 9-bp-long consensus motif of YY1 (Fig.3A&C).

Figure 3
Comparison of DNA-binding affinity between the longer and the known motifs of YY1

Recognition of the extended 5′-end bases by the first zinc finger unit of YY1

According to X-ray crystallography studies [10], the second, third and fourth zinc finger units of the YY1 protein recognize the CTC, CAT and TT portions of the YY1 binding site of the AAV promoter (5′-CTC-CAT-CTT-3′). This predicts that the extended bases at the 5′-end of the longer motifs will be recognized by the first finger unit of the YY1 protein. The zinc finger domain of Pho (a homolog of YY1 in the Drosophila lineage) shows 5 amino acid differences compared to that of vertebrates' YY1 (Fig.4A). Three substitutions are found within the first zinc finger unit while the two remaining substitutions are in the beginning portion of the fourth zinc finger unit. Concurrently, the DNA-binding motif of Pho is shorter (GCCAT) than that of YY1 (CGCCATnTT). This also supports the possibility that the first zinc finger unit may be responsible for recognizing the extended bases at the 5′-side of the longer motif.

Figure 4
DNA-binding motifs of mutYY1

To confirm the above possibility, we performed another series of DNA binding analyses (Fig.4B). We substituted the amino acids at the three positions of the first finger unit of YY1 with those found in D. melanogaster (mutYY1). The GST-mutYY1 fusion protein was expressed, and used for another DNA-binding motif study. Three out of 26 bound DNAs contain an identical sequence to the known consensus motif of YY1, but most of the bound DNAs contain much shorter motifs than the YY1 consensus motif. Tabulation of base preferences yielded one sequence, CCATT, as a dominant motif among the selected sequences. This shorter motif is almost identical to the known motif of Pho, GCCAT, but with one base shift towards the 3′-side direction. Thus, the motif shortening by the substitutions confirms that the extended bases on the 5′-side of YY1′ longer motifs are indeed recognized by the first zinc finger unit of YY1. Interestingly, 17 out of 26 bound DNAs have two core motifs (CCAT), and these selected sequences did not use the prefixed CC bases of the randomized oligonucleotide, CGT(N)7CC(N)7ACG, as part of their binding sites. Instead, the shorter binding sites were formed independently within the two small randomized regions, (N)7. This indicates that the amino acid substitutions have shortened the overall size of the DNA binding motifs, from 12 to less than 7 bp in length. Also, although the substitutions are located in the first finger unit, the same changes affected the binding of the mutYY1 protein to both the 5′- and 3′-ends of its target DNAs. This further implies that the DNA recognition by YY1 is mediated through an overall protein structure contributed by its four zinc finger units, but not through modular protein structures contributed by individual finger units.

The DNA-binding of YY1 is methylation-sensitive: methylation on the CpG dinucleotide within CGCCATnTT blocks the binding to the YY1 protein. According to the results described above, the same CpG site appears to be recognized by the first finger unit, which has the three amino acid substitutions in the fly lineage. Coincidently, the fly lineage, the host genome of Pho, is known to have lost its DNA methylation mechanism [17]. This suggests the possibility that the loss of DNA methylation in the fly lineage might have contributed to the relaxation of functional constraints on the first finger unit. If this is the case, the Pho protein should be methylation-insensitive. To test this possibility, we determined the methylation sensitivity of the mutYY1 protein using gel shift assays (Fig.5). Contrary to our prediction, however, the mut-YY1 protein was still methylation-sensitive, which is similar to the YY1 protein. This refutes the initial prediction that the three amino acid substitutions found in the Pho protein may be an outcome of relaxed constraints on the methylation-sensitivity of the YY1 protein.

Figure 5
Methylation-sensitive DNA-binding of YY1 and mutYY1 proteins

Discussion

The current study revealed that the DNA-binding motifs of YY1 located within the two imprinted genes, Peg3 and Xist, are unusually longer than the known consensus motif of YY1. These longer motifs have two additional bases (either GG or GC) on their 5′-sides compared to the known shorter motif (CGCCATnTT). These additional bases are shown to be recognized by the first finger unit of YY1, and also increase their DNA-binding affinity to the YY1 protein. Overall, the recognition of the newly identified longer motifs requires an intact protein structure contributed by the four finger units of the YY1 protein.

In the past decade, the DNA-binding motifs of YY1, represented by a 9-bp-long consensus sequence (CGCCATnTT), have been confirmed repeatedly through independent binding motif studies as well as promoter analyses of individual genes. In most cases, the sizes of the identified YY1 binding sites are about 9 bp long or shorter. The X-ray crystallography study also confirmed that three zinc finger units of the YY1 protein (Fingers 2 through 4 but not Finger 1) contact closely with the 9-bp-long target DNA. Interestingly, however, Finger 1's contribution to DNA binding has not been well understood until now. The results derived from the current study demonstrated for the first time that Finger 1 recognizes two additional bases (either GC or GG) located on the 5′-side of the longer motif (Fig.2). Despite the observed higher affinity to the YY1 protein (Fig.3), these motifs are not common to all the known genes controlled by YY1, but are found in Peg3 and Xist (14; Kang & Kim, unpublished). The exact reason for this scarcity is unknown, but may be related to the following possibility. It is plausible that the longer motif may induce a slightly different DNA-bound structure of YY1 than the shorter motif due to the involvement of Finger 1. The contact between Finger 1 and the DNA can be either tight or loose depending upon long or short motifs, which may trigger slightly different protein shapes in the adjacent N-terminal portion of the YY1 protein. The N-terminal portion of YY1 has several small protein domains that are very critical for various YY1 functions [1, 3, 8]. Depending upon how Finger 1 contacts with the DNA, these small protein domains could either go to the surface or interior of the overall DNA-bound structure of YY1, which could eventually decide the actual function of a given YY1 binding. Thus, we hypothesize that the longer motifs may have different roles than the shorter motifs. This possibility needs to be investigated in the near future, but it is intriguing to point out the presence of the unusual longer motifs in the two imprinted genes, Peg3 and Xist, one allele of which is unusually repressed by DNA methylation. It will be of great interest to test if the recognition of the additional bases by Finger 1 is a prerequisite for special roles played by YY1, such as attracting DNA methylation to the longer YY1 binding sites during development.

Each zinc finger unit of the C2H2 type can bind 2 to 4 bp long DNA, and most zinc finger proteins of this type have more than 3 finger units. Thus, a given zinc finger protein can easily recognize about 10-bp-long DNA sequences. This is consistent with the fact that the YY1 protein with 4 finger units recognizes 9 to 12 bp-long DNA sequences. Despite this prediction, however, most YY1 binding sites found in individual genes are quite often shorter forms, represented by a core motif (GCCAT). This suggests that different finger units may have different levels of contribution to recognizing their target DNA sequences. In the case of YY1, the two internal finger units (Finger 2 and 3) probably have much more contribution to selecting DNA sequences since Finger 2 and 3 are known to contact with the core motif (Fig.4) [10,16]. This also agrees with the somewhat unexpected outcome of the three amino acid substitutions in Finger 1 of YY1 (Fig.4). The changes resulted in the shortening of the YY1 binding motif instead of inducing slightly different 9 to 12 bp-long motifs. A similar pattern is often observed from other zinc finger proteins with multi-finger units. For example, the 11-finger CTCF protein binds to 14-bp-long consensus motifs, and only 5 internal finger units (Finger 4 through 8) are responsible for recognizing its consensus motif [19]. It is interesting to note that internal fingers, not outside fingers, have more contribution to recognizing DNAs in both YY1 and CTCF proteins. The detailed nature of DNA binding by C2H2-type zinc finger proteins needs to be studied more, but the results in this study suggests that individual zinc finger units have different levels of functional contributions.

Materials and Methods

Sequence analyses

The genomic sequences of Peg3 and Xist were obtained through a series of database searches using NCBI, University of California Santa Cruz and Ensembl databases. YY1 binding sites were identified from the following genomic sequences, human (GenBank accession no. NC000019.8, 62015615…62045876), chimpanzee (NC006486.2, 62665221…62697348), mouse (NC000073.5, 6658671…6683130), cow (NC007316.2, 62353384…62376892), rhesus (NW001106534.1, 62714070…62737530) and dog (NC006583.2, 104184489…104227960) for the 1st intron region of Peg3, and human (M97168), mouse (M97167), cow (AF104906), horse (U50911) and rabbit (U50910) for the 2nd promoter of Xist. We also used bl2seq (www.ncbi.nlm.nih.gov/BLAST/) to show the sequence variation of the zinc finger domains of human YY1 (NP003394.1) and Drosophila melanogaster PHO (NM079891.2).

Expression of fusion proteins and DNA-binding motif study

The zinc finger regions of YY1 (NM009537.2) and mutYY1 were amplified from mouse brain cDNAs by the following primer sets: YY1 (mYY1Zn5, 5′-CCAAGAACAATAGCTTGCCCTC-3′ and mYY1Zn3, 5′-TCACTGGTTGTTTTTGGCTTTAGCG-3′), mutYY1 (PhoZn5, 5′-ATAGCTTGCCCTCATAAAGGCTGCAACAAGCATTTCAGGGATAGCTCTGC-3′ and mYY1Zn3, 5′-TCACTGGTTGTTTTTGGCTTTAGCG-3′). The amplified products were first cloned into the pCR4-TOPO vector (Invitrogen), and later transferred to the EcoRI site of the pGEX-4T-2 vector (Amersham Biosciences). The constructed vectors were transformed into BL21 (DE3) competent cells for bacterial expression (Stratagen). The optimum induction of the constructs by IPTG was monitored through SDS-PAGE analyses.

DNA-binding motif studies were conducted as described in the previous studies with the following modifications [16]: 6 rounds of selection were performed with slightly different randomized oligonucleotides. Randomized duplex DNAs were prepared with PCR (Maxime PCR premix kit, Intron Biotech) using the following oligonucleotides: 10 ng of a randomized template, NTCC57, 5′-CTGTCGGAATTCGCTGACGT(N)7CC(N)7ACGTCTTATCGGATCCTACGT-3′; 0.1 μg of two primers, UpNt, 5′-CTGTCGGAATTCGCTGACGT-3′ and DwNt, 5′-ACGTAGGATCCGATAAGACG-3′. After 6 rounds of DNA binding and amplification, the DNAs were subcloned into pCR4-TOPO vector (Invitrogen). For each fusion protein, 30 to 40 clones were purified and sequenced.

Gel shift assay of DNA-binding motifs

The Gel Shift Assay system (Promega) was used for DNA binding assay. About 5 μg of HeLa nuclear extract (Promega) or 50 μg of E.coli total extract containing each fusion protein was used for each experiment with the [γ-32P] ATP-labeled duplex probes: GCC-a, 5′-CGCTCCGTGCCGCCATTTTGGGCGGCTGGT-3′, and GCC-b, 5′-ACCAGCCGCCCAAAATGGCGGCACGGAGCG-3′; GGC-a, 5′-CGCTCCGTGGCGCCATTTTGGGCGGCTGGT-3′, and GGC-b, 5′-ACCAGCCGCCCAAAATGGCGCCACGGAGCG-3′; GCC-A-a, 5′-CGCTCCGTGCCGCCATTTTAGGCGGCTGGT-3′, and GCC-A-b, 5′ACCAGCCGCCTAAAATGGCGGCACGGAGCG-3′; ACC-a, 5′-CGCTCCGTACCGCCATTTTGGGCGGCTGGT-3′, and ACC-b, 5′-ACCAGCCGCCCAAAATGGCGGTACGGAGCG-3′; AAC-a, 5′-CGCTCCGTAACGCCATTTTGGGCGGCTGGT-3′, and AAC-b, 5′-ACCAGCCGCCCAAAATGGCGTTACGGAGCG-3′, CSE2-a, 5′-CCCACCCACCTGGGCGCCATCTTTAATGAAAG-3′, and CSE2-B, 5′-CTTTCATTAAAGATGGCGCCCAGGTGGGTGGG-3′; mCSE2-a, 5′-CCCACCCACCTGGGC*GCCATCTTTAATGAAAG-3′, and mCSE2-B, 5′-CTTTCATTAAAGATGGC*GCCCAGGTGGGTGGG-3′. For the competition binding assay, unlabeled duplex competitors with varying amounts (0, 5, 10, and 25 fold) were pre-incubated with the HeLa nuclear extract before adding radiolabeled duplex probes.

Acknowledgments

This study was supported by NIH grant GM66225 (to J.K.).

Footnotes

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