Abstract
Transcription factor GATA-1 is essential for red blood cell maturation and, therefore, for survival of developing mouse embryos. GATA-1 is also expressed in megakaryocytes, mast cells, eosinophils, multipotential hematopoietic progenitors and Sertoli cells of the testis, where its functions have been elusive. Indeed, interpretation of gene function in conventional knockout mice is often limited by embryonic lethality or absence of mature cells of interest, creating the need for alternate methods to assess gene function in selected cell lineages. Emerging strategies for conditional gene inactivation through site-specific recombinases rely on the availability of mouse strains with high fidelity of transgene expression and efficient, tissue-restricted DNA excision. In an alternate approach, we modified sequences upstream of the GATA-1 locus in embryonic stem cells, including a DNase I-hypersensitive region. This resulted in generation of mice with selective loss of megakaryocyte GATA-1 expression, yet sufficient erythroid cell levels to avoid lethal anemia. The mutant mice have markedly reduced platelet numbers, associated with deregulated megakaryocyte proliferation and severely impaired cytoplasmic maturation. These findings reveal a critical role for GATA-1 in megakaryocyte growth regulation and platelet biogenesis, and illustrate how targeted mutation of cis-elements can generate lineage-specific knockout mice.
MeSH Terms
Animals
Blood Platelets/cytology
Cell Division/genetics,physiology
Cell Lineage
DNA-Binding Proteins/genetics,physiology
Erythroid-Specific DNA-Binding Factors
Female
GATA1 Transcription Factor
Gene Expression Regulation
Gene Targeting
Male
Megakaryocytes/cytology
Mice
Mice, Knockout
Mutagenesis
Neomycin/pharmacology
Transcription Factors/genetics,physiology
Chemicals
DNA-Binding Proteins
Erythroid-Specific DNA-Binding Factors
GATA1 Transcription Factor
Gata1 protein, mouse
Transcription Factors
Neomycin
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Shivdasani R A
Department of Medicine, Dana-Farber Cancer Institute, Children's Hospital, Harvard Medical School, Boston, MA 02115, USA.
Fujiwara Y
McDevitt M A
Orkin S H
References (33)
33 references, click to expand
-
Phorbol diesters stimulate the development of an early murine progenitor cell. The burst-forming unit-megakaryocyte.
J Clin Invest. 1985 Aug;76(2):431-8
PMID: 3875629
-
GATA-1 reprograms avian myelomonocytic cell lines into eosinophils, thromboblasts, and erythroblasts.
Genes Dev. 1995 May 15;9(10):1250-62
PMID: 7758949
-
Altering the genome by homologous recombination.
Science. 1989 Jun 16;244(4910):1288-92
PMID: 2660260
-
Tissue-specific control elements of the Thy-1 gene.
EMBO J. 1990 Mar;9(3):833-40
PMID: 1968831
-
Thrombopoietin derived from human embryonic kidney cells stimulates an increase in DNA content of murine megakaryocytes in vivo.
Exp Hematol. 1990 Aug;18(7):758-63
PMID: 2199205
-
Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1.
Nature. 1991 Jan 17;349(6306):257-60
PMID: 1987478
-
Targeted insertion of exogenous DNA into the eukaryotic genome by the Cre recombinase.
New Biol. 1990 May;2(5):441-9
PMID: 2288914
-
Recombinase-mediated gene activation and site-specific integration in mammalian cells.
Science. 1991 Mar 15;251(4999):1351-5
PMID: 1900642
-
Cell-type-specific and hypoxia-inducible expression of the human erythropoietin gene in transgenic mice.
Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8725-9
PMID: 1924331
-
The -6.1-kilobase chicken lysozyme enhancer is a multifactorial complex containing several cell-type-specific elements.
Mol Cell Biol. 1992 May;12(5):2339-50
PMID: 1569954
-
Targeted mutation of the DNA methyltransferase gene results in embryonic lethality.
Cell. 1992 Jun 12;69(6):915-26
PMID: 1606615
-
GATA and Ets cis-acting sequences mediate megakaryocyte-specific expression.
Mol Cell Biol. 1993 Jan;13(1):668-76
PMID: 8417360
-
Erythroid transcription factor GATA-1 is abundantly transcribed in mouse testis.
Nature. 1993 Apr 1;362(6419):466-8
PMID: 8464479
-
Ectopic expression of a conditional GATA-2/estrogen receptor chimera arrests erythroid differentiation in a hormone-dependent manner.
Genes Dev. 1993 Jun;7(6):1097-109
PMID: 8504932
-
Deletion of a DNA polymerase beta gene segment in T cells using cell type-specific gene targeting.
Science. 1994 Jul 1;265(5168):103-6
PMID: 8016642
-
Classes of primitive murine megakaryocytic progenitor cells.
Exp Hematol. 1994 Sep;22(10):954-8
PMID: 8088378
-
Developmental stage- and spermatogenic cycle-specific expression of transcription factor GATA-1 in mouse Sertoli cells.
Development. 1994 Jul;120(7):1759-66
PMID: 7924983
-
Immortalization of multipotent growth-factor dependent hemopoietic progenitors from mice transgenic for GATA-1 driven SV40 tsA58 gene.
EMBO J. 1994 Oct 3;13(19):4577-86
PMID: 7925299
-
Distinct DNase-I hypersensitive sites are associated with TAL-1 transcription in erythroid and T-cell lines.
Blood. 1994 Dec 1;84(11):3819-27
PMID: 7949138
-
Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL.
Nature. 1995 Feb 2;373(6513):432-4
PMID: 7830794
-
Targeting gene expression to haemopoietic stem cells: a chromatin-dependent upstream element mediates cell type-specific expression of the stem cell antigen CD34.
EMBO J. 1995 Feb 1;14(3):564-74
PMID: 7532132
-
Development of hematopoietic cells lacking transcription factor GATA-1.
Development. 1995 Jan;121(1):163-72
PMID: 7867497
-
Conditional site-specific recombination in mammalian cells using a ligand-dependent chimeric Cre recombinase.
Proc Natl Acad Sci U S A. 1995 Jul 18;92(15):6991-5
PMID: 7624356
-
Inducible gene targeting in mice.
Science. 1995 Sep 8;269(5229):1427-9
PMID: 7660125
-
Transgenic knockouts reveal a critical requirement for pancreatic beta cell glucokinase in maintaining glucose homeostasis.
Cell. 1995 Oct 6;83(1):69-78
PMID: 7553875
-
Targeted deletion of 5'HS2 of the murine beta-globin LCR reveals that it is not essential for proper regulation of the beta-globin locus.
Genes Dev. 1995 Sep 15;9(18):2203-13
PMID: 7557375
-
Rearrangement-enhancing element upstream of the mouse immunoglobulin kappa chain J cluster.
Science. 1996 Mar 8;271(5254):1416-20
PMID: 8596914
-
Know your neighbors: three phenotypes in null mutants of the myogenic bHLH gene MRF4.
Cell. 1996 Apr 5;85(1):1-4
PMID: 8620528
-
Analysis of mice containing a targeted deletion of beta-globin locus control region 5' hypersensitive site 3.
Mol Cell Biol. 1996 Jun;16(6):2906-12
PMID: 8649401
-
Ligand-activated site-specific recombination in mice.
Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):10887-90
PMID: 8855277
-
Arrested development of embryonic red cell precursors in mouse embryos lacking transcription factor GATA-1.
Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12355-8
PMID: 8901585
-
Subregion- and cell type-restricted gene knockout in mouse brain.
Cell. 1996 Dec 27;87(7):1317-26
PMID: 8980237
-
Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
Anal Biochem. 1987 Apr;162(1):156-9
PMID: 2440339