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JOURNAL ARTICLES
Development of hematopoietic cells lacking transcription factor GATA-1
L. Pevny, C.S. Lin, V. D'Agati, M.C. Simon, S.H. Orkin, F. Costantini
Development 1995 121: 163-172;

Summary

GATA-1 is a zinc-finger transcription factor believed to play an important role in gene regulation during the development of erythroid cells, megakaryocytes and mast cells. Other members of the GATA family, which can bind to the same DNA sequence motif, are co-expressed in several of these hemopoietic lineages, raising the possibility of overlap in function. To examine the specific roles of GATA-1 in hematopoietic cell differentiation, we have tested the ability of embryonic stem cells, carrying a targeted mutation in the X-linked GATA-1 gene, to contribute to various blood cell types when used to produce chimeric embryos or mice. Previously, we reported that GATA-1- mutant cells failed to contribute to the mature red blood cell population, indicating a requirement for this factor at some point in the erythroid lineage (L. Pevny et al., (1991) Nature 349, 257–260). In this study, we have used in vitro colony assays to identify the stage at which mutant erythroid cells are affected, and to examine the requirement for GATA-1 in other lineages. We found that the development of erythroid progenitors in embryonic yolk sacs was unaffected by the mutation, but that the cells failed to mature beyond the proerythroblast stage, an early point in terminal differentiation. GATA-1- colonies contained phenotypically normal macrophages, neutrophils and megakaryocytes, indicating that GATA-1 is not required for the in vitro differentiation of cells in these lineages. GATA-1- megakaryocytes were abnormally abundant in chimeric fetal livers, suggesting an alteration in the kinetics of their formation or turnover. The lack of a block in terminal megakaryocyte differentiation was shown by the in vivo production of platelets expressing the ES cell-derived GPI-1C isozyme. The role of GATA-1 in mast cell differentiation was examined by the isolation of clonal mast cell cultures from chimeric fetal livers. Mutant and wild-type mast cells displayed similar growth and histochemical staining properties after culture under conditions that promote the differentiation of cells resembling mucosal or serosal mast cells. Thus, the mast and megakaryocyte lineages, in which GATA-1 and GATA-2 are co-expressed, can complete their maturation in the absence of GATA-1, while erythroid cells, in which GATA-1 is the predominant GATA factor, are blocked at a relatively early stage of maturation.

Reference

    1. Andrews N. C.,
    2. Erdjument-Bromage H.,
    3. Davidson M. B.,
    4. Tempst P.,
    5. Orkin S. H.
    (1993) Erythroid transcription factor NF-E2 is a haematopoietic-specific basic-leucine zipper protein. Nature 362, 722–728
    OpenUrlCrossRefPubMedWeb of Science
    1. Crotta S.,
    2. Nicolis S.,
    3. Ronchi A.,
    4. Ottolenghi S.,
    5. Ruzzi L.,
    6. Shimada Y.,
    7. Migliaccio A. R.,
    8. Migliaccio G.
    (1990) Progressive inactivation of the expression of an erythroid transcriptional factor in GM-and G-CSF-dependent myeloid cell lines. Nucleic Acids Res 18, 6863–6869
    OpenUrlAbstract/FREE Full Text
    1. Dai W.,
    2. Murphy M. J. J.
    (1993) Downregulation of GATA-1 expression during phorbol myristate acetate-induced megakaryocytic differentiation of human erythroleukemia cells. Blood 81, 1214–1221
    OpenUrlAbstract/FREE Full Text
    1. Evans T.,
    2. Felsenfeld G.
    (1989) The erythroid-specific transcription factor Eryf1: a new finger protein. Cell 58, 877–85
    OpenUrlCrossRefPubMedWeb of Science
    1. Galli S. J.
    (1993) New concepts about the mast cell. New England J. Med 328, 257–265
    OpenUrlCrossRefPubMedWeb of Science
    1. Ginsberg M. H.,
    2. Plow E. F.
    (1981) Fibronectin expression on the platelet surface occurs in concert with secretion. J. Supramol. Struct 17, 91–98
    1. Gurish M. F.,
    2. Ghildyal N.,
    3. McNeil H. P.,
    4. Austen K. F.,
    5. Gillis S.,
    6. Stevens R. L.
    (1992) Differential expression of secretory granule proteases in mouse mast cells exposed to interleukin 3 and c-kit ligand. J. Exp. Med 175, 1003–1012
    OpenUrlAbstract/FREE Full Text
    1. Ishizaka T.,
    2. Okodaira H.,
    3. Mauser L. E.,
    4. Ishizaka K.
    (1976) Development of rat mast cells in vitro. I. Differentiation of mast cells from thymus cells. J. Immunol 116, 747–754
    OpenUrlAbstract/FREE Full Text
    1. Jackson C. W.
    (1973) Cholinesterase as a possible marker for early cells of the megakaryocyte series. Blood 42, 413–421
    OpenUrlAbstract/FREE Full Text
    1. Jordan C. T.,
    2. McKearn J. P.,
    3. Lemischka I. R.
    (1990) Cellular and developmental properties of fetal hematopoietic stem cells. Cell 61, 953–963
    OpenUrlCrossRefPubMedWeb of Science
    1. Keller G.,
    2. Kennedy M.,
    3. Papayannopoulou T.,
    4. Wiles M. V.
    (1993) Hematopoietic commitment during embryonic stem cell differentiation in culture. Mol. Cell Biol 13, 473–486
    OpenUrlAbstract/FREE Full Text
    1. Kitamura Y.,
    2. Shimada M.,
    3. Go S.
    (1979) Presence of mast cell precursors in fetal liver of mice. Dev. Biol 70, 510–514
    OpenUrlCrossRefPubMed
    1. Ko L. J.,
    2. Engel J. D.
    (1993) DNA-binding specificities of the GATA transcription factor family. Mol. Cell Biol 13, 4011–4022
    OpenUrlAbstract/FREE Full Text
    1. Lemarchandel V.,
    2. Ghysdael J.,
    3. Mignotte V.,
    4. Rahuel C.,
    5. Romeo P. H.
    (1993) GATA and Ets cis-acting sequences mediate megakaryocyte-specific expression. Mol. Cell Biol 13, 668–676
    OpenUrlAbstract/FREE Full Text
    1. Leonard M.,
    2. Brice M.,
    3. Engel J. D.,
    4. Papayannopoulou T.
    (1993) Dynamics of GATA transcription factor expression during erythroid cell differentiation. Blood 82, 1071–1079
    OpenUrlAbstract/FREE Full Text
    1. Levi-Schaffer F.,
    2. Austen K. F.,
    3. Gravallese P. M.,
    4. Stevens R. L.
    (1986) Coculture of interleukin 3-dependent mouse mast cells with fibroblasts results in a phenotypic change of the mast cells. Proc. Natl. Acad. Sci. USA 83, 6485–6488
    OpenUrlAbstract/FREE Full Text
    1. Long M. W.,
    2. Smolen J. E.,
    3. Szczepanski P.,
    4. Boxer L. A.
    (1984) Role of phorbol diesters in in vitro murine megakaryocyte colony formation. J. Clin. Invest 74, 1686–1692
    1. Long M. W.,
    2. Williams N.
    (1982) Immature megakaryocytes in the mouse: morphology and quantitation by acetylcholinesterase staining. Blood 58, 1032–1039
    OpenUrlAbstract/FREE Full Text
    1. Martin D. I.,
    2. Zon L. I.,
    3. Mutter G.,
    4. Orkin S. H.
    (1990) Expression of an erythroid transcription factor in megakaryocytic and mast cell lineages. Nature 344, 444–447
    OpenUrlCrossRefPubMedWeb of Science
    1. Merika M.,
    2. Orkin S. H.
    (1993) DNA-binding specificity of GATA family transcription factors. Mol. Cell Biol 13, 3999–4010
    OpenUrlAbstract/FREE Full Text
    1. Miller I. J.,
    2. Bieker J. J.
    (1993) Identification of a novel, erythroid-specific murine transcription factor structurally related to the Kr_ppel family of nuclear proteins. Mol. Cell Biol 13, 2776–2786
    OpenUrlAbstract/FREE Full Text
    1. Mouthon M. A.,
    2. Bernard O.,
    3. Mitjavila M. T.,
    4. Romeo P. H.,
    5. Vainchenker W.,
    6. Mathieu M. D.
    (1993) Expression of tal-1 and GATA-binding proteins during human hematopoiesis. Blood 81, 647–655
    OpenUrlAbstract/FREE Full Text
    1. Nakahata T.,
    2. Spicer S. S.,
    3. Cantey J. R.,
    4. Ogawa M.
    (1982) Clonal assay of mouse mast cell colonies in methylcellulose culture. Blood 60, 352–361
    OpenUrlAbstract/FREE Full Text
    1. Nakano T.,
    2. Sonoda T.,
    3. Hayashi C.,
    4. Yamatodani A.,
    5. Kanayama Y.,
    6. Yamamura T.,
    7. Asai H.,
    8. Yonezawa T.,
    9. Kitamura Y.,
    10. Galli S. J.
    (1985) Fate of bone marrow-derived cultured mast cells after intracutaneous, intraperitoneal, and intravenous transfer into genetically mast cell-deficient w/w vmice. J. Exp. Med 162, 1025–1043
    OpenUrlAbstract/FREE Full Text
    1. Nocka K.,
    2. Majumder S.,
    3. Chabot B.,
    4. Ray P.,
    5. Cervone M.,
    6. Bernstein A.,
    7. Besmer P.
    (1989) Expression of c-kit gene products in known cellular targets of W mutations in normal and W mutant mice--evidence for an impaired c-kit kinase in mutant mice. Genes Dev 3, 816–826
    OpenUrlAbstract/FREE Full Text
    1. Orkin S. H.
    (1990) Cell-specific transcription and cell differentiation in the erythroid lineage. Curr. Opin. Cell Biol 2, 1003–1012
    OpenUrlCrossRefPubMed
    1. Orkin S. H.
    (1990) Globin gene regulation and switching: circa 1990. Cell 63, 665–672
    OpenUrlCrossRefPubMedWeb of Science
    1. Orkin S. H.
    (1992) GATA-binding transcription factors in hematopoietic cells. Blood 80, 575–581
    OpenUrlFREE Full Text
    1. Padua R. A.,
    2. Bulfield G.,
    3. Peters J.
    (1978) Biochemical genetics of a new glucosephosphate isomerase allele (Gpi-1c) from wild mice. Biochem. Genet 16, 127–143
    OpenUrlCrossRefPubMed
    1. Pevny L.,
    2. Simon M. C.,
    3. Robertson E.,
    4. Klein W. H.,
    5. Tsai S. F.,
    6. DAgati V.,
    7. Orkin S. H.,
    8. Costantini F.
    (1991) Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1. Nature 349, 257–260
    OpenUrlCrossRefPubMedWeb of Science
    1. Ravid K.,
    2. Doi T.,
    3. Beeler D. L.,
    4. Kuter D. J.,
    5. Rosenberg R. D.
    (1991) Transcriptional regulation of the rat platelet factor 4 gene: interaction between an enhancer/silencer domain and the GATA site. Mol. Cell Biol 11, 6116–27
    OpenUrlAbstract/FREE Full Text
    1. Rentrop M.,
    2. Knapp B.,
    3. Winter H.,
    4. Schweizer J.
    (1986) Aminoalkylsilane-treated glass slides as support for in situ hybridization of keratin cDNA to frozen tissue sections under varying fixation and pretreatment conditions. Histochem. J 18, 271–276
    OpenUrlCrossRefPubMedWeb of Science
    1. Romeo P. H.,
    2. Prandini M. H.,
    3. Joulin V.,
    4. Mignotte V.,
    5. Prenant M.,
    6. Vainchenker W.,
    7. Marguerie G.,
    8. Uzan G.
    (1990) Megakaryocytic and erythrocytic lineages share specific transcription factors. Nature 344, 447–449
    OpenUrlCrossRefPubMed
    1. Simon M. C.,
    2. Pevny L.,
    3. Wiles M. V.,
    4. Keller G.,
    5. Costantini F.,
    6. Orkin S. H.
    (1992) Rescue of erythroid development in gene targeted GATA-1-mouse embryonic stem cells. Nature Genetics 1, 92–98
    OpenUrlCrossRefPubMedWeb of Science
    1. Sonoda T.,
    2. Hayashi C.,
    3. Kitamura Y.
    (1983) Presence of mast cell precursors in the yolk sac of mice. Dev. Biol 97, 89–94
    OpenUrlCrossRefPubMedWeb of Science
    1. Sposi N. M.,
    2. Zon L. I.,
    3. Care A.,
    4. Valtieri M.,
    5. Testa U.,
    6. Gabbianelli M.,
    7. Mariana G.,
    8. Bottero L.,
    9. MAther C.,
    10. Orkin S. H.,
    11. Peschle C.
    (1992) Cell cycle-dependent initiation and lineage-dependent abrogation of GATA-1 expression in pure differentiating hematopoietic progenitors. Proc. Natl. Acad. Sci. USA 89, 6353–6357
    OpenUrlAbstract/FREE Full Text
    1. Tsai M.,
    2. Shih L.-S.,
    3. Newlands G. F. J.,
    4. Takeishi T.,
    5. Langley K. E.,
    6. Zsebo K. M.,
    7. Miller H. R. P.,
    8. Geissler E. N.,
    9. Galli S. J.
    (1991) The rat c-kit ligand, stem cell factor, induces the development of connective tissue-type and mucosal mast cells in vivo. J. Exp. Med 174, 125–131
    OpenUrlAbstract/FREE Full Text
    1. Tsai S. F.,
    2. Martin D. I.,
    3. Zon L. I.,
    4. DAndrea A. D.,
    5. Wong G. G.,
    6. Orkin S. H.
    (1989) Cloning of cDNA for the major DNA-binding protein of the erythroid lineage through expression in mammalian cells. Nature 339, 446–451
    OpenUrlCrossRefPubMed
    1. Visvader J. E.,
    2. Elefanty A. G.,
    3. Strasser A.,
    4. Adams J. M.
    (1992) GATA-1 but not SCL induces megakaryocytic differentiation in an early myeloid line. EMBO J 11, 4557–4564
    OpenUrlPubMedWeb of Science
    1. Weiss M. J.,
    2. Keller G.,
    3. Orkin S. H.
    (1994) Novel insights into erythroid development revealed through in vitro differentiation of GATA-1-embryonic stem cells. Genes Dev 8, 1184–1197
    OpenUrlAbstract/FREE Full Text
    1. West J. D.
    (1977) Red blood cell selection in chimeric mice. Exp. Hemat 5, 1–7
    OpenUrlPubMedWeb of Science
    1. Wiles M. V.,
    2. Keller G.
    (1991) Multiple hematopoietic lineages develop from embryonic stem (ES) cells in culture. Development 111, 259–267
    OpenUrlAbstract
    1. Wong P. M. C.,
    2. Chung S.-W.,
    3. Reicheld S. M.,
    4. Chui D. H. K.
    (1986) Hemoglobin switching during murine embryonic development: evidence for two populations of embryonic erythropoietic progenitor cells. Blood 67, 716–721
    OpenUrlAbstract/FREE Full Text
    1. Yam L. T.,
    2. Li C. Y.,
    3. Crosby W. H.
    (1971) Cytochemical identification of monocytes and granulocytes. Amer. J. Clin. Path 55, 283–290
    OpenUrlPubMedWeb of Science
    1. Yamamoto M.,
    2. Ko L. J.,
    3. Leonard M. W.,
    4. Beug H.,
    5. Orkin S. H.,
    6. Engel J. D.
    (1990) Activity and tissue-specific expression of the transcription factor NF-E1 multigene family. Genes Dev 4, 1650–1662
    OpenUrlAbstract/FREE Full Text
    1. Zon L. I.,
    2. Gurish M. F.,
    3. Stevens R. L.,
    4. Mather C.,
    5. Reynolds D. S.,
    6. Austen K. F.,
    7. Orkin S. H.
    (1991) GATA-binding transcription factors in mast cells regulate the promoter of the mast cell carboxypeptidase A gene. J. Biol. Chem 266, 22948–22953
    OpenUrlAbstract/FREE Full Text
    1. Zon L. I.,
    2. Tsai S. F.,
    3. Burgess S.,
    4. Matsudaira P.,
    5. Bruns G. A.,
    6. Orkin S. H.
    (1990) The major human erythroid DNA-binding protein (GF-1): primary sequence and localization of the gene to the X chromosome. Proc. Natl Acad. Sci. USA 87, 668–672
    OpenUrlAbstract/FREE Full Text
    1. Zon L. I.,
    2. Yamaguchi Y.,
    3. Yee K.,
    4. Albee E. A.,
    5. Kimura A.,
    6. Bennett J. C.,
    7. Orkin S. H.,
    8. Ackerman S. J.
    (1993) Expression of mRNA for the GATA-binding proteins in human eosinophils and basophils: potential role in gene transcription. Blood 81, 3234–3241
    OpenUrlAbstract/FREE Full Text
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JOURNAL ARTICLES
Development of hematopoietic cells lacking transcription factor GATA-1
L. Pevny, C.S. Lin, V. D'Agati, M.C. Simon, S.H. Orkin, F. Costantini
Development 1995 121: 163-172;
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