Master regulatory GATA transcription factors: mechanistic principles and emerging links to hematologic malignancies
Identifieur interne : 004229 ( Pmc/Corpus ); précédent : 004228; suivant : 004230Master regulatory GATA transcription factors: mechanistic principles and emerging links to hematologic malignancies
Auteurs : Emery H. Bresnick ; Koichi R. Katsumura ; Hsiang-Ying Lee ; Kirby D. Johnson ; Archibald S. PerkinsSource :
- Nucleic Acids Research [ 0305-1048 ] ; 2012.
Abstract
Numerous examples exist of how disrupting the actions of physiological regulators of blood cell development yields hematologic malignancies. The master regulator of hematopoietic stem/progenitor cells GATA-2 was cloned almost 20 years ago, and elegant genetic analyses demonstrated its essential function to promote hematopoiesis. While certain GATA-2 target genes are implicated in leukemogenesis, only recently have definitive insights emerged linking GATA-2 to human hematologic pathophysiologies. These pathophysiologies include myelodysplastic syndrome, acute myeloid leukemia and an immunodeficiency syndrome with complex phenotypes including leukemia. As GATA-2 has a pivotal role in the etiology of human cancer, it is instructive to consider mechanisms underlying normal GATA factor function/regulation and how dissecting such mechanisms may reveal unique opportunities for thwarting GATA-2-dependent processes in a therapeutic context. This article highlights GATA factor mechanistic principles, with a heavy emphasis on GATA-1 and GATA-2 functions in the hematopoietic system, and new links between GATA-2 dysregulation and human pathophysiologies.
Url:
DOI: 10.1093/nar/gks281
PubMed: 22492510
PubMed Central: 3401466
Links to Exploration step
PMC:3401466Le document en format XML
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<front><div type="abstract" xml:lang="en"><p>Numerous examples exist of how disrupting the actions of physiological regulators of blood cell development yields hematologic malignancies. The master regulator of hematopoietic stem/progenitor cells GATA-2 was cloned almost 20 years ago, and elegant genetic analyses demonstrated its essential function to promote hematopoiesis. While certain GATA-2 target genes are implicated in leukemogenesis, only recently have definitive insights emerged linking GATA-2 to human hematologic pathophysiologies. These pathophysiologies include myelodysplastic syndrome, acute myeloid leukemia and an immunodeficiency syndrome with complex phenotypes including leukemia. As GATA-2 has a pivotal role in the etiology of human cancer, it is instructive to consider mechanisms underlying normal GATA factor function/regulation and how dissecting such mechanisms may reveal unique opportunities for thwarting GATA-2-dependent processes in a therapeutic context. This article highlights GATA factor mechanistic principles, with a heavy emphasis on GATA-1 and GATA-2 functions in the hematopoietic system, and new links between GATA-2 dysregulation and human pathophysiologies.</p>
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<biblStruct><analytic><author><name sortKey="Zhang, Sj" uniqKey="Zhang S">SJ Zhang</name>
</author>
<author><name sortKey="Shi, Jy" uniqKey="Shi J">JY Shi</name>
</author>
<author><name sortKey="Li, Jy" uniqKey="Li J">JY Li</name>
</author>
</analytic>
</biblStruct>
</listBibl>
</div1>
</back>
</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Nucleic Acids Res</journal-id>
<journal-id journal-id-type="iso-abbrev">Nucleic Acids Res</journal-id>
<journal-id journal-id-type="publisher-id">nar</journal-id>
<journal-id journal-id-type="hwp">nar</journal-id>
<journal-title-group><journal-title>Nucleic Acids Research</journal-title>
</journal-title-group>
<issn pub-type="ppub">0305-1048</issn>
<issn pub-type="epub">1362-4962</issn>
<publisher><publisher-name>Oxford University Press</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">22492510</article-id>
<article-id pub-id-type="pmc">3401466</article-id>
<article-id pub-id-type="doi">10.1093/nar/gks281</article-id>
<article-id pub-id-type="publisher-id">gks281</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Survey and Summary</subject>
</subj-group>
</article-categories>
<title-group><article-title>Master regulatory GATA transcription factors: mechanistic principles and emerging links to hematologic malignancies</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Bresnick</surname>
<given-names>Emery H.</given-names>
</name>
<xref ref-type="aff" rid="gks281-AFF1"><sup>1</sup>
</xref>
<xref ref-type="corresp" rid="gks281-COR1">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Katsumura</surname>
<given-names>Koichi R.</given-names>
</name>
<xref ref-type="aff" rid="gks281-AFF1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lee</surname>
<given-names>Hsiang-Ying</given-names>
</name>
<xref ref-type="aff" rid="gks281-AFF1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Johnson</surname>
<given-names>Kirby D.</given-names>
</name>
<xref ref-type="aff" rid="gks281-AFF1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Perkins</surname>
<given-names>Archibald S.</given-names>
</name>
<xref ref-type="aff" rid="gks281-AFF1"><sup>2</sup>
</xref>
</contrib>
</contrib-group>
<aff id="gks281-AFF1"><sup>1</sup>
Wisconsin Institutes for Medical Research, Paul Carbone Cancer Center, Department of Cell and Regenerative Biology, University of Wisconsin School of Medicine and Public Health, Madison, WI 53705 and<sup>2</sup>
Department of Pathology and Lab Medicine, University of Rochester, Rochester, NY 14642, USA</aff>
<author-notes><corresp id="gks281-COR1">*To whom correspondence should be addressed. Tel: +1 608 265 6446; Fax: +1 608 262 1257; Email: <email>ehbresni@wisc.edu</email>
</corresp>
</author-notes>
<pmc-comment>For NAR both ppub and collection dates generated for PMC processing 1/27/05 beck</pmc-comment>
<pub-date pub-type="collection"><month>7</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="ppub"><month>7</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="epub"><day>5</day>
<month>4</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>5</day>
<month>4</month>
<year>2012</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
. </pmc-comment>
<volume>40</volume>
<issue>13</issue>
<fpage>5819</fpage>
<lpage>5831</lpage>
<history><date date-type="received"><day>14</day>
<month>2</month>
<year>2012</year>
</date>
<date date-type="rev-recd"><day>13</day>
<month>3</month>
<year>2012</year>
</date>
<date date-type="accepted"><day>14</day>
<month>3</month>
<year>2012</year>
</date>
</history>
<permissions><copyright-statement>© The Author(s) 2012. Published by Oxford University Press.</copyright-statement>
<copyright-year>2012</copyright-year>
<license license-type="creative-commons" xlink:href="http://creativecommons.org/licenses/by-nc/3.0"><license-p><pmc-comment>CREATIVE COMMONS</pmc-comment>
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc/3.0">http://creativecommons.org/licenses/by-nc/3.0</ext-link>
), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p>
</license>
</permissions>
<abstract><p>Numerous examples exist of how disrupting the actions of physiological regulators of blood cell development yields hematologic malignancies. The master regulator of hematopoietic stem/progenitor cells GATA-2 was cloned almost 20 years ago, and elegant genetic analyses demonstrated its essential function to promote hematopoiesis. While certain GATA-2 target genes are implicated in leukemogenesis, only recently have definitive insights emerged linking GATA-2 to human hematologic pathophysiologies. These pathophysiologies include myelodysplastic syndrome, acute myeloid leukemia and an immunodeficiency syndrome with complex phenotypes including leukemia. As GATA-2 has a pivotal role in the etiology of human cancer, it is instructive to consider mechanisms underlying normal GATA factor function/regulation and how dissecting such mechanisms may reveal unique opportunities for thwarting GATA-2-dependent processes in a therapeutic context. This article highlights GATA factor mechanistic principles, with a heavy emphasis on GATA-1 and GATA-2 functions in the hematopoietic system, and new links between GATA-2 dysregulation and human pathophysiologies.</p>
</abstract>
<counts><page-count count="13"></page-count>
</counts>
</article-meta>
</front>
<body><sec><title>INTRODUCTION</title>
<p>Drilling into mechanisms governing the control of hemoglobin synthesis led to the discovery in the 1980s of a new class of transcription factors containing a highly conserved Cys4 dual zinc finger DNA-binding module. These proteins were deemed GATA factors based on the nucleotide composition of their cognate DNA-binding motif (<xref ref-type="bibr" rid="gks281-B1">1</xref>
). The discovery of GATA-1 was followed by the cloning of five additional mammalian GATA factors (GATA-2–6) (<xref ref-type="bibr" rid="gks281-B2 gks281-B3 gks281-B4 gks281-B5 gks281-B6 gks281-B7 gks281-B8 gks281-B9">2–9</xref>
). Historically, GATA-1, GATA-2 and GATA-3 are deemed the hematopoietic GATA factors (<xref ref-type="bibr" rid="gks281-B10">10</xref>
), while GATA-4, GATA-5 and GATA-6 are termed the cardiac GATA factors (<xref ref-type="bibr" rid="gks281-B11">11</xref>
,<xref ref-type="bibr" rid="gks281-B12">12</xref>
). Extensive biological and genetic analyses have revealed exceptions to this generalization, including expression of the hematopoietic GATA factors in endothelium (<xref ref-type="bibr" rid="gks281-B9">9</xref>
,<xref ref-type="bibr" rid="gks281-B13">13</xref>
,<xref ref-type="bibr" rid="gks281-B14">14</xref>
), breast and prostate (<xref ref-type="bibr" rid="gks281-B15">15</xref>
,<xref ref-type="bibr" rid="gks281-B16">16</xref>
) and neurons (<xref ref-type="bibr" rid="gks281-B17">17</xref>
,<xref ref-type="bibr" rid="gks281-B18">18</xref>
).</p>
<p>Loss-of-function analyses established the essential GATA-1 functions to promote erythrocyte, megakaryocyte, mast cell and eosinophil development (<xref ref-type="bibr" rid="gks281-B19 gks281-B20 gks281-B21 gks281-B22 gks281-B23 gks281-B24 gks281-B25">19–25</xref>
) and GATA-3 functions to promote specific aspects of T-cell lymphopoiesis (<xref ref-type="bibr" rid="gks281-B26">26</xref>
,<xref ref-type="bibr" rid="gks281-B27">27</xref>
). GATA-2 is uniquely essential for the genesis and/or function of hematopoietic stem/progenitor cells (<xref ref-type="bibr" rid="gks281-B28 gks281-B29 gks281-B30">28–30</xref>
). <italic>Gata2</italic>
-null mouse embryos are severely anemic and die at approximately embryonic day (E) 10 (<xref ref-type="bibr" rid="gks281-B28">28</xref>
). Despite the critical GATA-2 requirement for the formation of all lineages of blood cells, some primitive erythroblasts exist in <italic>Gata2</italic>
-null embryos. The absence of these cells in <italic>Gata1</italic>
<sup>−/–</sup>
–<italic>Gata2</italic>
<sup>−/–</sup>
compound mutants indicate that GATA-1 and GATA-2 can function redundantly in the genesis and/or survival of primitive erythroblasts (<xref ref-type="bibr" rid="gks281-B31">31</xref>
). The GATA-2 requirement for the control of hematopoietic stem/progenitor cells is dose dependent, as <italic>Gata2</italic>
<sup>+/–</sup>
HSCs are functionally impaired, even though the mice are viable (<xref ref-type="bibr" rid="gks281-B30">30</xref>
,<xref ref-type="bibr" rid="gks281-B32">32</xref>
). GATA-2 overexpression in murine bone marrow is also inhibitory for hematopoiesis (<xref ref-type="bibr" rid="gks281-B33">33</xref>
). While this result has potentially important pathophysiological implications, transcription factor overexpression studies are difficult to interpret, given ample opportunities for overexpressed proteins to aberrantly engage cellular regulatory factors. As GATA-2 is also expressed in endothelial cells, placenta, prostate, pituitary and select neurons, it will be instructive to compare GATA-2 mechanisms in hematopoietic versus non-hematopoietic systems, although this is currently a virgin territory. Clearly, many unanswered questions remain regarding cell type-specific GATA factor mechanisms and biological actions.</p>
</sec>
<sec><title>GATA FACTOR MECHANISMS: FUNDAMENTAL PRINCIPLES</title>
<p>The purification and cloning of GATA-1 (<xref ref-type="bibr" rid="gks281-B34">34</xref>
,<xref ref-type="bibr" rid="gks281-B35">35</xref>
) ushered in studies that elucidated mechanistic principles governing GATA factor function (<xref ref-type="bibr" rid="gks281-B36">36</xref>
). The zinc finger residing closest to the carboxy-terminus (C-finger) mediates sequence-specific DNA binding to WGATAR motifs (<xref ref-type="bibr" rid="gks281-B37">37</xref>
,<xref ref-type="bibr" rid="gks281-B38">38</xref>
), while the zinc finger proximal to the amino-terminus (N-finger) mediates an important protein–protein interaction with the nine zinc finger-containing coregulator Friend of GATA-1 (<xref ref-type="bibr" rid="gks281-B39 gks281-B40 gks281-B41 gks281-B42">39–42</xref>
). The N-finger may also stabilize DNA binding in certain contexts (<xref ref-type="bibr" rid="gks281-B43">43</xref>
). Additional interactions involving the zinc fingers have been documented (<xref ref-type="bibr" rid="gks281-B44">44</xref>
,<xref ref-type="bibr" rid="gks281-B45">45</xref>
), including binding to the myeloid transcription factor PU.1 (<xref ref-type="bibr" rid="gks281-B46">46</xref>
), the erythroid transcription factor ELKF (<xref ref-type="bibr" rid="gks281-B47">47</xref>
) and the mediator complex component Med1 (<xref ref-type="bibr" rid="gks281-B48">48</xref>
). Much less is known about the structural basis and biological implications of these interactions. The broad GATA-1 N-terminus enhances endogenous target gene activation in a context-dependent manner (<xref ref-type="bibr" rid="gks281-B49">49</xref>
). Missense mutations in the N-terminus trigger the usage of an alternative translational start site, yielding a mutant that is strongly associated with the development of transient myeloproliferative disease and acute megakaryoblastic leukemia (<xref ref-type="bibr" rid="gks281-B50 gks281-B51 gks281-B52">50–52</xref>
).</p>
<p>Despite approximately 7 million GATA motifs in the human genome, all capable of forming high-affinity complexes with GATA factors and naked DNA <italic>in vitro</italic>
, GATA-1 and GATA-2 occupy only 0.1–1% of these motifs in erythroblasts, based on chromatin immunoprecipitation coupled with massively parallel sequencing and real-time PCR validation (<xref ref-type="bibr" rid="gks281-B14">14</xref>
,<xref ref-type="bibr" rid="gks281-B53">53</xref>
,<xref ref-type="bibr" rid="gks281-B54">54</xref>
). While the molecular determinants for this exquisite discrimination are not fully understood (<xref ref-type="bibr" rid="gks281-B55">55</xref>
), FOG-1 facilitates GATA-1 occupancy at a subset of chromatin sites (<xref ref-type="bibr" rid="gks281-B56">56</xref>
,<xref ref-type="bibr" rid="gks281-B57">57</xref>
). Genome-wide analysis of <italic>cis</italic>
-elements residing at endogenous GATA-1 and GATA-2 occupancy sites led to refinement of the GATA consensus from WGATAR to WGATAA. However, the percent of total WGATAA motifs occupied remains very low. Beyond GATA motif sequence composition, the most rudimentary determinant of chromatin occupancy, diagnostic patterns of histone posttranslational modifications demarcate occupied versus unoccupied sites, both containing conserved GATA motifs (<xref ref-type="bibr" rid="gks281-B53">53</xref>
,<xref ref-type="bibr" rid="gks281-B58 gks281-B59 gks281-B60">58–60</xref>
) (<xref ref-type="fig" rid="gks281-F1">Figure 1</xref>
, Principle 1). In principle, the unique epigenetic signature of occupied sites may represent primed chromatin structures recognized by GATA-1 as a pivotal determinant of site selection. Alternatively, the signature may arise as a consequence of GATA-1 chromatin occupancy, followed by recruitment of GATA-1 coregulators that modify chromatin surrounding the occupancy site.</p>
<p>GATA-1 chromatin occupancy leads to either activation or repression of target genes, both of which can be mediated by FOG-1 (<xref ref-type="bibr" rid="gks281-B36">36</xref>
) (<xref ref-type="fig" rid="gks281-F1">Figure 1</xref>
, Principle 2). One mode of FOG-1 function involves interaction of its N-terminus with the NuRD chromatin remodeling complex (<xref ref-type="bibr" rid="gks281-B61 gks281-B62 gks281-B63">61–63</xref>
), which can mediate both repression and activation. GATA-1 utilizes FOG-1 to induce higher order chromatin loops, based on chromosome conformation capture (3C) data (<xref ref-type="bibr" rid="gks281-B64 gks281-B65 gks281-B66">64–66</xref>
). In principle, such loops can mediate activation or repression, dependent upon the physical relationship between the loop and functional features of a gene and the precise nature of the structure formed. GATA-1 also recruits the chromatin remodeler BRG1 to chromatin, which can mediate higher order looping (<xref ref-type="bibr" rid="gks281-B67 gks281-B68 gks281-B69">67–69</xref>
).
<fig id="gks281-F1" position="float"><label>Figure 1.</label>
<caption><p>GATA factor mechanistic principles. The models depict mechanistic principles derived from studies of GATA-1 and GATA-2. While the fundamental nature of these principles is likely to be shared by other GATA factors, additional GATA factor-specific mechanistic permutations are expected. Principle 1: GATA factors occupy a very small percent of the WGATAA motifs in a genome (<1%), suggesting that crucial mechanisms exist that control the discrimination among these highly abundant motifs. However, such mechanisms are not firmly established. The model depicts the occlusion of select GATA motifs, thus creating an obligate requirement for chromatin remodeling/modification reactions to increase access of the WGATAA residues required for GATA factor binding and/or to selectively occlude the vast majority of sites. At certain sites, FOG-1 (<xref ref-type="bibr" rid="gks281-B56">56</xref>
,<xref ref-type="bibr" rid="gks281-B57">57</xref>
) and GATA-1 acetylation (<xref ref-type="bibr" rid="gks281-B95">95</xref>
) enhance chromatin access. Presumably, a host of regulatory factors mediate the essential process of establishing/maintaining accessible and occluded sites. Principle 2: GATA factors activate and repress target genes via multiple mechanisms, including with or without FOG-1 (<xref ref-type="bibr" rid="gks281-B36">36</xref>
). Presumably, this mechanistic diversity reflects the specific chromatin architecture at a genetic locus, the subnuclear environment in which the locus resides and the regulatory mileau characteristic of the specific environment. Principle 3: GATA-1 and GATA-2 commonly co-localize with Scl/TAL1, another master regulator of hematopoiesis (<xref ref-type="bibr" rid="gks281-B96">96</xref>
), at chromatin sites. The model illustrates GATA factor and Scl/TAL1 occupancy of a composite element consisting of an E-box and a WGATAA motif, which was originally described by Wadman <italic>et al</italic>
. (<xref ref-type="bibr" rid="gks281-B76">76</xref>
). Similar to the description above, only a very small percentage of composite elements are occupied by GATA factors in cells (<xref ref-type="bibr" rid="gks281-B53">53</xref>
,<xref ref-type="bibr" rid="gks281-B58">58</xref>
). As co-localization does not require the E-box (<xref ref-type="bibr" rid="gks281-B72">72</xref>
), there is much to be learned about the biochemical nature of the GATA factor and Scl/TAL1 interaction. However, the co-localization measured by ChIP often correlates with transcriptional activity (<xref ref-type="bibr" rid="gks281-B54">54</xref>
,<xref ref-type="bibr" rid="gks281-B58">58</xref>
,<xref ref-type="bibr" rid="gks281-B72">72</xref>
). Principle 4: GATA switches are defined as a molecular transition in which one GATA factor replaces another from a chromatin site, which is often associated with an altered transcriptional output. The GATA switch depicted reflects that occurring at the <italic>Gata2</italic>
locus during erythropoiesis, in which GATA-1 displaces GATA-2 from chromatin, which rapidly instigates repression (<xref ref-type="bibr" rid="gks281-B87">87</xref>
). Context-dependent GATA switches may either activate or repress transcription and, in certain cases, may sustain the original transcriptional output (<xref ref-type="bibr" rid="gks281-B36">36</xref>
).</p>
</caption>
<graphic xlink:href="gks281f1"></graphic>
</fig>
</p>
<p>Additional GATA-1 mechanisms exist, including FOG-1-independent activation and repression (<xref ref-type="bibr" rid="gks281-B41">41</xref>
,<xref ref-type="bibr" rid="gks281-B70">70</xref>
,<xref ref-type="bibr" rid="gks281-B71">71</xref>
), although these mechanisms remain poorly understood. GATA-1 commonly co-localizes on chromatin with the stem cell leukemia/T-cell acute lymphocytic leukemia-1 (Scl/TAL1) protein (<xref ref-type="bibr" rid="gks281-B58">58</xref>
,<xref ref-type="bibr" rid="gks281-B59">59</xref>
,<xref ref-type="bibr" rid="gks281-B72">72</xref>
), and the co-localization commonly correlates with transcriptional activity (<xref ref-type="bibr" rid="gks281-B54">54</xref>
,<xref ref-type="bibr" rid="gks281-B58">58</xref>
,<xref ref-type="bibr" rid="gks281-B72">72</xref>
) (<xref ref-type="fig" rid="gks281-F1">Figure 1</xref>
, Principle 3). Scl/TAL1 is a master regulator of hematopoiesis that binds E-boxes and non-DNA-binding components including LMO2, LDB1, ETO2, and single-stranded DNA-binding proteins (<xref ref-type="bibr" rid="gks281-B73 gks281-B74 gks281-B75 gks281-B76 gks281-B77 gks281-B78 gks281-B79">73–79</xref>
). In the context of naked DNA, optimal composite elements that support complex formation contain an E-box, a downstream GATA motif, and an 8-bp spacer (<xref ref-type="bibr" rid="gks281-B76">76</xref>
). The 8-bp spacing is crucial for GATA-2-dependent enhancer activity in a transient transfection assay using cells expressing endogenous GATA-2 (<xref ref-type="bibr" rid="gks281-B58">58</xref>
). However, GATA-1 and Scl/TAL1 also co-localize at certain chromatin sites lacking composite elements (<xref ref-type="bibr" rid="gks281-B59">59</xref>
,<xref ref-type="bibr" rid="gks281-B72">72</xref>
). Notably, the additional protein constituents of the complex modulate its transcriptional regulatory activity in a context-dependent manner (<xref ref-type="bibr" rid="gks281-B80">80</xref>
) and are linked to the development and/or progression of human hematologic malignancies (<xref ref-type="bibr" rid="gks281-B81 gks281-B82 gks281-B83 gks281-B84">81–84</xref>
). Sophisticated ChIP-seq analyses in the HPC-7 multipotent hematopoietic cell line demonstrated that additional components co-localized with GATA-2 and Scl/TAL1 (<xref ref-type="bibr" rid="gks281-B85">85</xref>
). This analysis revealed 1015 regions of 200 bp or less in which Scl/TAL1, LYL1, LMO2, GATA-2, ERG, FLI-1 and RUNX1 occupancy was detected. As each of these factors is likely to engage additional important partners, considerably more work is required to understand the structure/function of these higher order chromatin complexes containing multiple master regulators of hematopoiesis.</p>
<p>GATA factor interplay appears to be a common mechanism for controlling developmental processes (<xref ref-type="bibr" rid="gks281-B36">36</xref>
,<xref ref-type="bibr" rid="gks281-B86">86</xref>
). During the development of erythrocytes, GATA-1 displaces GATA-2 from chromatin sites at target genes, and this GATA switch (defined as an exchange of different GATA factors at a chromatin site) is tightly coupled to an altered transcriptional output (<xref ref-type="bibr" rid="gks281-B53">53</xref>
,<xref ref-type="bibr" rid="gks281-B87 gks281-B88 gks281-B89 gks281-B90">87–90</xref>
) (<xref ref-type="fig" rid="gks281-F1">Figure 1</xref>
, Principle 4). GATA switches were first described at the <italic>Gata2</italic>
locus, at which GATA-1 binding instigates repression, thus explaining the differential GATA-1 and GATA-2 expression pattern during erythropoiesis (<xref ref-type="bibr" rid="gks281-B36">36</xref>
,<xref ref-type="bibr" rid="gks281-B87">87</xref>
). GATA-1 utilizes FOG-1 to displace GATA-2 from chromatin (<xref ref-type="bibr" rid="gks281-B56">56</xref>
). The capacity of FOG-1 to bind the NuRD complex is required for the GATA switch, as GATA switches were impaired in a knock-in mouse strain expressing FOG-1 defective in NuRD complex binding (<xref ref-type="bibr" rid="gks281-B62">62</xref>
). Ectopic FOG-1 expression in mast cell progenitors induces a GATA switch in which GATA-1 replaces GATA-2 from the –2.8 kb GATA switch site of the <italic>Gata2</italic>
locus, which was linked to <italic>Gata2</italic>
repression and generation of erythroid, megakaryocytic and granulocytic progeny (<xref ref-type="bibr" rid="gks281-B97">97</xref>
). During the differentiation of trophoblast giant cells, GATA-2 displaces GATA-3 at <italic>Gata2</italic>
, which is associated with transcriptional activation (<xref ref-type="bibr" rid="gks281-B91">91</xref>
). Though GATA switches have not been studied in many systems, it is attractive to propose that they represent common devices to change transcriptional activity in diverse biological contents.</p>
<p>Two aspects of the GATA switch paradigm merit careful consideration. First, erythroid GATA switches inform us that different GATA factors can exert qualitatively distinct functions through an identical chromatin site; one GATA factor mediates target gene activation, while the other confers repression or vice versa. Thus, while different GATA factors share certain biochemical attributes, including their highly conserved zinc finger module (<xref ref-type="bibr" rid="gks281-B92">92</xref>
), intrinsic differences underlie the qualitatively distinct activities. A notable difference is the relative high and low stabilities of GATA-1 and GATA-2, respectively (<xref ref-type="bibr" rid="gks281-B93">93</xref>
,<xref ref-type="bibr" rid="gks281-B94">94</xref>
). As proteasome inhibition stabilizes GATA-2 and blocks GATA switches, the low stability appears to be an important determinant of GATA switches (<xref ref-type="bibr" rid="gks281-B93">93</xref>
). Another important implication of the GATA switch paradigm is that GATA switches and the requisite factors/signals that control the switches represent a novel tool to control developmental processes. Since certain non-hematopoietic cell types can express multiple GATA factors, it would not be surprising if the erythroid GATA switch mechanism were applicable to non-hematopoietic contexts. Despite major progress in elucidating GATA factor mechanistic principles, many questions remain unanswered regarding how cellular signaling pathways dynamically control GATA factor activities and GATA factor-dependent biological processes.</p>
<p>In summary, GATA factor mechanistic principles (<xref ref-type="fig" rid="gks281-F1">Figure 1</xref>
) include: (1) GATA factors target a small subset of chromatin sites containing a cis-element with the consensus sequence WGATAA; (2) GATA-1 activates or represses target genes in a FOG-1-dependent or -independent manner; (3) GATA-1 and GATA-2 commonly co-occupy chromatin sites with Scl/TAL1, and members of the Scl/TAL1 complex promote or suppress GATA factor-regulated transcription in a context-dependent manner; and (4) GATA switches can involve qualitatively distinct activities of different GATA factors through an identical chromatin site.</p>
</sec>
<sec><title>REGULATING GATA FACTORS POSTTRANSLATIONALLY</title>
<p>While multiple posttranslational modifications are implicated in regulating GATA factor function, progress on defining the respective mechanisms does not seem to be commensurate with the level of activity in the field. Common themes have not emerged regarding how posttranscriptional mechanisms regulate different GATA factors. Furthermore, the precise impact of most posttranslational modifications on GATA factor activities, including chromatin occupancy, coregulator recruitment, GATA switches and higher order chromatin transitions at endogenous loci is unknown.</p>
<p>GATA-1 harbors seven serines that can be phosphorylated in cultured cells (<xref ref-type="bibr" rid="gks281-B98">98</xref>
). Six of these serines (S26, S49, S72, S142, S178 and S187) reside in the N-terminal region, while another (S310) is near the C-finger. S72, S142 and S310 are conserved among multiple species. Whereas six serines in the N-terminal region are constitutively phosphorylated, S310 phosphorylation is elevated upon dimethyl sulfoxide (DMSO)-induced differentiation of mouse erythroleukemia (MEL) cells (<xref ref-type="bibr" rid="gks281-B98">98</xref>
). Substitution of all seven serines with alanines does not affect GATA-1 binding to naked DNA or transactivation activity in a non-erythroid cell transient transfection assay (<xref ref-type="bibr" rid="gks281-B98">98</xref>
). S310 resides in the region implicated in DNA bending, based on GATA-1 C-finger peptide binding to DNA (<xref ref-type="bibr" rid="gks281-B38">38</xref>
), but S310 mutations do not affect DNA bending (<xref ref-type="bibr" rid="gks281-B98">98</xref>
). Though mutation of S310 blocks fetal liver erythroid progenitor cell maturation (<xref ref-type="bibr" rid="gks281-B99">99</xref>
), mice bearing alanine substitutions at S72, S142 and S310 exhibit a normal phenotype, save moderately decreased erythroid burst-forming unit (BFU-E) and erythroid colony-forming unit (CFU-E) in bone marrow (<xref ref-type="bibr" rid="gks281-B100">100</xref>
). Phosphorylation of these residues is therefore either not essential for murine erythropoiesis or undefined mechanisms compensate for loss of phosphorylation sites <italic>in vivo</italic>
. Treatment of K562 cells with hemin, sodium butyrate (NaB) or N-acetylcysteine increases GATA-1 phosphorylation and enhances DNA binding <italic>in vitro</italic>
, but the phosphorylated residues mediating this effect are unknown (<xref ref-type="bibr" rid="gks281-B101">101</xref>
). Mitogen-activated protein kinase (MAPK)-mediated phosphorylation of S26 in interleukin 3 (IL-3)-dependent Ba/F3 hematopoietic cells increases expression of <italic>E4bp4</italic>
and <italic>Bcl-X<sub>L</sub>
</italic>
survival genes in a transient transfection assay (<xref ref-type="bibr" rid="gks281-B102">102</xref>
). Erythropoietin induces S310 phosphorylation via phosphatidylinositol 3-kinase (PI3K)/Akt (<xref ref-type="bibr" rid="gks281-B103">103</xref>
), and this enhances expression of <italic>TIMP-1</italic>
, which encodes tissue-inhibitor of metalloproteinase-1 (<xref ref-type="bibr" rid="gks281-B103">103</xref>
). Since multiple kinases phosphorylate GATA-1, and GATA-1 phosphorylation is regulated in distinct contexts, it is attractive to consider how extracellular stimuli, such as hematopoietic cytokines, instigate cellular signaling mechanisms that orchestrate GATA factor function in physiological and pathophysiological states. However, the triple phosphorylation site knockin mouse described above did not reveal compelling insights in this regard.</p>
<p>IL-3 induces GATA-2 phosphorylation in hematopoietic progenitor cell lines, which is dependent upon MAPK. However, the phosphorylated residues were not described (<xref ref-type="bibr" rid="gks281-B104">104</xref>
). In transiently transfected COS cells, GATA-2 phosphorylation does not affect reporter gene activity (<xref ref-type="bibr" rid="gks281-B104">104</xref>
). Insulin treatment of HEK293 cells stimulates PI3-K/Akt signaling, which induces GATA-2 phosphorylation at serine 401 (<xref ref-type="bibr" rid="gks281-B105">105</xref>
). Serine 401 phosphorylation was reported to impair nuclear translocation, based on overexpression of the mutant in HEK293 cells (<xref ref-type="bibr" rid="gks281-B105">105</xref>
). In addition, naked DNA-binding studies suggested that serine 401 phosphorylation impairs GATA-2 DNA-binding activity (<xref ref-type="bibr" rid="gks281-B105">105</xref>
). Additional work is required to discover the full ensemble of GATA-2 phosphorylation sites, relevant kinases and functional consequences of phosphorylation in distinct cell types <italic>in vivo</italic>
.</p>
<p>Analogous to phosphorylation, posttranslational acetylation of the ε-amino group of lysine represents a common mode of controlling protein structure/function (<xref ref-type="bibr" rid="gks281-B105 gks281-B106 gks281-B107 gks281-B109">106–109</xref>
). Acetylation of histone and non-histone proteins (<xref ref-type="bibr" rid="gks281-B110">110</xref>
) is mediated by a host of histone acetyltransferases (HATs) or histone deacetylases (HDACs). Through recruitment to chromatin via binding <italic>trans</italic>
-acting factors (<xref ref-type="bibr" rid="gks281-B111">111</xref>
), HATs acetylate the N-terminal flexible tails of core histones in nucleosomes at specific genetic loci. Molecular consequences of histone acetylation include neutralizing the lysine positive charge, which reduces the histone affinity for DNA and increases <italic>cis</italic>
-element accessibility to their cognate binding protein. Histone acetylation can also increase chromatin accessibility by opposing higher order chromatin folding (<xref ref-type="bibr" rid="gks281-B112">112</xref>
). Finally, acetyl-lysine binds a protein module termed a bromodomain (<xref ref-type="bibr" rid="gks281-B113">113</xref>
), thus creating a platform for protein recognition (<xref ref-type="bibr" rid="gks281-B114">114</xref>
,<xref ref-type="bibr" rid="gks281-B115">115</xref>
).</p>
<p>GATA factors contain multiple acetylation sites located predominantly within their zinc finger regions. The Adenovirus E1A-binding region of the HATs CREB-binding protein (CBP) (<xref ref-type="bibr" rid="gks281-B116">116</xref>
) and its paralog p300 (<xref ref-type="bibr" rid="gks281-B117">117</xref>
) bind and acetylate the GATA-1 C-finger (<xref ref-type="bibr" rid="gks281-B118">118</xref>
). Studies with the CBP/p300 inhibitor E1A provided evidence for an important role of CBP/p300 in erythroid maturation and gene regulation (<xref ref-type="bibr" rid="gks281-B118">118</xref>
). Two lysine-rich motifs (amino acids 243–246 and 312–315) at the C-terminus of the GATA-1 zinc fingers are acetylated (<xref ref-type="bibr" rid="gks281-B119">119</xref>
). GATA-1 acetylation facilitates transactivation in transient transfection assays (<xref ref-type="bibr" rid="gks281-B119">119</xref>
) and promotes GATA-1 chromatin occupancy (<xref ref-type="bibr" rid="gks281-B95">95</xref>
). Acetylated GATA-1 binds and recruits Bromodomain Protein 3 (BRD3) to chromatin (<xref ref-type="bibr" rid="gks281-B120">120</xref>
). As a small molecule inhibitor that antagonizes this interaction reduces GATA-1 and BRD3 chromatin occupancy and decreases erythroid maturation of G1E-ER4 cells, it will be interesting to further explore the mechanistic and biological implications of this interaction. GATA-1 recruits CBP/p300 to chromatin sites, including the β-globin LCR and <italic>βmajor</italic>
promoter, and presumably this underlies GATA-1-dependent induction of H3 and H4 acetylation at these sites (<xref ref-type="bibr" rid="gks281-B120 gks281-B121 gks281-B123">121–123</xref>
).</p>
<p>GATA-2 is acetylated at K102 within the N-terminal region and at multiple additional lysines within the zinc finger module including K281, 285, 334, 336, 389, 390, 399, 403, 405, 406, 408 and 409 (<xref ref-type="bibr" rid="gks281-B124">124</xref>
) (<xref ref-type="fig" rid="gks281-F2">Figure 2</xref>
). p300-mediated acetylation of GATA-2 in hematopoietic cells enhances its DNA binding and transactivation activities in a transient transfection assay and inhibits GATA-2-mediated growth inhibition (<xref ref-type="bibr" rid="gks281-B124">124</xref>
). A GATA-2 mutant lacking four lysine acetylation sites, C-terminal to the C-finger, was unable to rescue primitive erythropoiesis in GATA-2 morphant <italic>Xenopus</italic>
tadpoles (<xref ref-type="bibr" rid="gks281-B125">125</xref>
). In this system, Ca<sup>+2</sup>
-calmodulin-dependent kinase-4 signaling inhibits GATA-2 acetylation and function (<xref ref-type="bibr" rid="gks281-B125">125</xref>
). Thus, signal-dependent control of GATA-2 acetylation appears to represent an important mode of regulating GATA-2 activity. HDAC3 and HDAC5, but not HDAC1, bind GATA-2, suppressing GATA-2 transactivation activity in HEK293T cells (<xref ref-type="bibr" rid="gks281-B126">126</xref>
).
<fig id="gks281-F2" position="float"><label>Figure 2.</label>
<caption><p>GATA-2 mutations in human hematologic disorders (<xref ref-type="bibr" rid="gks281-B143 gks281-B144 gks281-B145 gks281-B146">143–146</xref>
). Specific GATA-2 mutations in human patients are indicated, with details denoted in the legend. Each symbol represents a single patient with the particular mutation. The diagram of GATA-2 protein organization illustrates the N- and C-fingers, acetylation sites (<xref ref-type="bibr" rid="gks281-B124">124</xref>
), the serine 401 phosphorylation site and two sumoylation consensus motifs. The diagram at the bottom illustrates the amino acid sequence composition of the C-finger and neighboring regions, with the positions of disease mutations highlighted. Stop, mutation that creates stop codon; frs, frameshift mutation; del, deletion.</p>
</caption>
<graphic xlink:href="gks281f2"></graphic>
</fig>
</p>
<p>Certain posttranslational modifications involve the conjugation of small proteins, including ubiquitin and related small ubiquitin-related modifier (SUMO) proteins, to recipient proteins. The four vertebrate SUMO proteins are ∼10 kDa and structurally resemble ubiquitin (<xref ref-type="bibr" rid="gks281-B127">127</xref>
,<xref ref-type="bibr" rid="gks281-B128">128</xref>
). While SUMO-2 and SUMO-3 share >90% sequence identity, SUMO-1 is only 50% identical to SUMO-2/3 (<xref ref-type="bibr" rid="gks281-B129">129</xref>
). SUMO-4 has sequence similarity to SUMO-2, but endogenous SUMO-4 has not been detected (<xref ref-type="bibr" rid="gks281-B130">130</xref>
). Sumoylation, which covalently links SUMO to a lysine within a target protein, is reversible and dynamically regulated (<xref ref-type="bibr" rid="gks281-B131">131</xref>
). Sumoylation involves an enzymatic cascade, analogous to ubiquitination (<xref ref-type="bibr" rid="gks281-B132">132</xref>
). The E1 activating enzyme Aos1-Uba2 forms a thioester bond with SUMO in an ATP-dependent reaction and subsequently transfers SUMO to the E2 conjugating enzyme Ubc9. An E3 ligase facilitates the transfer of SUMO to its substrate and an isopeptide bond is formed between the C-terminal glycine residue and the ε–amino group of a lysine residue of the acceptor protein. Conjugating enzymes and SUMO-specific proteases regulate the level of sumoylation. Six mammalian sentrin/SUMO-specific protease (SENP) homolog (SENP1–3, SENP5–7) have been identified (<xref ref-type="bibr" rid="gks281-B133">133</xref>
). Whereas polyubiquitination triggers proteasome-mediated proteolysis, sumoylation commonly controls protein–protein interactions by regulating the activity, localization and stability of target proteins, masking an existing binding site, occluding a site for a distinct modification or providing an interface for interaction with proteins containing a SUMO-interacting/binding motif (SIM/SBM) (<xref ref-type="bibr" rid="gks281-B134">134</xref>
).</p>
<p>GATA-1, GATA-2 and GATA-4 sumoylation have been described (<xref ref-type="bibr" rid="gks281-B135 gks281-B136 gks281-B137">135–137</xref>
). Though most sumoylation substrates contain the consensus motif ΨKXE (<xref ref-type="bibr" rid="gks281-B138">138</xref>
) (Ψ, large hydrophobic amino acid; X, any amino acid), some SUMO targets lack this consensus, and experimental analysis is required to determine whether a consensus is a <italic>bona fide</italic>
sumoylation site <italic>in vivo</italic>
. GATA-1 is sumoylated at K137, which is embedded in a sumoylation consensus, within the N-terminal region. The SUMO ligase PIASy can sumoylate K137 (<xref ref-type="bibr" rid="gks281-B136">136</xref>
). Initial analyses using a transient transfection assay in non-erythroid cells and a <italic>Xenopus</italic>
animal cap explant assay suggested that the K137R mutant and wild-type GATA-1 have similar activities (<xref ref-type="bibr" rid="gks281-B136">136</xref>
). PIASy binds GATA-1 and was reported to repress GATA-1-mediated transactivation via a K137-independent mechanism in a transient transfection assay with overexpressed factors. In genetic complementation analysis in GATA-1-null erythroid precursor (G1E) cells expressing GATA-1 fused with an estrogen-receptor ligand-binding domain (ER-GATA-1) at near physiological levels, K137 sumoylation promotes GATA-1-mediated transcriptional regulation (both activation and repression) at a subset of endogenous GATA-1 target genes (<xref ref-type="bibr" rid="gks281-B139">139</xref>
). SUMO-dependent genes are predominantly FOG-1-dependent targets. The GATA-1 V205G mutant, defective in FOG-1 binding, yields molecular phenotypes similar to the K137R mutant. Furthermore, SUMO-and FOG-1-dependent genes migrate away from the nuclear periphery upon GATA-1-induced erythroid maturation, while SUMO- and FOG-1-independent genes persist at the periphery (<xref ref-type="bibr" rid="gks281-B139">139</xref>
). The use of tiled bacterial artificial chromosome probes revealed that sumoylation endows GATA-1 with the capacity to expel the β-globin locus from the nuclear periphery without inducing gross changes in the positioning of neighboring chromosomal regions (<xref ref-type="bibr" rid="gks281-B140">140</xref>
). Given these mechanistic insights, it is of considerable interest to investigate how SUMO-specific proteases fit into the GATA factor regulatory circuitry. SENP1 knockout mice die from severe anemia between E13.5 and postnatal day 1 (<xref ref-type="bibr" rid="gks281-B141">141</xref>
). SENP1 knockout mice exhibit hematopoietic defects in the fetal liver, which correlate with accumulation of sumoylated GATA-1, as well as hypoxia-inducible factor-1α. As SENP1 desumoylates a broad spectrum of substrates, the hematopoietic defects presumably reflect the aggregate actions of this broad activity, presumably including FOG-1, which is sumoylated in erythroid cells (<xref ref-type="bibr" rid="gks281-B142">142</xref>
).</p>
<p>GATA-2 interacts with PIASy in transfected COS cells, which preferentially conjugates SUMO-2 to GATA-2 (<xref ref-type="bibr" rid="gks281-B135">135</xref>
). In a transient transfection assay in endothelial cells, PIASy suppresses GATA-2 transcriptional activity at the <italic>endothelin-1</italic>
(<italic>ET-1</italic>
) promoter. Whereas the repression requires the GATA-2-PIASy interaction, the PIASy RING-like domain with SUMO ligase activity is dispensable, indicating that PIASy regulates GATA factor activity independent of sumoylation. While GATA-2 contains two potential sumoylation sites (human amino acids 221–224 and 388–391) that conform to the consensus (<xref ref-type="fig" rid="gks281-F2">Figure 2</xref>
), the sumoylation site has not been described. Further analysis is required to elucidate the function of GATA-2 sumoylation at endogenous loci. GATA-4 is sumoylated at K366 in the C-terminal region (<xref ref-type="bibr" rid="gks281-B137">137</xref>
). Based on the initial evidence for functional significance of at least certain GATA-1 and GATA-2 posttranslational modifications, it is attractive to propose that signal-dependent targeting of GATA factors represents a canonical mode of regulating hematopoiesis. By contrast to well-established cytoplasmic to nuclear signaling paradigms, many questions remain unanswered regarding the nature of the signaling pathways that target GATA factors, the precise molecular consequences of the posttranslational modifications and how dysregulated signaling, often a hallmark of hematologic malignancies, influences GATA factor activity.</p>
</sec>
<sec><title>HUMAN PATHOPHYSIOLOGIES CAUSED BY GATA-2 DYSREGULATION</title>
<p>Given the essential GATA-2 function to promote hematopoiesis, alterations in GATA-2 levels/activity would be expected to initiate and/or promote the development of hematologic malignancies. However, until recently, only circumstantial evidence implicated GATA-2 in human cancers. Four related human disease syndromes harboring germline mutations in <italic>GATA2</italic>
are associated with an increased incidence of myeloid neoplasia, either myelodysplastic syndrome (MDS) or acute myeloid leukemia (AML). Three of the four syndromes—Monocytopenia/Mycobacterium avium complex (MonoMAC) (<xref ref-type="bibr" rid="gks281-B143">143</xref>
,<xref ref-type="bibr" rid="gks281-B144">147</xref>
), Dendritic cell, monocyte, B and Natural Killer Lymphoid deficiency (DCML deficiency) (<xref ref-type="bibr" rid="gks281-B143">144</xref>
) and Emberger’s syndrome (<xref ref-type="bibr" rid="gks281-B145">145</xref>
,<xref ref-type="bibr" rid="gks281-B148">148</xref>
)—share the hallmark feature of immune dysfunction with an increased propensity to develop MDS or AML. The fourth, a familial MDS/AML, lacks the immune dysfunction and systemic symptomatology characteristic of the other cases (<xref ref-type="bibr" rid="gks281-B146">146</xref>
). Though these entities appear to be rare, their study provides new insight into the role of <italic>GATA2</italic>
in immune function and in the regulation of growth, maturation and apoptosis in the myeloid compartment.</p>
<p>Sequencing of candidate gene exons in the genomic DNA of pedigrees of familial MDS/AML revealed a T354M <italic>GATA2</italic>
mutation in three pedigrees and a T355del in one pedigree (<xref ref-type="bibr" rid="gks281-B146">146</xref>
). This analysis also revealed several pedigrees harboring mutations in <italic>RUNX1</italic>
or <italic>CEBPA</italic>
, disease genes for familial AML (<xref ref-type="bibr" rid="gks281-B149">149</xref>
). Molecular modeling suggested that T354 and T355 stabilize the GATA-2 C-finger (<xref ref-type="bibr" rid="gks281-B146">146</xref>
). The T354M mutant exhibits lower affinity for DNA, reduced transactivation activity and is less effective in synergizing with PU.1 to activate the CSF1R (<italic>Fms</italic>
) promoter in a transient transfection assay (<xref ref-type="bibr" rid="gks281-B146">146</xref>
). When tested for the ability to block ATRA-induced maturation and apoptosis of HL-60 cells, the T355del mutant acted as a null, while the T354M mutant blocked ATRA effects, consistent with expectations for a leukemogenic oncogene. Based on gene expression profiling in HL-60 cells, the T354M and T355del mutants appeared to be null alleles (<xref ref-type="bibr" rid="gks281-B146">146</xref>
). Two additional pedigrees harboring the T354M mutation were recently reported (<xref ref-type="bibr" rid="gks281-B150">150</xref>
,<xref ref-type="bibr" rid="gks281-B151">151</xref>
). Further mechanistic analysis is required to rigorously analyze the function of these disease mutants at endogenous loci and in diverse cellular contexts.</p>
<p>Holland’s group had previously described a syndrome of monocytopenia with susceptibility to opportunistic infections by the <italic>Mycobacterium avium</italic>
complex, termed MonoMAC (<xref ref-type="bibr" rid="gks281-B143">143</xref>
,<xref ref-type="bibr" rid="gks281-B147">147</xref>
), which occurs in both sporadic and autosomal dominant familial form. The immune deficiencies were significant: patients suffered from disseminated cutaneous human papilloma virus infection, aspergillosis, histoplasmosis or cryptococcal meningitis. In addition, some suffered from pulmonary alveolar proteinosis, which is typically associated with macrophage dysfunction. Patients had markedly diminished circulating monocytes (10 cells per microliter, average), as well as B cells and natural killer (NK) cells; T cells were variable (<xref ref-type="bibr" rid="gks281-B147">147</xref>
). Other causes typically associated with the particular spectrum of immune defect seen in these patients (e.g. HIV infection, IL12/IL23/IFNg or NF-κB dysfunction) were ruled out (<xref ref-type="bibr" rid="gks281-B147">147</xref>
).</p>
<p>The frequency of myeloid neoplasia (MDS or AML) in the combined familial and sporadic cases of MonoMAC was 50%; these were associated with trisomy 8, monosomy 7 and dicentric chromosome 6 (<xref ref-type="bibr" rid="gks281-B147">147</xref>
). Given the <italic>GATA2</italic>
mutations in familial MDS/AML (<xref ref-type="bibr" rid="gks281-B146">146</xref>
), the authors investigated such mutations in the MonoMAC kindreds, 13 of the 16 they originally reported. This revealed frameshift mutations (G81fs, M1del290, D259fs and N317fs), a deletion spanning the N- and C-fingers (D340–381), a small deletion in the C-finger (Δ362–365) and missense mutations within the GATA-2 C-finger (T354M, N371K, R396W, R396Q, R398W) (<xref ref-type="bibr" rid="gks281-B143">143</xref>
). In addition, one missense mutation occurred outside the finger region: P254L.</p>
<p>Bigley <italic>et al</italic>
. (<xref ref-type="bibr" rid="gks281-B152">152</xref>
) further characterized the immune deficiency in four patients with MonoMAC syndrome, referring to it as DCML deficiency. DCML is associated with the absence of granulocyte monocyte progenitors (GMPs) and common lymphoid progenitors (CLPs) (<xref ref-type="bibr" rid="gks281-B152">152</xref>
). As expected, with long latency, DCML can lead to MDS (<xref ref-type="bibr" rid="gks281-B153">153</xref>
,<xref ref-type="bibr" rid="gks281-B154">154</xref>
). Exome sequencing revealed <italic>GATA2</italic>
mutations in these four patients: a frame shift after amino acid 200; a T354M missense mutation; a R398W missense mutation and a D340–381 deletion spanning the C-terminal end of the N-finger, extending into the C-finger (<xref ref-type="bibr" rid="gks281-B144">144</xref>
).</p>
<p>Emberger’s syndrome is characterized by lymphedema with myelodysplasia progressing to AML, as well as immune dysfunction (widespread cutaneous warts and sensoneural deafness) (<xref ref-type="bibr" rid="gks281-B148">148</xref>
). Whole-exome sequencing of three individuals with Emberger syndrome revealed <italic>GATA2</italic>
mutations, and further analysis of additional cases of Emberger syndrome (four more sporadic cases and additional individuals from the two affected kindreds) revealed additional <italic>GATA2</italic>
mutations (<xref ref-type="bibr" rid="gks281-B145">145</xref>
). These mutations span from the N-terminus to the C-finger, and include five frame shift mutations, one nonsense mutation and two missense mutations within the C-finger (R361L and C373R) (<xref ref-type="bibr" rid="gks281-B145">145</xref>
). Using a luciferase reporter bearing a GATA-2-responsive CD34 promoter construct transfected into HEK293 cells, they demonstrated that the R361L and C373R mutants have a decreased capacity to transactivate the reporter. However, the molecular basis for the defective activity was not established.</p>
<p>It is instructive to consider the mechanistic basis of the immune deficiency in MonoMAC/DCML deficiency and Emberger’s syndrome. It is unlikely that the myeloid neoplasia in these patients yields immune dysfunction, since the spectrum of opportunistic infections is distinct from that seen in the neutropenia of MDS, but is similar to that seen in IRF8 deficiency and IFNgamma/IL-12 deficiency. There are several clues that through its interaction with PU.1 (<xref ref-type="bibr" rid="gks281-B155">155</xref>
), GATA-2 plays an important role in monocyte/macrophage/dendritic cell development. First, GATA-2 controls phagocytosis by pulmonary alveolar macrophages (<xref ref-type="bibr" rid="gks281-B156">156</xref>
), and pulmonary alveolar proteinosis is a feature of the MonoMAC syndrome. Second, with haploinsufficient GATA-2 mice, there is loss of lymphoid and monocytic cells with retention of granulocytes (<xref ref-type="bibr" rid="gks281-B32">32</xref>
). Furthermore, there are specific defects in the granulocyte/macrophage progenitor pool (<xref ref-type="bibr" rid="gks281-B157">157</xref>
). GATA-2 interacts with and represses PU.1 (<xref ref-type="bibr" rid="gks281-B158">158</xref>
), which induces <italic>c-Fms</italic>
and <italic>Flt3</italic>
expression (<xref ref-type="bibr" rid="gks281-B159">159</xref>
,<xref ref-type="bibr" rid="gks281-B160">160</xref>
). The common developmental origin for macrophage/dendritic cells and lymphoid cells (<xref ref-type="bibr" rid="gks281-B161">161</xref>
) may tie together the deficiencies in B and NK cells seen in MonoMAC patients. In addition to PU.1, GATA-2 can bind C/EBP-α (<xref ref-type="bibr" rid="gks281-B162">162</xref>
), a key regulator of granulopoiesis. Whether GATA-2 disease mutations affect this interaction, thereby altering C/EBP-α function, has not been addressed.</p>
<p>Regarding mechanisms underlying the pathogenic activities of mutant <italic>GATA2</italic>
alleles, do the proteins function as null alleles? Dickinson <italic>et al</italic>
. posit that the frameshift and 42 amino acid deletions act as null alleles, though N-terminal frameshifts in <italic>GATA1</italic>
(associated with AML) can be translated through initiation at a downstream codon, resulting in the production of an N-terminally truncated mutant with reduced activity (<xref ref-type="bibr" rid="gks281-B50">50</xref>
); whether this happens with GATA-2 frameshift mutations is not known. Strikingly, nearly all the point mutations identified in these four papers localize to the <italic>GATA2</italic>
C-finger. Initial mechanistic analyses (<xref ref-type="bibr" rid="gks281-B146">146</xref>
) suggested that the T354M and T355del alleles exhibit certain functional differences. While we propose that these mutations lead to haploinsufficiency, considerably more work is required to evaluate functional consequences of the mutations.</p>
<p>Are there links between the immune deficiency and MDS/AML? It was suggested that the increased incidence of MDS in patients with GATA-2 mutation-induced MonoMAC syndrome may result from defective regulation of HSC proliferation: in the face of systemic immune dysfunction and recurrent infection, the stem cell compartment is stimulated to proliferate, and since committed progenitors are also dysfunctional due to GATA-2 haploinsufficiency, this leads to chronic stress on the HSC compartment, HSC exhaustion and MDS (<xref ref-type="bibr" rid="gks281-B163">163</xref>
). GATA-2 haploinsufficient mice have a decreased stem cell pool, with a higher percentage of quiescent LSK cells and increased apoptosis (<xref ref-type="bibr" rid="gks281-B32">32</xref>
). The immune deficiency and MDS/AML may not be linked, since GATA-2 mutations alone, independent of immune dysfunction, may lead to MDS/AML (<xref ref-type="bibr" rid="gks281-B146">146</xref>
). The presence of chromosomal aberrations (trisomy 8 and 21, monosomy 7 and dicentric chromosome 6 (<xref ref-type="bibr" rid="gks281-B147">147</xref>
) suggest that additional events are needed for malignancy to develop and/or GATA-2 mutations increase the likelihood of these mutagenic events occurring. These points may explain the long latency for the development of this set of syndromes and the low penetrance of MDS/AML development. Alternatively, the long latency and variable penetrance may be due to the time required for subtle deregulation of hematopoiesis to segue to a full-blown malignancy.</p>
<p>GATA-2 expression can be upregulated in AML, and this portends a poor prognosis (<xref ref-type="bibr" rid="gks281-B164 gks281-B165 gks281-B166 gks281-B167">164–167</xref>
). By contrast, GATA-2 can be downregulated in murine retroviral transplant models of AML, and forced GATA-2 expression did not sustain leukemic cell growth (<xref ref-type="bibr" rid="gks281-B168">168</xref>
). GATA2 has been identified as a common site of proviral insertional activation in AMLs occurring in retrovirally infected NUP98-HOXD13 transgenic mice (<xref ref-type="bibr" rid="gks281-B169">169</xref>
). Zhang <italic>et al</italic>
. (<xref ref-type="bibr" rid="gks281-B170">170</xref>
) identified a gain-of-function GATA-2 mutation occurring in the accelerated phase (AP) and blast crisis (BC) phase of CML (<xref ref-type="bibr" rid="gks281-B170">170</xref>
). They analyzed 85 cases of CML in either accelerated phase or blast crisis for genetic alterations in any of 13 candidate genes of known importance to hematopoiesis or tumor progression. Eleven of these had mutations in Runx1 (AML1), while eight had a L359V mutation. Another case had a six amino acid internal deletion (D341–346). Both these reside in the C-finger. Kaplan–Meier-type analysis of patients with the L359V mutation showed a statistically significant shortening of time to disease progression. Though more work needs to be done to establish the mechanism, Zhang <italic>et al</italic>
. provide initial evidence that the L359V mutant acts as a dominant-active allele: it appears to bind naked DNA more tightly; to bind to PU.1 more tightly, and to more strongly inhibit PU.1-mediated transactivation on target promoters; it had a modest inhibitory effect on vitamin D3 and all-trans retinoic acid differentiation of HL-60 cells and caused BCR-ABL-transduced primary hematopoietic cells to take on a more monocytic phenotype (<xref ref-type="bibr" rid="gks281-B170">170</xref>
). Analysis of 688 DNA samples from patients with non-CML-AP/BC hematologic malignancies failed to identify sequence alterations in <italic>GATA2</italic>
, emphasizing that the L359V mutation is specific to AP/BC phase of CML (<xref ref-type="bibr" rid="gks281-B171">171</xref>
).</p>
</sec>
<sec><title>CONCLUDING REMARKS</title>
<p>Despite the emergence of compelling mechanistic principles, knowledge of how cellular signaling pathways regulate GATA factor activity remains primitive. Taken together with the many unanswered questions regarding how GATA-2 coding region mutations dysregulate GATA-2 function, major efforts are required to construct a lucid picture of how physiological GATA-2 activity suppresses the development of MDS and leukemia. Elucidating the cell type-specific regulatory circuitry in which GATA-2 is embedded, and careful scrutiny of the dynamics of this circuitry, will reveal key regulatory components/nodes that offer opportunities for innovative and efficacious targeted interventions. Given the rapidity of progress vis-à-vis linking GATA-2 dysregulation to hematologic pathophysiologies, and the ever-increasing ease in conducting whole-genome analyses, further rigorous explorations into this rich pipeline will almost certainly yield pivotal insights into the molecular basis of the human diseases discussed and more.</p>
</sec>
<sec><title>FUNDING</title>
<p><funding-source>National Institutes of Health (NIH)</funding-source>
(<award-id>DK68034</award-id>
, <award-id>DK50107</award-id>
to E.H.B., <award-id>CA120313</award-id>
to A.S.P.). H.-Y.L. was the recipient of an <funding-source>American Heart Association Predoctoral Fellowship</funding-source>
. Funding for open access charge: <funding-source>NIH</funding-source>
.</p>
<p><italic>Conflict of interest statement</italic>
. None declared.</p>
</sec>
</body>
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