GATA-1 but not SCL induces megakaryocytic differentiation in an early myeloid line. (original) (raw)

EMBO J. 1992 Dec; 11(12): 4557–4564.

Walter and Eliza Hall Institute of Medical Research, Royal Melbourne Hospital, Victoria, Australia.

Abstract

GATA-1, a transcription factor of the 'zinc-finger' family, is required for the development of mature erythroid cells and is also highly expressed in the megakaryocytic and mast cell lineages. The helix-loop-helix gene SCL (or TAL) is expressed in the same three hematopoietic lineages as GATA-1. To explore the role of GATA-1 and SCL in hematopoietic differentiation, we introduced a new expression vector bearing each gene into the early myeloid cell line 416B, which could originally differentiate in vivo along the megakaryocytic and granulocytic lineages. Enforced expression of SCL at high levels did not provoke differentiation, but GATA-1 induced the appearance of megakaryocytes as assessed by morphology, the presence of acetylcholinesterase and a polyploid DNA content. Although GATA-1 is thought to stimulate its own transcription in erythrocytes, expression of the endogenous gene was not increased in the megakaryocytic lines; hence GATA-1 may not be autoregulatory in this lineage. Megakaryocytic differentiation was accompanied by a marked decrease in the myeloid surface marker Mac-1. The absence of mast cell or erythroid differentiation suggests that GATA-1 may not be sufficient to provoke maturation along these lineages or that these pathways are impeded in 416B cells. These results demonstrate that a member of the GATA gene family can act as an important regulator of megakaryocytic differentiation.

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Begley CG, Aplan PD, Denning SM, Haynes BF, Waldmann TA, Kirsch IR. The gene SCL is expressed during early hematopoiesis and encodes a differentiation-related DNA-binding motif. Proc Natl Acad Sci U S A. 1989 Dec;86(24):10128–10132. [PMC free article] [PubMed] [Google Scholar]
Begley CG, Visvader J, Green AR, Aplan PD, Metcalf D, Kirsch IR, Gough NM. Molecular cloning and chromosomal localization of the murine homolog of the human helix-loop-helix gene SCL. Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):869–873. [PMC free article] [PubMed] [Google Scholar]
Bernard O, Guglielmi P, Jonveaux P, Cherif D, Gisselbrecht S, Mauchauffe M, Berger R, Larsen CJ, Mathieu-Mahul D. Two distinct mechanisms for the SCL gene activation in the t(1;14) translocation of T-cell leukemias. Genes Chromosomes Cancer. 1990 Jan;1(3):194–208. [PubMed] [Google Scholar]
Bowtell DD, Johnson GR, Kelso A, Cory S. Expression of genes transferred to haemopoietic stem cells by recombinant retroviruses. Mol Biol Med. 1987 Aug;4(4):229–250. [PubMed] [Google Scholar]
Chen Q, Cheng JT, Tasi LH, Schneider N, Buchanan G, Carroll A, Crist W, Ozanne B, Siciliano MJ, Baer R. The tal gene undergoes chromosome translocation in T cell leukemia and potentially encodes a helix-loop-helix protein. EMBO J. 1990 Feb;9(2):415–424. [PMC free article] [PubMed] [Google Scholar]
Cooper MC, Levy J, Cantor LN, Marks PA, Rifkind RA. The effect of erythropoietin on colonial growth of erythroid precursor cells in vitro. Proc Natl Acad Sci U S A. 1974 May;71(5):1677–1680. [PMC free article] [PubMed] [Google Scholar]
Cory S, Maekawa T, McNeall J, Metcalf D. Murine erythroid cell lines derived with c-myc retroviruses respond to leukemia-inhibitory factor, erythropoietin, and interleukin 3. Cell Growth Differ. 1991 Mar;2(3):165–172. [PubMed] [Google Scholar]
Crotta S, Nicolis S, Ronchi A, Ottolenghi S, Ruzzi L, Shimada Y, Migliaccio AR, Migliaccio G. Progressive inactivation of the expression of an erythroid transcriptional factor in GM- and G-CSF-dependent myeloid cell lines. Nucleic Acids Res. 1990 Dec 11;18(23):6863–6869. [PMC free article] [PubMed] [Google Scholar]
D'Andrea AD, Lodish HF, Wong GG. Expression cloning of the murine erythropoietin receptor. Cell. 1989 Apr 21;57(2):277–285. [PubMed] [Google Scholar]
Dexter TM, Allen TD, Scott D, Teich NM. Isolation and characterisation of a bipotential haematopoietic cell line. Nature. 1979 Feb 8;277(5696):471–474. [PubMed] [Google Scholar]
Elefanty AG, Cory S. bcr-abl-Induced cell lines can switch from mast cell to erythroid or myeloid differentiation in vitro. Blood. 1992 Mar 1;79(5):1271–1281. [PubMed] [Google Scholar]
Elefanty AG, Hariharan IK, Cory S. bcr-abl, the hallmark of chronic myeloid leukaemia in man, induces multiple haemopoietic neoplasms in mice. EMBO J. 1990 Apr;9(4):1069–1078. [PMC free article] [PubMed] [Google Scholar]
Fraser JK, Lin FK, Berridge MV. Expression of high affinity receptors for erythropoietin on human bone marrow cells and on the human erythroleukemic cell line, HEL. Exp Hematol. 1988 Nov;16(10):836–842. [PubMed] [Google Scholar]
Green AR, Salvaris E, Begley CG. Erythroid expression of the 'helix-loop-helix' gene, SCL. Oncogene. 1991 Mar;6(3):475–479. [PubMed] [Google Scholar]
Green AR, Lints T, Visvader J, Harvey R, Begley CG. SCL is coexpressed with GATA-1 in hemopoietic cells but is also expressed in developing brain. Oncogene. 1992 Apr;7(4):653–660. [PubMed] [Google Scholar]
Greenberg SM, Rosenthal DS, Greeley TA, Tantravahi R, Handin RI. Characterization of a new megakaryocytic cell line: the Dami cell. Blood. 1988 Dec;72(6):1968–1977. [PubMed] [Google Scholar]
Hannon R, Evans T, Felsenfeld G, Gould H. Structure and promoter activity of the gene for the erythroid transcription factor GATA-1. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3004–3008. [PMC free article] [PubMed] [Google Scholar]
Hofer E, Darnell JE., Jr The primary transcription unit of the mouse beta-major globin gene. Cell. 1981 Feb;23(2):585–593. [PubMed] [Google Scholar]
Ikuta K, Kina T, MacNeil I, Uchida N, Peault B, Chien YH, Weissman IL. A developmental switch in thymic lymphocyte maturation potential occurs at the level of hematopoietic stem cells. Cell. 1990 Sep 7;62(5):863–874. [PubMed] [Google Scholar]
Ishibashi T, Koziol JA, Burstein SA. Human recombinant erythropoietin promotes differentiation of murine megakaryocytes in vitro. J Clin Invest. 1987 Jan;79(1):286–289. [PMC free article] [PubMed] [Google Scholar]
Ishibashi T, Kimura H, Uchida T, Kariyone S, Friese P, Burstein SA. Human interleukin 6 is a direct promoter of maturation of megakaryocytes in vitro. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5953–5957. [PMC free article] [PubMed] [Google Scholar]
KARNOVSKY MJ, ROOTS L. A "DIRECT-COLORING" THIOCHOLINE METHOD FOR CHOLINESTERASES. J Histochem Cytochem. 1964 Mar;12:219–221. [PubMed] [Google Scholar]
Krishan A. Rapid flow cytofluorometric analysis of mammalian cell cycle by propidium iodide staining. J Cell Biol. 1975 Jul;66(1):188–193. [PMC free article] [PubMed] [Google Scholar]
Li L, Olson EN. Regulation of muscle cell growth and differentiation by the MyoD family of helix-loop-helix proteins. Adv Cancer Res. 1992;58:95–119. [PubMed] [Google Scholar]
McNiece IK, Langley KE, Zsebo KM. Recombinant human stem cell factor synergises with GM-CSF, G-CSF, IL-3 and epo to stimulate human progenitor cells of the myeloid and erythroid lineages. Exp Hematol. 1991 Mar;19(3):226–231. [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]
Metcalf D. The molecular control of cell division, differentiation commitment and maturation in haemopoietic cells. Nature. 1989 May 4;339(6219):27–30. [PubMed] [Google Scholar]
Mizushima S, Nagata S. pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res. 1990 Sep 11;18(17):5322–5322. [PMC free article] [PubMed] [Google Scholar]
Nicolis S, Bertini C, Ronchi A, Crotta S, Lanfranco L, Moroni E, Giglioni B, Ottolenghi S. An erythroid specific enhancer upstream to the gene encoding the cell-type specific transcription factor GATA-1. Nucleic Acids Res. 1991 Oct 11;19(19):5285–5291. [PMC free article] [PubMed] [Google Scholar]
Nishi N, Nakahata T, Koike K, Takagi M, Naganuma K, Akabane T. Induction of mixed erythroid-megakaryocyte colonies and bipotential blast cell colonies by recombinant human erythropoietin in serum-free culture. Blood. 1990 Oct 1;76(7):1330–1335. [PubMed] [Google Scholar]
Odell TT, Jr, Jackson CW, Friday TJ. Megakaryocytopoiesis in rats with special reference to polyploidy. Blood. 1970 Jun;35(6):775–782. [PubMed] [Google Scholar]
Ogura M, Morishima Y, Ohno R, Kato Y, Hirabayashi N, Nagura H, Saito H. Establishment of a novel human megakaryoblastic leukemia cell line, MEG-01, with positive Philadelphia chromosome. Blood. 1985 Dec;66(6):1384–1392. [PubMed] [Google Scholar]
Orkin SH. Globin gene regulation and switching: circa 1990. Cell. 1990 Nov 16;63(4):665–672. [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]
Poncz M, Surrey S, LaRocco P, Weiss MJ, Rappaport EF, Conway TM, Schwartz E. Cloning and characterization of platelet factor 4 cDNA derived from a human erythroleukemic cell line. Blood. 1987 Jan;69(1):219–223. [PubMed] [Google Scholar]
Rachinsky TL, Camp S, Li Y, Ekström TJ, Newton M, Taylor P. Molecular cloning of mouse acetylcholinesterase: tissue distribution of alternatively spliced mRNA species. Neuron. 1990 Sep;5(3):317–327. [PubMed] [Google Scholar]
Ravid K, Doi T, Beeler DL, Kuter DJ, Rosenberg RD. Transcriptional regulation of the rat platelet factor 4 gene: interaction between an enhancer/silencer domain and the GATA site. Mol Cell Biol. 1991 Dec;11(12):6116–6127. [PMC free article] [PubMed] [Google Scholar]
Romeo PH, Prandini MH, Joulin V, Mignotte V, Prenant M, Vainchenker W, Marguerie G, Uzan G. Megakaryocytic and erythrocytic lineages share specific transcription factors. Nature. 1990 Mar 29;344(6265):447–449. [PubMed] [Google Scholar]
Scolnick EM, Weeks MO, Shih TY, Ruscetti SK, Dexter TM. Markedly elevated levels of an endogenous sarc protein in a hemopoietic precursor cell line. Mol Cell Biol. 1981 Jan;1(1):66–74. [PMC free article] [PubMed] [Google Scholar]
Serfling E. Autoregulation--a common property of eukaryotic transcription factors? Trends Genet. 1989 May;5(5):131–133. [PubMed] [Google Scholar]
Springer T, Galfré G, Secher DS, Milstein C. Mac-1: a macrophage differentiation antigen identified by monoclonal antibody. Eur J Immunol. 1979 Apr;9(4):301–306. [PubMed] [Google Scholar]
Strasser A, Whittingham S, Vaux DL, Bath ML, Adams JM, Cory S, Harris AW. Enforced BCL2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8661–8665. [PMC free article] [PubMed] [Google Scholar]
Thomas KR, Capecchi MR. Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell. 1987 Nov 6;51(3):503–512. [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]
Tsai SF, Strauss E, Orkin SH. Functional analysis and in vivo footprinting implicate the erythroid transcription factor GATA-1 as a positive regulator of its own promoter. Genes Dev. 1991 Jun;5(6):919–931. [PubMed] [Google Scholar]
Tso JY, Sun XH, Kao TH, Reece KS, Wu R. Isolation and characterization of rat and human glyceraldehyde-3-phosphate dehydrogenase cDNAs: genomic complexity and molecular evolution of the gene. Nucleic Acids Res. 1985 Apr 11;13(7):2485–2502. [PMC free article] [PubMed] [Google Scholar]
Visvader J, Begley CG. Helix-loop-helix genes translocated in lymphoid leukemia. Trends Biochem Sci. 1991 Sep;16(9):330–333. [PubMed] [Google Scholar]
Visvader J, Begley CG, Adams JM. Differential expression of the LYL, SCL and E2A helix-loop-helix genes within the hemopoietic system. Oncogene. 1991 Feb;6(2):187–194. [PubMed] [Google Scholar]
Wendling F, Shreeve M, McLeod D, Axelrad A. A self-renewing, bipotential erythroid/mast cell progenitor in continuous cultures of normal murine bone marrow. J Cell Physiol. 1985 Oct;125(1):10–18. [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]

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