Erythroid-cell-specific properties of transcription factor GATA-1 revealed by phenotypic rescue of a gene-targeted cell line. (original) (raw)
- Journal List
- Mol Cell Biol
- v.17(3); 1997 Mar
- PMC231889
Mol Cell Biol. 1997 Mar; 17(3): 1642–1651.
Children's Hospital, Dana-Farber Cancer Institute, Department of Pediatrics, Harvard Medical School, Boston, Massachusetts 02115, USA.
Abstract
The zinc finger transcription factor GATA-1 is essential for erythropoiesis. In its absence, committed erythroid precursors arrest at the proerythroblast stage of development and undergo apoptosis. To study the function of GATA-1 in an erythroid cell environment, we generated an erythroid cell line from in vitro-differentiated GATA-1- murine embryonic stem (ES) cells. These cells, termed G1E for GATA-1- erythroid, proliferate as immature erythroblasts yet complete differentiation upon restoration of GATA-1 function. We used rescue of terminal erythroid maturation in G1E cells as a stringent cellular assay system in which to evaluate the functional relevance of domains of GATA-1 previously characterized in nonhematopoietic cells. At least two major differences were established between domains required in G1E cells and those required in nonhematopoietic cells. First, an obligatory transactivation domain defined in conventional nonhematopoietic cell transfection assays is dispensable for terminal erythroid maturation. Second, the amino (N) zinc finger, which is nonessential for binding to the vast majority of GATA DNA motifs, is strictly required for GATA-1-mediated erythroid differentiation. Our data lead us to propose a model in which a nuclear cofactor(s) interacting with the N-finger facilitates transcriptional action by GATA-1 in erythroid cells. More generally, our experimental approach highlights critical differences in the action of cell-specific transcription proteins in different cellular environments and the power of cell lines derived from genetically modified ES cells to elucidate gene function.
Full Text
The Full Text of this article is available as a PDF (888K).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Abel T, Michelson AM, Maniatis T. A Drosophila GATA family member that binds to Adh regulatory sequences is expressed in the developing fat body. Development. 1993 Nov;119(3):623–633. [PubMed] [Google Scholar]
- Blobel GA, Simon MC, Orkin SH. Rescue of GATA-1-deficient embryonic stem cells by heterologous GATA-binding proteins. Mol Cell Biol. 1995 Feb;15(2):626–633. [PMC free article] [PubMed] [Google Scholar]
- Burstein SA, Friese P, Downs T, Mei RL. Characteristics of a novel rat anti-mouse platelet monoclonal antibody: application to studies of megakaryocytes. Exp Hematol. 1992 Nov;20(10):1170–1177. [PubMed] [Google Scholar]
- Crossley M, Merika M, Orkin SH. Self-association of the erythroid transcription factor GATA-1 mediated by its zinc finger domains. Mol Cell Biol. 1995 May;15(5):2448–2456. [PMC free article] [PubMed] [Google Scholar]
- Cunningham TS, Cooper TG. Expression of the DAL80 gene, whose product is homologous to the GATA factors and is a negative regulator of multiple nitrogen catabolic genes in Saccharomyces cerevisiae, is sensitive to nitrogen catabolite repression. Mol Cell Biol. 1991 Dec;11(12):6205–6215. [PMC free article] [PubMed] [Google Scholar]
- Davis RL, Cheng PF, Lassar AB, Weintraub H. The MyoD DNA binding domain contains a recognition code for muscle-specific gene activation. Cell. 1990 Mar 9;60(5):733–746. [PubMed] [Google Scholar]
- Deng C, Zhang P, Harper JW, Elledge SJ, Leder P. Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell. 1995 Aug 25;82(4):675–684. [PubMed] [Google Scholar]
- Dranoff G, Jaffee E, Lazenby A, Golumbek P, Levitsky H, Brose K, Jackson V, Hamada H, Pardoll D, Mulligan RC. Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3539–3543. [PMC free article] [PubMed] [Google Scholar]
- Evans T, Felsenfeld G. The erythroid-specific transcription factor Eryf1: a new finger protein. Cell. 1989 Sep 8;58(5):877–885. [PubMed] [Google Scholar]
- Evans T, Felsenfeld G. trans-Activation of a globin promoter in nonerythroid cells. Mol Cell Biol. 1991 Feb;11(2):843–853. [PMC free article] [PubMed] [Google Scholar]
- Fong TC, Emerson BM. The erythroid-specific protein cGATA-1 mediates distal enhancer activity through a specialized beta-globin TATA box. Genes Dev. 1992 Apr;6(4):521–532. [PubMed] [Google Scholar]
- Fu YH, Marzluf GA. nit-2, the major nitrogen regulatory gene of Neurospora crassa, encodes a protein with a putative zinc finger DNA-binding domain. Mol Cell Biol. 1990 Mar;10(3):1056–1065. [PMC free article] [PubMed] [Google Scholar]
- Gstaiger M, Georgiev O, van Leeuwen H, van der Vliet P, Schaffner W. The B cell coactivator Bob1 shows DNA sequence-dependent complex formation with Oct-1/Oct-2 factors, leading to differential promoter activation. EMBO J. 1996 Jun 3;15(11):2781–2790. [PMC free article] [PubMed] [Google Scholar]
- Keller G, Kennedy M, Papayannopoulou T, Wiles MV. Hematopoietic commitment during embryonic stem cell differentiation in culture. Mol Cell Biol. 1993 Jan;13(1):473–486. [PMC free article] [PubMed] [Google Scholar]
- Ko LJ, Engel JD. DNA-binding specificities of the GATA transcription factor family. Mol Cell Biol. 1993 Jul;13(7):4011–4022. [PMC free article] [PubMed] [Google Scholar]
- König H, Pfisterer P, Corcoran LM, Wirth T. Identification of CD36 as the first gene dependent on the B-cell differentiation factor Oct-2. Genes Dev. 1995 Jul 1;9(13):1598–1607. [PubMed] [Google Scholar]
- Korsmeyer SJ. Bcl-2 initiates a new category of oncogenes: regulators of cell death. Blood. 1992 Aug 15;80(4):879–886. [PubMed] [Google Scholar]
- Kudla B, Caddick MX, Langdon T, Martinez-Rossi NM, Bennett CF, Sibley S, Davies RW, Arst HN., Jr The regulatory gene areA mediating nitrogen metabolite repression in Aspergillus nidulans. Mutations affecting specificity of gene activation alter a loop residue of a putative zinc finger. EMBO J. 1990 May;9(5):1355–1364. [PMC free article] [PubMed] [Google Scholar]
- Kulessa H, Frampton J, Graf T. GATA-1 reprograms avian myelomonocytic cell lines into eosinophils, thromboblasts, and erythroblasts. Genes Dev. 1995 May 15;9(10):1250–1262. [PubMed] [Google Scholar]
- Laverriere AC, MacNeill C, Mueller C, Poelmann RE, Burch JB, Evans T. GATA-4/5/6, a subfamily of three transcription factors transcribed in developing heart and gut. J Biol Chem. 1994 Sep 16;269(37):23177–23184. [PubMed] [Google Scholar]
- Leonard M, Brice M, Engel JD, Papayannopoulou T. Dynamics of GATA transcription factor expression during erythroid differentiation. Blood. 1993 Aug 15;82(4):1071–1079. [PubMed] [Google Scholar]
- Lowe SW, Ruley HE, Jacks T, Housman DE. p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell. 1993 Sep 24;74(6):957–967. [PubMed] [Google Scholar]
- Luo Y, Roeder RG. Cloning, functional characterization, and mechanism of action of the B-cell-specific transcriptional coactivator OCA-B. Mol Cell Biol. 1995 Aug;15(8):4115–4124. [PMC free article] [PubMed] [Google Scholar]
- Martin DI, Zon LI, Mutter G, Orkin SH. Expression of an erythroid transcription factor in megakaryocytic and mast cell lineages. Nature. 1990 Mar 29;344(6265):444–447. [PubMed] [Google Scholar]
- Martin DI, Orkin SH. Transcriptional activation and DNA binding by the erythroid factor GF-1/NF-E1/Eryf 1. Genes Dev. 1990 Nov;4(11):1886–1898. [PubMed] [Google Scholar]
- Merika M, Orkin SH. DNA-binding specificity of GATA family transcription factors. Mol Cell Biol. 1993 Jul;13(7):3999–4010. [PMC free article] [PubMed] [Google Scholar]
- Merika M, Orkin SH. Functional synergy and physical interactions of the erythroid transcription factor GATA-1 with the Krüppel family proteins Sp1 and EKLF. Mol Cell Biol. 1995 May;15(5):2437–2447. [PMC free article] [PubMed] [Google Scholar]
- Metz T, Harris AW, Adams JM. Absence of p53 allows direct immortalization of hematopoietic cells by the myc and raf oncogenes. Cell. 1995 Jul 14;82(1):29–36. [PubMed] [Google Scholar]
- Molkentin JD, Black BL, Martin JF, Olson EN. Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell. 1995 Dec 29;83(7):1125–1136. [PubMed] [Google Scholar]
- Orkin SH. GATA-binding transcription factors in hematopoietic cells. Blood. 1992 Aug 1;80(3):575–581. [PubMed] [Google Scholar]
- Osada H, Grutz G, Axelson H, Forster A, Rabbitts TH. Association of erythroid transcription factors: complexes involving the LIM protein RBTN2 and the zinc-finger protein GATA1. Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9585–9589. [PMC free article] [PubMed] [Google Scholar]
- Pear WS, Nolan GP, Scott ML, Baltimore D. Production of high-titer helper-free retroviruses by transient transfection. Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8392–8396. [PMC free article] [PubMed] [Google Scholar]
- Pevny L, Lin CS, D'Agati V, Simon MC, Orkin SH, Costantini F. Development of hematopoietic cells lacking transcription factor GATA-1. Development. 1995 Jan;121(1):163–172. [PubMed] [Google Scholar]
- Pevny L, Simon MC, Robertson E, Klein WH, Tsai SF, D'Agati V, Orkin SH, Costantini F. Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1. Nature. 1991 Jan 17;349(6306):257–260. [PubMed] [Google Scholar]
- Ryan TM, Behringer RR, Martin NC, Townes TM, Palmiter RD, Brinster RL. A single erythroid-specific DNase I super-hypersensitive site activates high levels of human beta-globin gene expression in transgenic mice. Genes Dev. 1989 Mar;3(3):314–323. [PubMed] [Google Scholar]
- Schubart DB, Sauter P, Massa S, Friedl EM, Schwarzenbach H, Matthias P. Gene structure and characterization of the murine homologue of the B cell-specific transcriptional coactivator OBF-1. Nucleic Acids Res. 1996 May 15;24(10):1913–1920. [PMC free article] [PubMed] [Google Scholar]
- Serrano M, Lee H, Chin L, Cordon-Cardo C, Beach D, DePinho RA. Role of the INK4a locus in tumor suppression and cell mortality. Cell. 1996 Apr 5;85(1):27–37. [PubMed] [Google Scholar]
- Shivdasani RA, Orkin SH. The transcriptional control of hematopoiesis. Blood. 1996 May 15;87(10):4025–4039. [PubMed] [Google Scholar]
- Simon MC, Pevny L, Wiles MV, Keller G, Costantini F, Orkin SH. Rescue of erythroid development in gene targeted GATA-1- mouse embryonic stem cells. Nat Genet. 1992 May;1(2):92–98. [PubMed] [Google Scholar]
- Souyri M, Vigon I, Penciolelli JF, Heard JM, Tambourin P, Wendling F. A putative truncated cytokine receptor gene transduced by the myeloproliferative leukemia virus immortalizes hematopoietic progenitors. Cell. 1990 Dec 21;63(6):1137–1147. [PubMed] [Google Scholar]
- Spieth J, Shim YH, Lea K, Conrad R, Blumenthal T. elt-1, an embryonically expressed Caenorhabditis elegans gene homologous to the GATA transcription factor family. Mol Cell Biol. 1991 Sep;11(9):4651–4659. [PMC free article] [PubMed] [Google Scholar]
- Strubin M, Newell JW, Matthias P. OBF-1, a novel B cell-specific coactivator that stimulates immunoglobulin promoter activity through association with octamer-binding proteins. Cell. 1995 Feb 10;80(3):497–506. [PubMed] [Google Scholar]
- Tapscott SJ, Davis RL, Thayer MJ, Cheng PF, Weintraub H, Lassar AB. MyoD1: a nuclear phosphoprotein requiring a Myc homology region to convert fibroblasts to myoblasts. Science. 1988 Oct 21;242(4877):405–411. [PubMed] [Google Scholar]
- Tournamille C, Colin Y, Cartron JP, Le Van Kim C. Disruption of a GATA motif in the Duffy gene promoter abolishes erythroid gene expression in Duffy-negative individuals. Nat Genet. 1995 Jun;10(2):224–228. [PubMed] [Google Scholar]
- Trainor CD, Omichinski JG, Vandergon TL, Gronenborn AM, Clore GM, Felsenfeld G. A palindromic regulatory site within vertebrate GATA-1 promoters requires both zinc fingers of the GATA-1 DNA-binding domain for high-affinity interaction. Mol Cell Biol. 1996 May;16(5):2238–2247. [PMC free article] [PubMed] [Google Scholar]
- Tsai SF, Martin DI, Zon LI, D'Andrea AD, Wong GG, Orkin SH. Cloning of cDNA for the major DNA-binding protein of the erythroid lineage through expression in mammalian cells. Nature. 1989 Jun 8;339(6224):446–451. [PubMed] [Google Scholar]
- Visvader J, Adams JM. Megakaryocytic differentiation induced in 416B myeloid cells by GATA-2 and GATA-3 transgenes or 5-azacytidine is tightly coupled to GATA-1 expression. Blood. 1993 Sep 1;82(5):1493–1501. [PubMed] [Google Scholar]
- Visvader JE, Elefanty AG, Strasser A, Adams JM. GATA-1 but not SCL induces megakaryocytic differentiation in an early myeloid line. EMBO J. 1992 Dec;11(12):4557–4564. [PMC free article] [PubMed] [Google Scholar]
- Visvader JE, Crossley M, Hill J, Orkin SH, Adams JM. The C-terminal zinc finger of GATA-1 or GATA-2 is sufficient to induce megakaryocytic differentiation of an early myeloid cell line. Mol Cell Biol. 1995 Feb;15(2):634–641. [PMC free article] [PubMed] [Google Scholar]
- Weiss MJ, Keller G, Orkin SH. Novel insights into erythroid development revealed through in vitro differentiation of GATA-1 embryonic stem cells. Genes Dev. 1994 May 15;8(10):1184–1197. [PubMed] [Google Scholar]
- Weiss MJ, Orkin SH. GATA transcription factors: key regulators of hematopoiesis. Exp Hematol. 1995 Feb;23(2):99–107. [PubMed] [Google Scholar]
- Weiss MJ, Orkin SH. In vitro differentiation of murine embryonic stem cells. New approaches to old problems. J Clin Invest. 1996 Feb 1;97(3):591–595. [PMC free article] [PubMed] [Google Scholar]
- Weiss MJ, Orkin SH. Transcription factor GATA-1 permits survival and maturation of erythroid precursors by preventing apoptosis. Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9623–9627. [PMC free article] [PubMed] [Google Scholar]
- Whyatt DJ, deBoer E, Grosveld F. The two zinc finger-like domains of GATA-1 have different DNA binding specificities. EMBO J. 1993 Dec 15;12(13):4993–5005. [PMC free article] [PubMed] [Google Scholar]
- Wickrema A, Koury ST, Dai CH, Krantz SB. Changes in cytoskeletal proteins and their mRNAs during maturation of human erythroid progenitor cells. J Cell Physiol. 1994 Sep;160(3):417–426. [PubMed] [Google Scholar]
- Yamamoto M, Ko LJ, Leonard MW, Beug H, Orkin SH, Engel JD. Activity and tissue-specific expression of the transcription factor NF-E1 multigene family. Genes Dev. 1990 Oct;4(10):1650–1662. [PubMed] [Google Scholar]
- Yang HY, Evans T. Distinct roles for the two cGATA-1 finger domains. Mol Cell Biol. 1992 Oct;12(10):4562–4570. [PMC free article] [PubMed] [Google Scholar]
- Yang HY, Evans T. Homotypic interactions of chicken GATA-1 can mediate transcriptional activation. Mol Cell Biol. 1995 Mar;15(3):1353–1363. [PMC free article] [PubMed] [Google Scholar]
- Zon LI, Mather C, Burgess S, Bolce ME, Harland RM, Orkin SH. Expression of GATA-binding proteins during embryonic development in Xenopus laevis. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10642–10646. [PMC free article] [PubMed] [Google Scholar]
Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis