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18 December 2000, Volume 19, Number 55, Pages 6533-6548
Table of contents    Previous  Article  Next   [PDF]
Original Paper
Ets target genes: past, present and future
Victor I Sementchenko1 and Dennis K Watson1,2

1Center for Molecular and Structural Biology, Hollings Cancer Center, Medical University of South Carolina, Charleston, South Carolina, SC 29403, USA

2Department of Pathology and Laboratory Medicine, Medical University of South Carolina, Charleston, South Carolina, SC 29403, USA


Correspondence to: D K Watson, Medical University of South Carolina, Hollings Cancer Center, 86 Jonathan Lucas Street, Charleston SC 29425, USA


Ets is a family of transcription factors present in species ranging from sponges to human. All family members contain an approximately 85 amino acid DNA binding domain, designated the Ets domain. Ets proteins bind to specific purine-rich DNA sequences with a core motif of GGAA/T, and transcriptionally regulate a number of viral and cellular genes. Thus, Ets proteins are an important family of transcription factors that control the expression of genes that are critical for several biological processes, including cellular proliferation, differentiation, development, transformation, and apoptosis. Here, we tabulate genes that are regulated by Ets factors and describe past, present and future strategies for the identification and validation of Ets target genes. Through definition of authentic target genes, we will begin to understand the mechanisms by which Ets factors control normal and abnormal cellular processes. Oncogene (2000) 19, 6533-6548.


Ets; transcription; target genes; expression arrays



Regulation of gene expression is controlled through the combinatorial action of multiple transcription factors, which function to activate or repress transcription via binding to cis-regulatory elements present in target genes. Identification of functional target gene promoters that are regulated by specific transcription factors is critical for initiating studies to increase understanding of the molecular mechanisms that control transcription. Furthermore, identification of target gene promoters for normal and oncogenic transcription factors provides insight into the regulation of genes that are involved in control of normal cell growth, and differentiation, as well as provide information critical to understanding cancer development.

It has been over 15 years since Ets was originally identified as one of the two genes (Ets and Myb) transduced by the avian leukemia virus, E26 (Watson et al., 1990); (Reviewed in this issue by Blair and Athanasiou). Since the cloning of the v-ets gene, over 30 Ets domain-containing genes have been identified, either by sequence homology or as sites of viral integration and activation. Ets genes have been characterized in species ranging from sponges, nematodes and insects to humans. The Ets family proteins are transcription factors containing a winged helix-turn-helix DNA binding domain. (Reviewed (Ghysdael and Boureux, 1997; Graves and Petersen, 1998; Watson, 2001)). All Ets transcription factors bind to unique GGAA/T DNA sequences (EBS, Ets Binding Sites). Such EBS have been identified in the promoter/enhancer regions of viral and cellular genes, and thus control the expression of genes critical for the proper control of cellular proliferation, differentiation, development, hematopoiesis, apoptosis, metastasis, tissue remodeling, angiogenesis and transformation. Our current literature survey allowed identification of over 200 Ets target genes, and the number of genes shown to be regulated via EBS is constantly increasing. This number of Ets target genes is between those previously estimated for p53 (estimated between 200-300 target genes, (Tokino et al., 1994)) and for the hormone receptor family (50-100 genes; (Evans, 1988)). Further establishing the importance of Ets factors, a recent study demonstrated that EBS were among the eight most important DNA motifs in minimal responsive synthetic promoters generated using random oligonucleotides (Edelman et al., 2000). In addition to their importance in normal cellular control, based upon predominance of target genes, Ets products have also been implicated in several malignant and genetic disorders. For example, the human Ets genes, FLI1, TEL and ERG, are located at the translocation breakpoints of several leukemias and solid tumors, forming chimeric proteins believed to be responsible for tumorigenesis (Dittmer and Nordheim, 1998); (Mavrothalassitis and Ghysdael, Truong and Ben-David, in this issue). In addition, Ets factors have been found to be overexpressed (e.g., Ets2 in prostate and breast cancer (Sapi et al., 1998; Sementchenko et al., 1998)) or lost (e.g. PSE in prostate cancer (Nozawa et al., 2000)) during cancer development. Most of the target genes that mediate phenotypes associated with dysregulated expression remain to be defined.

The importance of the Ets family of transcription factors in various biological and pathological processes necessitates the identification of downstream cellular target genes of specific Ets proteins. Although some overlap in the biological function of different Ets proteins may exist, the emergence of a family of closely related transcription factors suggests that individual Ets members may have evolved unique roles, manifested through the control of specific target genes. Several key areas are critical for understanding what defines a functionally important Ets target gene: First, the functional importance of the EBS must be demonstrated by mutagenesis. Second, the Ets factor or factors responsible for transcriptional control of specific target genes need to be identified. While extensive publications have identified functionally important Ets binding sites (EBS) and thus, Ets target genes (Table 1 parts a,b,c,d,e and f), relatively few investigations have identified definitive target genes for a specific Ets factor. Third, it is becoming increasingly evident that cellular context defines the direction and magnitude of response to Ets factors. Indeed, future efforts will lead to discovery of the co-factors that modulate transcriptional regulation by Ets factors. Collectively, we are beginning to define the molecular mechanisms that determine which Ets family member will regulate a particular target gene and are developing appropriate approaches to determine which target genes are necessary for Ets-dependent phenotypes.


Ets target genes: the past

Initially, identification of Ets targets was based upon the presence of the GGAA/T core sequences in the promoters/enhancers of various cellular or viral regulatory regions. Subsequently, synthetic oligonucleotides containing presumptive Ets binding sites (EBS) have been used in electrophoretic mobility shift assays (EMSAs) with proteins prepared as nuclear extracts or by in vitro transcription/translation of specific Ets factor cDNAs. Competition using excess oligonucleotide or with oligonucleotides containing mutations in the presumptive EBS are tests for specificity. The Ets factor(s) responsible for specific DNA-protein complexes has been identified by antibody inhibition/supershift analyses. Transient transfection with native promoter-reporter genes or reporters containing the minimal promoter linked to the putative Ets binding sites are often used to demonstrate transcriptional activation or repression via Ets factors. The functional importance of specific sequences can be further analysed using deletions of various regions in the promoter sequence. The importance of particular candidate EBS can thus be demonstrated by mutagenesis. Table 1 parts a,b,c,d,e and f provide a list of Ets target genes that have been identified using these approaches. Collectively, functional Ets sites have been characterized in viral genes and cellular genes encoding transcription factors, transforming and tumor-associated products, proteinases, cell cycle and apoptosis regulators, signaling molecules, receptors and other cell surface molecules, ligands and tissue specific products.


Ets target genes: the present

The consensus binding sites for several Ets factors have been determined by enrichment of high affinity oligonucleotides from pools of oligonucleotides with random sequences. Such analyses have demonstrated that Ets family members often differ in their exact binding site preference outside of the GGAA/T core, with factor-specific recognition spanning nine to 15 base pairs (Ghysdael and Boureux, 1997; Graves and Petersen, 1998). However, in the last several years it has become apparent that Ets factors are able to bind to sites that do not conform to their in vitro derived high affinity consensus sequences. For example, the J-chain transcription factor NF-JB was purified by DNA affinity chromatography using sequences derived from the J-chain promoter and was subsequently found to be identical to PU.1. Significantly, the NF-JB site does not contain what had been previously felt to be an invariant GGA core sequence, but rather AAGAAA (Shin and Koshland, 1993). PU.1 has subsequently been found to bind to other sequences lacking the GGA core, including Macrophage scavenger receptor (AGAGAAGT, (Moulton et al., 1994)) and IL-1beta (GCAGAAGT (Buras et al., 1995; Kominato et al., 1995)). Target gene specificity and affinity of Ets factors to EBS is ultimately controlled by the precise sequence context/geometry of the EBS in relation to other cis-elements. The importance of neighboring elements for maximizing function via EBS is explained in part by the ability of Ets factors to form complexes and act synergistically with members of other transcription factor families. One example of co-dependence between Ets and other transcription factors is the synergistic binding and cooperative activation via Ets1, CREB and AML1 non-consensus binding sites in the human T-cell receptor beta chain promoter. Furthermore, it has been suggested that such low-affinity sites mediate cooperative concentration-dependent promoter regulation, while high-affinity sites may be associated with constitutive activation (Halle et al., 1997). Unique combinations of protein-protein interactions are likely to direct different Ets factors to regulate the expression of specific target genes. It is this precise assembly of multiple transcription factors onto a chromatin template that enhances transcriptional specificity and defines activation or repression function. (For further discussion, see review by Li et al., in this issue).

A subset of Ets factors have repressor activity (e.g. ERF, YAN, TEL, NET) and may directly compete with other Ets factors for binding to EBS sites (Table 1 parts a,b,c,d,e and f, e.g. MMP-3/TEL, M-CSF/TEL, Prolactin/ERF and Rb/Fli1). In addition, interaction with other proteins can block the ability of Ets factors to activate transcription (See article by Mavrothalassitis and Ghysdael, in this issue). The ability of individual Ets factors to function as activators or repressors is also dependent upon promoter and cell context. For example, studies using dermal fibroblasts indicate that Fli1 can function as an activator for the TN-C promoter, while acting as a repressor in the context of the collagen promoter. Ets1, on the other hand, activates both promoters (Shirasaki et al., 1999; Czuwara-Ladykowska et al., submitted; Trojanowska, in this issue). Furthermore, Fli1 has been shown to act as a repressor of Rb (Tamir et al., 1999). Unique promoter interactions with specific Ets factors have also been demonstrated in the case of Ets2 (or Ets1) and Erg on the collagenase (MMP1) and stromelysin (MMP3) promoters. Erg appears to act as an activator of the collagenase promoter, while it inhibited stimulation of stromelysin promoter by Ets2, whereas Ets2 stimulated both (Buttice et al., 1996). Recruitment of CBP/p300 by Ets2 seems to play an important role in activation of the stromelysin promoter (Jayaraman et al., 1999). Importantly, Erg was not able to cooperate with CBP/p300 in the context of this promoter, which may explain differential effects of Ets2 and Erg on the activity of this promoter.

Successful identification of target genes controlled by one (or more) Ets factors will require the use of complementary RNA and DNA based approaches in vitro and in vivo.

RNA-based approaches

Efforts to identify Ets target genes have often been based upon analysis of expression following gain or loss of function. Gain of function experiments employ constitutive or inducible expression of a family member, followed by identification of differentially expressed genes. Tetracycline-inducible expression of p42-Ets1 leads to increased expression of Caspase 1, which may account in part for the Fas- and low serum-induced apoptosis in the Ets1 expressing cells (Li et al., 1999a). Several approaches are available to identify gene expression differences including subtraction hybridization, differential display, representational difference analysis (RDA) and more recently, serial analysis of gene expression (SAGE) and Expression Array Analysis. Candidate target genes identified by this approach can subsequently be evaluated in the knockout mutant mice (loss of function). Enforced expression experiments may result in aberrant expression level and distribution, leading to identification of invalid target genes. It is noteworthy that most of the presumptive Myc target genes identified by gain of function studies were found not to have altered expression in the Myc knockout (Bush et al., 1998). This apparent discrepancy may be a reflection of cell-type specificity, cell cycle dependence, growth conditions or other experimental conditions.

Use of knockout/transgenic mice as models for identification of Ets target genes

The candidate target gene approach is based upon the biology of an Ets gene. Such an approach may be coupled with phenotypes observed in knockout and transgenic mice. Loss of function PU.1 results in absence of monocyte/macrophage development and B cells with abnormal T-cell and granulocytic development. Consistent with the myeloid phenotype, Northern analyses demonstrated that homozygous (-/-) mutant PU.1 mice have greatly reduced levels of mRNAs for the receptors for M-CSF, G-CSF and GM-CSF. Each of these receptors had been previously proposed to be PU.1 responsive. However, a RDA study allowed for the identification of additional myeloid genes ((Iwama et al., 1998) and references within). Similarly, the megakaryocytic lineage defects observed with the recent Fli1 knockout mice (Hart et al., 2000; Spyropoulos et al., 2000) suggests that genes whose expression is necessary for this lineage may be Fli1 targets. RT-PCR studies demonstrate that gpIX (Hart et al., 2000) and c-mpl (Kawada et al., manuscript submitted) are reduced in mRNAs prepared from homozygous mutant mice, consistent with earlier in vitro studies (Alexander and Dunn, 1995; Bastian et al., 1999; Deveaux et al., 1996). Caution is warranted however, since loss of a particular lineage may affect the expression of indirect target genes as well. Furthermore, tissue-specific alterations in presumptive target genes can occur as demonstrated by the initial RNase protection analysis of Ets2(-/-) mice (Yamamoto et al., 1998).

The transgenic (gain of function) animals that have been generated for Fli1 (Zhang et al., 1995), Ets2 (Sumarsono et al., 1996), PU.1 (Moreau-Gachelin et al., 1996) and TEL-PDEFbeta (Ritchie et al., 1999) will potentially facilitate target gene identification. However, the transgenic approach will not provide as unambiguous a result as creating mice lacking expression of a specific Ets factor. First, the transgenic will have normal expression of the endogenous Ets factor, in addition to transgene expression. Second, improper timing, tissue context and level of ectopic expression may seriously compromise the value of the results using a transgenic approach.

One caveat/limitation to RNA based studies is that both direct and indirect target genes are identified. Expression of direct target genes is due to the interaction of Ets proteins with the regulatory elements present in the gene. In contrast, the regulation of indirect target genes may be controlled via proteins encoded by direct target genes. While kinetic arguments (time course of induction of a presumptive direct target gene relative to the expression of the Ets factor) can be used, an alternative approach to demonstrate direct regulation of a gene is the utilization of ER fusion constructs (Littlewood et al., 1995). Fusion of the estrogen receptor hormone binding domain (ER-HBD) to other proteins has been shown to result in ligand-dependent inducible activity of the resultant chimeric protein. Thus, in the absence of the ligand, the chimeric protein is expressed, but sequestered in the cytoplasm. Functional activity of the protein is dependent upon hormone addition and subsequent nuclear localization. Simultaneous addition of cycloheximide and hormone allows activation of target genes in the absence of protein synthesis and thus provides a method to distinguish primary and secondary target genes. One limitation to this approach is that not every protein fused ER turns out to be regulatable by ligand. In addition, in some cases, fusion of the ER domain to the amino terminus of the protein works better than fusion at the carboxy terminus (Trevor Littlewood, personal communications). Furthermore, such fusion protein may lose some of its ability to interact with its protein partners, which may also compromise experimental results. Although successful estrogen-mediated expression of ERM has been demonstrated (Pelczar et al., 1997), this chimeric protein has not yet been used to identify or validate ERM target genes. Not all attempts to develop hormone-regulated functionality will be successful. For example, we recently found that the human Fli1-Estrogen receptor fusion construct, joining the ER ligand binding domain to either the carboxy or amino terminal end of Fli1, was not regulated by hormone. Whether this was due in part to the observed functional interference between Fli1 and steroid hormone receptors (Darby et al., 1997) remains to be determined.

DNA based approaches

EMSA and in vitro footprinting assays have been used to demonstrate the potential for sequence-specific interaction between the labeled DNA and an Ets protein. To demonstrate in vivo Ets-DNA interactions, an early approach was analysis by in vivo footprinting (IVF). Sites of sequence-specific DNA-protein interactions are identified by altered reactivity to chemical modification in intact cells. Few studies have used this approach to evaluate whether an EBS is bound in vivo (Table 1 parts a,b,c,d,e and f, designated IVF). For example, IVF demonstrated cell type specificity of the functional EBS within the Rat tyrosine aminotransferase promoter (Espinas et al., 1994). However, in vivo footprinting studies do not allow identification of the specific Ets factor responsible for regulation of a given target. Other methodologies, such as whole-genome PCR and chromatin immunoprecipitation, have begun to be used for identification of targets for specific Ets factors. These methods allow the cloning of genomic DNA, based upon the presence of binding sites for a particular transcription factor.

Whole genome polymerase chain reaction (WGPCR)

WGPCR is one method that identifies direct target gene promoters/enhancer sequences for DNA binding proteins (Watson et al., 2000). Briefly, genomic DNA fragments are immuno-selected based upon their binding to a specific transcription factor and amplified by the polymerase chain reaction. The utility of WGPCR for the identification of Ets1 factor binding sites has been demonstrated. Among the clones isolated, three genomic fragments were found to be derived from the regulatory regions of the human serglycin, preproapolipoprotein C II and the Egr1 genes. Furthermore, the promoters of each of these genes contain consensus EBS able to bind to Ets proteins in EMSAs (Robinson et al., 1997).

Chromatin immunoprecipitation (ChIPs)

Chromatin immunoprecipitation is an exciting approach for the identification of target genes based upon in vivo occupancy of a promoter by a transcription factor and enrichment of transcription factor bound chromatin by immunoprecipitation using antibody against a specific transcription factor (Orlando, 2000). With this approach, cells are incubated with formaldehyde to crosslink proteins to DNA, and sonicated chromatin is subsequently incubated with Ets specific antibody or 'no antibody' control. Washed immunoprecipitates are analysed by PCR to determine whether candidate target genes are enriched in the Ets-immunoprecipitated samples. This approach has recently been used to demonstrate that the Rb gene is bound by Fli1 in vivo (Tamir et al., 1999). Another recent study utilizing ChIPs has demonstrated that following LPS stimulation, multiple Ets factors (Elk1, Ets1/2) are bound to the TNFalpha promoter in vivo (Tsai et al., 2000). It is important that ChIPs data be coupled with independent verification of the functional importance of the binding sites identified. Furthermore, DNA based approaches do not allow to immediately distinguish the direction of the interaction of a transcription factor (repression or activation) with the particular promoter.


Ets target genes: future directions

We will soon be able to generate libraries of Ets-specific target genes using in vivo chromatin immunoprecipitation. Subsequent DNA sequence analysis should begin to allow identification of specific combinations of EBS proximal to binding sites for other transcription factors, allowing for better definition of Ets target genes. Perhaps ChIP approaches using multiple antibodies, used sequentially, may allow identification of in vivo synergistic interactions previously implicated by transient transfection assays or never before identified. The role of post-translational modifications upon complex formation may be able to be evaluated in vivo using phosphorylation or acetylation specific antibodies, followed by Ets factor-specific antibodies.

Similarly, ChIPs provides a valuable approach to assess the in vivo kinetics of Ets factor binding to specific promoter sites and to assess whether single or multiple family members can bind a single promoter. It will be important to determine whether Ets factor occupancy on specific promoters is altered during differentiation of specific lineages in normal development. We know that temporal specific expression of Ets factors occurs during development. Whether such changes can be correlated with differences in occupancy of Ets target gene promoters and subsequent gene expression remains to be determined. For example, such studies may demonstrate whether TEL can compete directly with the transcriptional targets of Fli1, as well as indirectly block Fli1 transcriptional activity (Kwiatkowski et al., 1998). Perhaps similar interplay between other Ets factors may also serve as a molecular switch between gene repression and activation and vice versa. The stable integration of specific promoter constructs provides a possible experimental system to simultaneously examine transcriptional activity and transcription factor occupancy (Boyd and Farnham, 1999).

Co-localization studies

Confocal microscopy with double immunostaining is an approach to confirm the co-localization of an Ets factor with its presumptive target gene within a particular set of cells within a specific tissue. From such analyses, we will determine if there are Ets-dependent expression patterns for specific target genes that may be evident in a tissue or temporal specific manner. It is anticipated that in some tissues, expression of specific target genes would have an absolute requirement for a specific Ets factor and these genes would not be expressed in these tissues in the appropriate Ets homozygous knockout mice. On the other hand, in some tissues, the expression of Ets may not be absolutely required, suggesting that redundancy between Ets family transcription factors may be tissue-specific. Indeed, precise examination of the tissue and cellular expression of target genes in wild-type and homozygous mutant mice is likely to be the only way to identify tissue-specific redundant pathways. Initial analysis of target gene expression in the Ets2 knockout mouse clearly illustrates this complexity. Tissue-specific loss of expression was observed for several of the genes whose expression was altered; for example, Ets1, MMP3, MMP9 and uPA were found to be reduced in the skin, while the mRNAs for these genes were apparently unchanged in the mammary gland (Yamamoto et al., 1998). It remains to be determined whether different cell types (e.g., basal cells versus epithelia cells versus stromal cells) in a particular tissue have identical Ets factor and/or target gene profiles.

Trap approaches for the identification of target genes

Future studies may exploit an inducible gene trap approach similar to that recently used to identify homeoprotein-regulated loci (Mainguy et al., 2000) for identification of Ets-responsive genes. Briefly, independent clones are isolated from a library of ES cells constructed to have randomly integrated reporters under the control of the individual 'trapped' gene promoters (promoter trap). To identify an Ets responsive gene, single cell clones can be incubated with purified fusion protein, consisting of the Ets domain of a specific Ets factor fused to the third helix of the homeodomain for efficient internalization into the ES cell. The internalized recombinant protein should compete with endogenous Ets proteins binding to EBS present in Ets-responsive genes expressed in ES cells. This approach should enrich for fusion transcripts corresponding to the Ets responsive genes. In addition, since each clone in the library is in ES cells, this method could also allow for rapid generation of knockout mice for specific Ets-target genes.

Modifiers of Ets function

Genetic screens for modifiers of Ets function will further enhance our understanding of the mechanisms that control the expression of Ets target genes. Such studies could be initiated using one of the eight Drosophila Ets genes (see article in this issue, Hsu and Schulz). Both gain of function and loss of function phenotypes provide foundations for screening for modifiers of phenotype (Rebay et al., 2000). Availability of the complete sequence of the Drosophila genome and the use of Drosophila genetics (Rubin and Lewis, 2000) will provide an approach to identify modifiers of Ets function (as well as a means to identify targets). Once identified, these genes may serve as probes for the identification of relevant mammalian target genes and modulators of Ets transcription factors (Ashburner et al., 2000).



This work is dedicated to Takis S Papas, a friend, valued colleague and mentor. This work was supported in part by grants from the DOD [N00014-96-1-1298] and NCI [PO1 CA78582].


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Table 1a Table 1a Ets target genes

Table 1b Table 1b Ets target genes(Continued)

Table 1c Table 1c Ets target genes(Continued)

Table 1d Table 1d Ets target genes(Continued)

Table 1e Table 1e Ets target genes(Continued)

Table 1f Ets target genes(Continued)

18 December 2000, Volume 19, Number 55, Pages 6533-6548
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