The making of an erythroid cell molecular control ofhematopoiesis

Biotherapy

Volumn 10, Issue 4, 1998, Pages 251-268

  Migliaccio, Anna Rita ^a   Migliaccio, Giovanni ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Erythropoiesis; Erythropoietin receptor; Signal transduction; Stem cell differentiation; Transcription factors

Indexed keywords

ERYTHROPOIETIN RECEPTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; TRANSCRIPTION FACTOR;

ARTICLE; BONE MARROW CELL; BURST FORMING UNIT; CELL DIFFERENTIATION; CELL LINE; ERYTHROID CELL; ERYTHROPOIESIS; GENE EXPRESSION; GENE MUTATION; HEMATOPOIESIS; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; BONE MARROW; BONE MARROW CELLS; ERYTHROID PROGENITOR CELLS; HEMATOPOIESIS; HUMANS;

EID: 0031946318     PISSN: 0921299X     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF02678546     Document Type: Article

References (224)

1. Stewart, A. (Ed.) Trends in Genetics. Genetic Nomenclature Guide. Cambridge, UK: Elsevier Science Publishers, 1995.
2. McCulloch EA. Stem cells in normal and leukemic hemopoiesis. Blood 1983; 62:1-13.
3. Ogawa M, Porter PN, Nakahata T. Renewal and commitment of differentiation of hemopoietic stem cells. Blood 1983; 61: 823-829.
4. Ogawa M. Differentiation and proliferation of hematopoietic stem cells. Blood 1993; 81:2844-2853.
5. Migliaccio G, Migliaccio AR, Adamson JW. The biology of hematopoietic growth factors: studies in vitro under serumdeprived conditions. Exp Hematol 1990; 18: 1049-1055.
6. Rüssel ES. Hereditary anemias of the mouse: A review for geneticists. Adv Gen 1979; 20: 357-459.
7. Besmer P. The kit ligand encoded at the marine Steel locus: a pleiotropic growth and differentiation factor. Curr Biol 1991 ; 3: 939-946.
8. Barker JE, Starr E. Characterization of spleen colonies derived from mice with mutations at the W locus. J Cell Physiol 1991; 149:45158.
9. Migliaccio AR, Migliaccio G, Mancini G, Ratajczak M, Gewirtz AM, Adamson JW. Induction of the murine "W phenotype" in long-term cultures of human cord blood cells by c-kit antisense oligomers. J Cell Physiol 1993; 157:158-163.
10. Adamson JW. The erythropoietin/hematocrit relationship in normal and polycythemic man: implications of marrow regulation. Blood 1968; 32: 597-609.
11. Wn H, Liu X, Jaenisch R, Lodish HE Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell 1995; 83: 59-67.
12. Lin C-S, Lim S-K, D'Agati V, Constantini F. Differential effects of an erythropoietin receptor gene disruption on primitive and definitive erythropoiesis. Genes Devel, 1996; 10: 154-160.
13. Wu H, Klingmüller U, Besmer P, Lodish HF. Interaction of the erythropoietin and stem-cell-factor receptors. Nature 1995; 377: 242-246.
14. Trentin JJ. Influence of hematopoietic organstroma (hematopoietic inductive microenvironments) on stroma cell differentiation. In: Regulation of Hematopoiesis ho Gordon A.S. (ed.) New York: Appleton-Century-Crofts, 1970.
15. Van Zant G, Goldwasser E. Competition between erythropoietin and colony-stimulating factor for target cells in mouse marrow. Blood 1979; 53: 946-965.
16. Johnson GR. Is erythropoiesis an obligatory step in the commitment of multipotential hematopoietic stem cells? In: Baum SJ, Ledney GD, Kahn A (eds) Experimental Hematology Today. New York: Springer-Verlag, 1981.
17. Till JE, McCulloch EA, Sizninovitch L. A stochastic model of stem cell proliferation, based on the growth of spleen colonyforming cells. Proc Natl Acad Sei USA 1964; 51: 29-34.
18. Nakahata T, Gross AJ, Ogawa M. A stochastic model of selfrenewal and commitment to differentiation of the primitive hematopoietic stem cells in culture. J Cell Physiol 1982; 113: 455-458.
19. Koury MJ, Bondurant MC. Erythropoietin retards DNA breakdown and prevents programmed death in erythroid progenitor cells. Science 1990; 248: 378-381.
20. Williams GT, Smith CA, Spooncer E, Dexter TM, Taylor DR. Haemopoietic colony-stimulating factors promote cell survival by suppressing apoptosis. Nature 1990; 343:76-79.
21. Lassar AB, Paterson BM, Weintraub H. Transfection of a DNA locus that mediates the conversion of 10 XX 1/2 fibroblasts to myoblasts. Cell 1986; 47: 649-656.
22. D' Andrea AD, Lodish HF, Wong GG. Expression cloning of the murine erythropoietin receptor. Cell 1989; 57: 277-285.
23. Liboi E, Carroll M, D'Andréa AD, Mathey-Prevot B. Erythropoietin receptor signals both proliferation and erythroidspecific differentiation. Proc Natl Acad Sei USA 1993; 90: 11351-11355.
24. Migliaccio GM, Migliaccio AR, Kleider BL, Rovera G, Adamson JW. Selection of lineage-restricted cell lines immortalized at different stages of hematopoietic differentiation from the murine cell line 32D. J Cell Biol 1989; 109: 833841.
25. Carrol M, Zhu Y, D'Andrea AD. Erythropoietin-mduced cellular differentiation requires prolongation of the Gl phase of the cell cycle. Proc Natl Acad Sei USA 1995; 92:2869-2873.
26. Shimada Y, Migliaccio G, Ralph H, Migliaccio AR. Erythropoietin-specific cell cycle progression in erythroid subclones of the IL-3-dependent cell line 32D. Blood 1993; 81:935-941.
27. Fairbairn LJ, Cowling GJ, Reipert BM, Dexter TM. Suppression of apoptosis allows differentiation and development of a multipotent hemopoietic cell line in the absence of added growth factors. Cell 1993; 74: 823-832.
28. Nishijima I, Nakahata T, Hirabayashi Y, et al. A human GMCSF receptor expressed in transgenic mice stimulates proliferation and differentiation of hemopoietic progenitors to all lineages in response to human GM-CSF. Mol Cell Biol 1995; 6: 497-508.
29. Jones SS, D'Andréa AD, Haines LL, Wong GG. Human erythropoietin receptor: cloning, expression, and biologic characterization. Blood 1990; 76: 31-35.
30. D'Andréa AD, Zon LI. Erythropoietin receptor: Subunit structure and activation. J Clin Invest 1990; 86: 681-687.
31. Youssoufian H, Longmore G, Neumann D, Yoshimura A, Lodish HF. Structure function, and activation of the erythropoietin receptor. Blood 1993; 81: 2223-2226.
32. Bazan JF. Structural design and molecular evolution of a cytokine receptor superfamily. Proc Natl Acad Sei USA 1990; 87: 6934-6938.
33. Yoshimura A, Zimmers T, Neumann D, Longmore G, Yoshimura Y, Lodish HF. Mutations in the Trp-Ser-X-TrpSer motif of the erythropoietin receptor abolish processing, ligand binding, and activation of the receptor. J Biol Chem 1992; 267: 11619-11625.
34. Sawada K, Krantz SB, Sawyer ST, Civin CI. Quantitation of specific binding of erythropoietin to human erythroid colonyforming cells. J Cell Physiol 1988; 137: 337-345.
35. Landschulz KT, Noyes AN, Rogers O, Boyer SH. Erythropoietin receptors on murine erythroid colony-forming units: natural history. Blood 1989; 73: 1476-1486.
36. Broudy VC, Lin N, Brice M, Nakamoto B, Papayannopoulou T. Erythropoietin receptor characteristics on primary human erythroid ceUs. Blood 1991: 77: 2583-2590.
37. Ishibashi T, Koziol JA, Burstein SA. Human recombinant erythropoietin promotes differentiation of marine megakaryocytes in vitro. J Clin Invest 1987; 79: 286-289.
38. Barren C, Migliaccio AR, Migliaccio G, Jiang Y, Adamson JW, Ottolenghi S. Alternatively spliced mRNAs encoding soluble isoforms of the erythropoietin receptor in murine cell lines and bone marrow. Gene 1994; 147: 263-268.
39. Miura O, D'Andréa A, Rabat D, Ihle JN. Induction of tyrosine phosphorylation by the erythropoietin receptor correlates with mitogenesis. Mol Cell Biol 1991; 11: 4895-4899.
40. Gobert S, Porteu F, Fallu S, et al. Tyrosine phosphorylation of the erythropoietin receptor: Role for differentiation and mitogenic signal transduction. Blood 1995; 86: 598-606.
41. Komatsu N, Adamson JW, Yamamoto K, et al. Erythropoietin rapidly induces tyrosine phosphorylation in the human erythropoietin-dependent cell line, UT-7. Blood 1992; 80: 53-59.
42. Torti M, Marti KB, Altschuler D, Yamamoto K, Lapetina EG. Erythropoietin induces p21ras activation and p!2OGAP tyrosine phosphorylation in human erythroleukemia cells. J Biol Chem 1992; 267: 8293-8298.
43. Satoh T, Nakafuku M, Miyajima A, Kaziro Y. Involvement of ras p21 protein in signal-transduction pathways from interleukin 2, interleukin 3, and granulocyte/macrophage colonystimulating factor, but not from interleukin 4. Proc Natl Acad Sei USA 1991; 88: 3314-3318.
44. Miller BA, Scaduto RC, Tillotson DL, Botti JJ, Cheung JY. Erythropoietin stimulates a rise in intracellular free calcium concentration in single human erythroid precursors. J Clin Invest 1988; 82: 309-315.
45. Miller BA, Cheung JY, Tillotson DL, Hope SM, Scaduto RC. Erythropoietin stimulates a rise in intracellular free calcium concentration in single BFU-E derived erythroblasts at specific stages of differentiation. Blood 1989; 73: 1188-1194.
46. Mayeux P, Dusanter-Fourt I, Muller O, et al. Erythropoietin induces the association of phosphatidylinositol 3'-kinase with a tyrosine-phosphorylated protein complex containing the erythropoietin receptor. Eur J Biochem 1993; 216: 821828.
47. Klingmüller U, Lorenz U, Cantley LC, Neel BG, Lodish HF. Specific recruitment of SH-PTP1 to the erythropoietin receptor causes inactivation of JAK2 and termination of proliferative signals. Cell 1995; 80: 729-738.
48. Tauchi T, Feng GS, Shen R, et al. Involvement of SH2containing phosphotyrosine phosphatase Syp in erythropoietin receptor signal transduction pathways. J Biol Chem 1995; 270: 5631-5635.
49. Ihle, J.N. Cytokine receptor signalling. Nature 1995; 377: 591-594.
50. Silvennoinen O, Witthuhn BA, Quelle FW, Cleveland JL, Yi T, Ihle JN. Structure of the murine Jak2 protein-tyrosine kinase and its role in interleukin 3 signal transduction. Proc Natl Acad Sei USA 1993; 90: 8429-8433.
51. Fu XY. A transcription factor with SH2 and SH3 domains is directly activated by an Interferon -induced cytoplasmic protein tyrosine kinase(s). Cell 1990: 70: 323-335.
52. Schindler C, Shuai K, Prezioso VR, Darnell JE. Interferondependent tyrosine phosphorylation of a latent cytoplasmic transcription factor. Science 1992; 257: 809-813.
53. Witthuhn BA, Quelle FW, Silvennoinen O, et al. JAK2 associates with the erythropoietin receptor and is tyrosine phos-
54. phorylated and activated following stimulation with erythropoietin. Cell 1993; 74: 227-236.
55. Miura O, Nakamura N, Quelle FW, Witthuhn BA, Me JN, Aoki N. Erythropoietin induces association of the JAK2 protein tyrosine kinase with the erythropoietin receptor in vivo. Blood 1994; 84: 1501-1507.
56. Barber DL, D'Andréa AD. Erythropoietin and Interleukin-2 activate distinct JAK kinase family members. Mol Cell Biol 1994; 14: 6506-6514.
57. Zhuang H, Patel SV, He T-C, Sonsteby SK, Niu Z, Wojchowski DM. Inhibition of erythropoietin-induced mitogenesis by a kinase-deflcient form of Jak2. J Biol Chem 1994; 269: 21411-21414.
58. Tanner JW, Chen W, Young RL, Longmore GD, Shaw AS. The conserved box 1 motif of cytokine receptors is required for association with JAK kinases. J Biol Chem 1995; 270: 6523-6530.
59. Schindler C, Darnell JE. Transcriptional responses to polypetide ligands: The Jak Stat pathways. Annu Rev Biochem 1995; 64: 621-651.
60. Koch CA, Anderson D, Moran MF, Ellis C, Pawson T. SHZ and SH3 domains: Elements that control interactions of cytoplasmic signaling proteins. Science 1991; 252: 668-674.
61. Erpel T, Courtneidge SA. Src family protein tyrosine kinases and cellular signal transduction pathways. Curr Op Cell Biol 1995; 7: 176-182.
62. Rothman P, Kreider B, Azam M, et al. Cytokines and growth factors signal through tyrosine phosphorylation of a family of related transcription factors. Immunity 1994; 1:457-468.
63. Gouilleux F, Pallard C, Dusanter-Fourt I, et al. Prolactin, growth hormone, erythropoietin and granulocytemacrophage colony stimulating factor induce MGF-Stat5 DNA binding activity. EMBO J.1995; 14: 2005-2013.
64. Wakao H, Harada N, Kitamura T, Mui ALF, Miyajirna A. Interleukin 2 and erythropoietin activate STAT5/MGF via distinct pathways. EMBO J. 1995: 14: 2527-2535.
65. Pallard C, Gouilleux F, Charon M, Groner B, Gisselbrecht S, Fourt-Dusanter I. Interleukin-3, erythropoietin and prolactin activate a STAT5-like factor in lymphoid cells. J. Biol. Chem. 1995; 270:15942-15945.
66. Machide M, Mano H, Todokoro K. Interleukin 3 and erythropoietin induce association of Vav with Tec kinase through Tec homology domain. Oncogene 1995; 11: 619-625.
67. He T-C, Jiang N, Zhuang H, Wojchowski DM. Erythropoietininduced recruitment of She via a receptor phosphotyrosineindependent, Jak2-associated pathway. J Biol Chem 1995; 270:11055-11061.
68. Damen JE, Liu L, Cutler RL, Krystal G. Erythropoietin stimulates the tyrosine phosphorylation of She and its association with Grb2 and a 145-Kd tyrosine phosphorylated protein. Blood 1993; 82: 2296-2303.
69. Ren HY, Komatsu N, Shimizu R, Okada K, Miura Y. Erythropoietin induces tyrosine phosphorylation and activation of phospholipase C-Y1 in human erythropoietin-dependent cell line. J Biol Chem 1994; 269: 19633-19638.
70. Linnekin D, Evans GA, D Andrea A, Farrar WL. Association of the erythropoietin receptor with protein tyrosine kinase activity. Proc Nad Acad Sei USA 1992; 89: 6237-6241.
71. Bittorf J, Jaster R, Brock J. Rapid activation of the MAP kinase pathway in hematopoietic cells by erythropoietin, granulocyte-macrophage colony-stimulating factor and interleukin-3. Cell Sig 1994; 6: 305-311.
72. Patel HR, Sytkowski AJ. Erythropoietin activation of API (Fos/Jun). Exp Hematol 1995; 23: 619-625.
73. Gulbins E, Coggeshall KM, Baier G, Katzav S, Burn P, Altman A. Tyrosine kinase-stimulated guanine nucleotide exchange activity of Vav in T cell activation. Science 1993; 260: 822-825.
74. Miura O, Miura Y, Nakamura N, et al. Induction of tyrosine phosphorylation of Vav and expression of Pim-1 correlates with Jak2-mediated growth signaling from the erythropoietin receptor. Blood 1994; 84: 4135-4141.
75. Tarakhovsky A, Turner M, Schaal S, et al. Defective antigen receptor-mediated proliferation of B and T cells in the absence of vav. Nature 1995; 374: 467-470.
76. Zhang R, Alt FW, Davidson L, Orkin SH, Swat W. Defective signalling through the T- and B-cell antigen receptors in lymphoid cell lacking the vav proto-oncogene. Nature 1995; 374:470-473.
77. Mason-Garcia M, Harlan RE, Mallia C, et al. Interleukin-3 or erythropoietin induced nuclear localization of protein kinase C beta isoforms in hematopoietic target cells. Cell Prolif 1995 ; 28: 145-155.
78. Spangler R, Bailey SC, Sytkowski AJ. Erythropoietin increases c-myc mRNA by a protein kinase C-dependent pathway. J Biol Chem 1991; 266: 681-684.
79. Spangler R, Sytkowski AJ. c-myc is an erythropoietin early response gene in normal erythroid cells : evidence for a protein kinase C-mediated signal. Blood 1992; 79: 52-57.
80. Saris CJ, Domen J, Berns A. The pirn-1 oncogene encodes two related protein-serine/threonine kinases by alternative initiation at AUG and CUG. EMBO J 1991; 10:655-664.
81. Domen J, van der Lugt NMT, Laird PW, et al. Impaired IL-3 response in Pim-1 -deficient bone marrow-derived mast cells. Blood 1993; 82: 1445-1452.
82. te Riele H, Maandag ER, Clarke A, Hooper M, Berns A. Consecutive inactivation of both alleles of the pirn-1 protooncogene by homologous recombination in embryonic stem cells. Nature 1990; 348: 649-651.
83. van der Lugt NMT, Domen J, Verhoeven E, et al. Proviral tagging in Eju-myc transgenic mice lacking the Pim-1 protooncogene leads to compensatory activation of Pim-2. EMBO J 1995; 14:2536-2544.
84. Shen S-H, Bastien L, Posner BI, Chrétien P. A proteintyrosine phosphatase with sequence similarity to the SH2 domain of the protein-tyrosine kinases. Nature 1991; 352: 736-739.
85. Feng G-S, Hui C-C, Pawson T. SH2-containing phosphotyrosine phosphatase as a target of protein-tyrosine kinases. Science 1993; 259: 1607-1611.
86. Yi T, Cleveland JL, Ihle JN. Protein tyrosine phosphatase containing SH2 domains: Characterization, preferential expression in hematopoietic cells, and localization to human chromosome 12pl2-pl3. Mol Cell Biol 1992; 12: 836-846.
87. Tauchi T, Feng G-S, Marshall MS, et al. The ubiquitously expressed Syp phosphatase interacts with c-kit and Grb2 in hematopoietic cells. J Biol Chem 1994; 269: 25206-25211.
88. Vogel W, Lammers R, Huang J, Ulrich A. Activation of a phosphotyrosine phosphatase by tyrosine phosphorylation. Science 1993; 259: 1611-1614.
89. Busfield SJ, Klinken SP. Erythropoietin-induced stimulation of differentiation and proliferation in J2E cells is not mimicked by chemical induction. Blood 1992; 80: 412-419.
90. Taxman DJ, Wojchowski DM. Erythropoietin-induced transcription at the murine Bma;'-globm promoter. J Biol Chem 1995; 270: 6619-6627.
91. Lumelsky NL, Forget BG. Negative regulation of globin gene expression during megakaryocytic differentiation of a human erythroleukemic cell line. Mol Cell Biol 1991; 11: 35283536.
92. Migliaccio AR, Jiang Y, Migliaccio G, et al. Transcriptional and posttranscriptional regulation of the expression of the erythropoietin receptor gene in human erythropoietin-responsive cell line. Blood 1993; 82: 3760-3769.
93. Stamatoyannopoulos JA, Goodwin A, Joyce T, Lowrey CH. NF-E2 and GATA binding motifs are required for the formation of DNase I hypersensitive site 4 of the human /3-globin locus control region. EMBO J 1995; 14: 106-116.
94. Collis P, Antoniou M, Grosveld F. Definition of the minimal requirements within the human /3-globin gene and the dominant control region for high level expression. EMBO J 1990; 9: 223-240.
95. Walters M, Martin DIK. Functional erythroid promoters created by interaction of the transcription factor GATA-1 with CACCC and AP-l/NFE-2 elements. Proc Natl Acad Sei USA 1992; 89: 10444-10448.
96. Tsai SF, Martin DIK, Zon LI, D Andrea AD, Won GG, Orkin SH. Clonin of cDNA for the major DNA-binding protein of the erythroid lineage through expression in mammalian cells. Nature 1989; 339: 446-451.
97. Evans T, Felsenfeld G. The erythroid-specific transcription factor Eryf 1 : A new finger protein. Cell 1989: 58: 877-885.
98. Zon LI, Tsai SF, Burgess S, Matsudaira P, Bruns GAP, Orkin SH. The major human erythroid DNA-binding protein (GF1): Primary sequence and localization of the gene to the X chromosome. Proc Natl Acad Sei USA 1990; 87: 668-672.
99. Orkin SH. GATA-binding transcription factors in hematopoietic cells. Blood 1992; 80: 575-581.
100. Fong TC, Emerson BM. The erythroid-specific protein Gatal mediates distal enhancer activity through a specialized globin TATA box. Gene Devel 1992; 6: 521-532.
101. Kim CG, Swendeman SL, Barnhart KM, Sheffery M. Promoter elements and erythroid cell nuclear factors that regulate a-globin gene transcription in vitro. Mol Cell Biol 1990; 10: 5958-5966.
102. Zon LI, Youssoufian H, Mather C, Lodish HF, Orkin SH. Activation of the erythropoietin receptor promoter by transcription factor Gatal. Proc Natl Acad Sei USA 1991; 88: 10638-10641.
103. Hannon R, Evans T, Felsenfeld G, Gould H. Structure and promoter activity of the gene for the erythroid transcription factor Gatal. Proc Natl Acad Sei USA 1991 ; 88: 3004-3008.
104. Tsai, S-F, Stauss 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; 5: 919-931
105. Crotta S, Nicolis S, Ronchi A, et al. Progressive inactivation of the expression of an erythroid transcriptional factor in GMand G-CSF-dependent myeloid cell lines. Nucleic Acids Res 1990; 18:6863-6869.
106. Migliaccio, AR, Migliaccio G, Ashihara E, Moroni E, Giglioni B, Ottolenghi S. Erythroid-specific activation of the distal (testis) promoter of GATAI during differentiation of purified normal murine hamatopoietic stem cells. Acta Haematol, 1996; 95: 229-235.
107. Sposi NM, Zon LI, Carè A, et al. Cell cycle-dependent initiation and lineage-dependent abrogation of GATA-1 expression in pure differentiating hematopoietic progenitors. Proc Natl Acad Sei USA 1992; 89: 6353-6357.
108. 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 Sei USA 1991; 88: 10642-10646.
109. Romeo PH, Prandini MH, Joulin V, et al. Megakaryocytic and erythrocytic lineages share specific transcription factors. Nature 1990; 344: 447-449.
110. Martin DIK, Zon LI, Mutter G, Orkin SH. Expression of an erythroid transcription factor in megakaryocytic and mast cell lineages. Nature 1990; 344:444-447.
111. Kulessa H, Promptem J, Graf T. G ATA-1 reprograms avian myelomonocytic cell lines into eosinophils, thromboblasts, erythroblasts. Genes Dev 1995; 9: 1250-1262.
112. Farina SF, Girard LJ, Vanin EF, Nienhuis AW, Bodine DM. Dysregulated expression of GATA-1 following retrovirusmediated gene transfer into murine hematopoietic stem cells increases erythropoiesis. Blood 1995; 86:4124-4133.
113. Ashihara E, Vannucchi AM, Migliaccio G et al. Growth factor receptor expression during in vitro differentiation of partially purified populations containing murine stem cells. J. Cell Physiol. 1997; 171: 343-356.
114. Moroni E, Cairns L, Ottolenghi S, et al. Expression in hematopoietic cells of GATA-1 transcripts from the alternative "testis" promoter during development and cell differentiation. Biochem. Biophys. Res. Comm. 1997; 231: 299-304.
115. Ito E, Toki T, Ishihara H, et al. Erythroid transcription factor GATA-1 is abundantly transcribed in mouse testis. Nature 1993; 362:466-468.
116. Yomogida K, Ohtani H, Harigae H, et al. Developmental stage- and spermatogenic cycle-specific expression of transcription factor GATA -1 in mouse Sertoli cells. Development 1994; 120: 1759-1766.
117. Zon LI, Gurish MF, Stevens RL, et al. GATA-binding transcription factors in mast cells regulate the promoter of the mast cell carboxypeptidase A gene. J Biol Chem 1991; 266: 22948-22953.
118. Dorfman DM, Wilson DB, Bruns GAP, Orkin SH. Human transcription factor GATA-2: Evidence for regulation of preproendothelin-1 gene expression in edothelial cells. J Biol Chem 1992; 267: 1279-1285.
119. Lemarchandel V, Ghysdael J, Mignotte V, Rahuel C, Romeo PH. GATA and Ets cis-acting sequences mediate megakaryocyte-speciflc expression. Mol Cell Biol 1993; 13: 668-676.
120. Merika M, Orkin SH. DNA-binding specificity of GATA family transcription factors. Mol Cell Biol 1993; 13: 3999-4010.
121. Ko LJ, Engel JD. DNA-binding specificities of the GATA transcription factor family. Mol Cell Biol 1993; 13: 40114022.
122. 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; 8: 11841197.
123. Pevny L, Simon MC, Robertson E, et al. Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor Gatal. Nature 1991; 349: 257-260.
124. Blobel GA, Simon MC, Orkin SH. Rescue of GATA1-deficient embryonic stem cells by heterologous GATAbinding proteins. Mol Cell Biol 1995; 15: 626-633.
125. Labbaye C, Valtieri M, Barberi T, et al. Differential expression and functional role of GATA-2, NF-E2, and GATA-1 in normal adult hematopoiesis. J Clin Invest 1995; 95: 23462358
126. Leonard M, Brice M, Engel JD, Papayannopoulou T. Dynamics of GATA transcription factor expression during erythroid differentiation. Blood 1993; 82: 1071-1079.
127. Zon LI, Yarnaguchi Y, Yee K, et al. Expression of mRNA for the GATA-binding proteins in human eosinophils and basophils: Potential role in gene transcription. Blood 1993: 81:3234-3241.
128. Tsai FY, Keller G, Kuo FC, et al. An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature 1994; 371: 221-226.
129. Andrews NC, Erdjument-Bromage H, Davidson MB, Tempst P, Orkin SH. Erythroid transcription factor NF-E2 is a haematopoietic-specific basic-leucine zipper protein. Nature 1993; 362: 722-728.
130. Ney PA, Andrews NC, Jane SM, et al. Purification of the human NF-E2 complex: cDNA cloning of the hematopoietic cell-specific subunit and evidence for an associated partner. Mol Cell Biol 1993; 13: 5604-5612.
131. Landschulz WH, Johnson PF, McKnight SL. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science, 1988; 240: 1759-1764.
132. Andrews NC, Kotkow KJ, Ney PA, Erdjument-Bromage H, Tempst P, Orkin SH. The ubiquitous subunit of erythroid transcription factor NF-E2 is a small basic-leucine zipper protein related to the v-maf oncogene. Proc Natl Acad Sei USA 1993; 90: 11488-11492.
133. Igarashi K, Kataoka K, Itoh K, Hayashi N, Nishizawa M, Yamamoto M. Regulation of transcription by dimerization of erythroid factor NF-E2 p45 with small Maf proteins. Nature 1994; 367: 568-572.
134. Kataoka K, Nishizawa M, Kawai S. Structure-function analysis of the maf oncogene product, a member of the b-Zip protein family. J Virol 1993; 67: 2133-2141.
135. Orlic D, Anderson S, Biesecker LG, Sorrentino BP, Bodine DM. Pluripotent hematopoietic stem cells contain high levels of mRNA for c-kit, GATA-2, p45 NF-E2, and c-myb and low levels or no mRNA for c-fms and the receptors for granulocyte colony-stimulating factor and interleukins 5 and 7. Proc Natl Acad Sei USA 1995; 92: 4601-4605.
136. Ney PA, Sorrentino BP, Lowrey CH, Nienhuis AW. Inducibility of the HSII enhancer depends on binding of an erythroid specific nuclear protein. Nucleic Acid Res 1990; 18: 60116017.
137. Talbot D, Philipsen S, Fräser P, Grosveld F. Detailed analysis of the site 3 region of the human /J-globin dominant control region. EMBO J 1990; 9: 2169-2178.
138. Pondel MD, George M, Proudfoot NJ. The LCR-like aglobin positive regulatory element functions as an enhancer in transiently transfected cells during erythroid differentiation. Nucleic Acid Res 1992; 20: 237-243.
139. Jarman AP, Wood WG, Sharpe JA, Gourdon G, Ayyub H, Higgs DR. Characterization of the major regulatory element upstream of the human a-globin gene cluster. Mol Cell Biol 1991; 11:46791689.
140. Ney PA, Sorrentino BP, McDonagh KT, Nienhuis AW. Tandem AP-1 binding sites within the human /3-globin dominant control region function as an inducible enhancer in erythroid cells. Genes Dev 1990; 4: 993-1006.
141. Talbot D, Grosveld F. The 5'SH2 of the globin locus control region enhances transcription through the interaction of a multimeric complex binding at two functionally distinct NFE2 binding sites. EMBO J, 1991; 10: 1391-1398.
142. Sorrentino B, Ney P, Bodine D, Nienhius AW. A 46 base pair enhancer sequence within the locus activating region is required for induced expression of the gamma-globin gene during erythroid differentiation. Nucleic Acid Res 1990; 18: 2721-2731.
143. Mignotte V, Eleouet JF, Raich N, Romeo P-H. Cis and transacting elements involved in the regulation of the erythroid promoter of the human porphobilinogen deaminase gene. Proc Nad Acad Sei USA 1989; 86:6548-6552.
144. Taketani S, Inazawa J, Nakahashi Y, Abe T, Tokunaga R. Structure of the human ferrochelatase gene. Exon/intron gene organization and location of the gene to chromosome 18. Euro J Biochem 1992; 205: 217-222.
145. Cox TC, Bawden MJ, Martin A, May BK. Human erythroid 5-aminolevulinate synthase: promoter analysis and identification of an iron-responsive element in the mRNA. EMBO J 1991; 10: 1891-1902.
146. Ben-David Y, Bani MR, Chabot B, De Koven A, Bernstein A. Retroviral insertion downstream of the heterogeneous nuclear ribonucleoprotein Al gene in erythroleukemia cells: evidence that A1 is not essential for cell growth. Mol Cell Biol 1992; 12: 4449-4455.
147. Lu S-J, Rowan S, Bani MR, Ben-David Y. Retroviral integration within the Fli-2 locus results in inactivation of the erythroid transcription factor NF-E2 in Friend erythroleukemias: Evidence that NF-E2 is essential for globin expression. Proc Natl Acad Sei USA 1994; 91: 8398-8402.
148. Shivdasani RA, Rosenblatt MF, Zncker-Franklin D, et al. Transcription factor NF-E2 is required for platelet formation independent of the action of thrombopoietin/MGDF in megakaryocyte development. Cell 1995; 81: 695-704.
149. Miller IJ, Bieker JJ. A novel erythroid cell-specific murine transcription factor that binds to the CACCC element and is related to the Krüppel family of nuclear proteins. Mol Cell Biol 1993; 13: 2776-2786.
150. Feng WC, Southwood CM, Bieker JJ. Analyses of thalassemia mutant DNA interactions with erythroid Kruppellike factor (EKLF), and erythroid cell-specific transcription factor. J Biol Chem 1994; 269: 1493-1500.
151. Crossley M, Tsang AP, Bieker JJ, Orkin SH. Regulation of the erythroid Kruppel-like factor (EKLF) gene promoter by the erythroid transcription factor Gâtai. J Biol Chem 1994; 269: 15440-15444.
152. Tsai S-F, 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; 5: 919-931.
153. Begley CG, Aplan PD, Denning SM, Haynes BF, Waldmann TA, Kirsch IR. The gene SCL is expressed during early hernatopoiesis and encodes a differentiation-related DNA binding motif. Proc Natl Acad Sei USA 1989; 86: 10128-10132.
154. Begley CG, Visvader J, Green AR, et al. Molecular cloning and chromosomal localization of the murine homolog of the human helix-loop-helix gene SCL. Proc Natl Acad Sei USA 1991; 88: 869-873.
155. Mouthon M-A, Berbard O, Mitjavila M-T, Romeo H-P, Vainchenker W, Mathieu-Mahul D. Expression of tal-1 and GATA-binding proteins during human hematopoiesis. Blood 1993; 81: 647-655.
156. Visvader J, Begley CO, Adams JM. Differential expression of the Lyl, SCL and E2A helix-loop-helix genes within the hemopoietic system. Oncogene 1991; 6: 187-194.
157. Green AR, Salvaris E, Begley CG. Erythroid expression of the helix-loop-helix gene. Oncogene 1991; 6:475-479.
158. Green AR, Lints T, Visvader J, Harvey R, Begley CG. SCL is coexpressed with Gatal in hemopoietic cells but is also expressed in developing brain. Oncogene 1992; 7: 653-660.
159. Xia Y, Brown L, Yang CY-C, et al. TAL2, a helix-loop-helix gene activated by the (7;9)(q34;q32) translocation in human T-cell leukemia. Proc Natl Acad Sei USA 1991; 88: 1141611420.
160. Mellentin JD, Smith SD, Clearly ML. lyl-\, a novel gene altered by chromosomal translocation in T cell' leukemia, codes for a protein with a helix-loop-helix DNA binding motif. Cell 1989; 58: 77-83.
161. Quertermous EE, Hidai H, Blanar MA, Quertermous T. Cloning and characterization of a basic helix-loop-helix protein expressed in early mesoderm and the developing somites. Proc Natl Acad Sei USA 1994; 91: 7066-7070.
162. Hsu H-L, Cheng J-T, Chen Q, Baer R. Enhancer-binding activity of the tal-l oncoprotein in association with the E47/E12 helix-loop-helix proteins. Mol Cell Biol 1991; 11: 3037-3042.
163. Green AR, Rockman S, DeLuca E, Begley CG. Induced myeloid differentiation of K562 with downregulation of erythroid and megakaryocytic transcription factors. A novel experimental model for haemopoietic lineage restriction. Exp Hematol 1993; 21: 525-531.
164. Apian PD, Nakahara K, Orkin SH, Kirsch IR. The SCL gene product: a positive regulator of erythroid differentiation. EMBO J 1992; 11: 4073-4081.
165. Green AR, DeLuca E, Begley CG. Antisense SCL suppresses self-renewal and enhances spontaneous erythroid differentiation of the human leukaemic cell line K562. EMBO J 1991; 10:4153158.
166. Visvader JE, Elefanty AG, Strasser A, Adams JM. Gatal but not SCL induces megakaryocitic differentiation in an early myeloid line. EMBO J. 1992; 11:4557-4564.
167. Apian PD, Begley CG, Bertness V, et al. The SCL gene is formed from transcriptionally complex locus. Mol Cell Biol 1990; 10: 6426-6435.
168. Voronova AF, Lee F. The E2A and tal-l helix-loop-helix proteins associate in vivo and are modulated by Id proteins during interleukin 6-induced myeloid differentiation. Proc Natl Acad Sei USA 1994; 91: 5952-5956.
169. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 1990; 61: 49-59.
170. Sun X-H, Copeland NG, Jenkins NA, Baltimore D. Id proteins Id I and Id2 selectively inhibit DNA binding by one clas of helix-loop-helix proteins. Mol Cell Biol 1991; 11: 56035611.
171. Shoji W, Yamamoto T, Obinata M. The helix-loop-helix protein Id inhibits differentiation of murine erythroleukemia cells. J Biol Chem 1994; 269: 5078-5084.
172. Condorelli G, Vitelli L, Valtieri M, et al. Coordinate expression and developmental role of Id2 protein and TAL1/EZA heterodimer in erythroid progenitor differentiation. Blood 1995; 86: 164-175.
173. Prasad KSS, Jordan JE, Koury MK, Bondurant MC, Brandt SJ. Erythropoietin stimulates transcription of the TALI/SCL gene and phosphorylation of its protein products. J Biol Chem 1995; 270: 11603-11611.
174. Shivdasani RA, Nayer EL, Orkin SL. Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal1/SCL. Nature 1995; 373: 432-434.
175. Robb L, Lyons I, Li R, et al. Absence of yolk sac hematopoiesis from mice with a targeted disruption of the scl gene. Proc Natl Acad Sei USA 1995 92: 7075-7079.
176. Scott EW, Simon MC, Anastasi J, Singh H. Requirement of transcription factor PU.l in the development of multiple hematopoietic lineages. Science 1994; 265: 1573-1577.
177. Boehm T, Foroni L, Kaneko Y, Perutz MF, Rabbitts TH. The rhombotin family of cystein-rich LIM domain oncogenes : distinct members are involved in T-cell translocations to human chromosomes llplS and Ilpl3. Proc Natl Acad Sei USA 1991; 88: 4367-4371.
178. Royer-Pokora B, Loos U, Ludwig W-D. TTG-2, a new gene encoding a cystein-rich protein with the LIM motif, is overexpressed in acute T-cell leukaemia with the t(ll;14)(pl3;ql). Oncogene 1991; 6: 1887-1893.
179. Foroni L, Boehm T, White L, et al. The rhombotin gene family encode related LIM-domain proteins whose differing expression suggests multiple roles in mouse development. J Mol Biol 1992; 226: 747-761.
180. Boehm T, Forono II., Kennedy M, Rabbitts TH. The rhombotin gene belongs to a class of transcriptional regulators with a potential novel protein dimerization motif. Oncogene 1990; 5: 1103-1105.
181. Sanchez-Garcia I, Rabbitts TH. LIM domain proteins in leukemia and development. Sem Cane Biol 1993; 4: 349358.
182. Warren AJ, Colledge WH, Carlton MBL, Evans MJ, Smith AJH, Rabbitts TH. The oncogenic cystein-rich LIM domain protein Rbtn2 is essential for erythroid development. Cell 1994; 78:45-57.
183. Valge-Archer VE, Osada H, Warren AJ, et al. The LIM protein Rbtn2 and the basic helix-loop-helix protein TALI are present in a complex in erythroid cells. Proc Natl Acad Sei USA 1994; 91: 8617-8621.
184. Wadman I, Li J, Bash RO, et al. Specific in vivo association between the bHLH and LIM proteins implicated in human T cell leukemia. EMBO 1994; 13: 4831839.
185. Sheiness D, Gardinier M. Expression of a proto-oncogene (proto-myb) in hematopoietic tissues of mice. Mol Cell Biol 1984; 4: 1206-1212.
186. Gonda TJ, Metcalf D. Expression of myb, myc and fas protooncogenes during the differentiation of a murine myeloid leukaemia. Nature 1984; 310: 249-251.
187. Ramsay RG, Ikeda K, Rifkind RA, Marks PA. Changes in gene expression associated with induced differentiation of erythroleukemia: protooncogenes, globin genes, and cell division. Proc Natl Acad Sei USA 1986; 83: 6849-6853.
188. Henkemeyer MJ, Bennett RL, Gertler FB, Hoffman FM. DNA sequence, structure, and tyrosine kinase activity of the Drosophila melanogaster Abelson proto-oncogene homolog. Mol Cell Biol 1988; 8: 843-853.
189. Tokodoro K, Watson RJ, Higo H, et al. Down-regulation of c-myb gene expression is a prerequisite for erythropoietininduced erythroid differentiation. Proc Natl Acad Sei USA 1988; 85: 8900-8904.
190. Rosson D, O'Brien TG. Constitutive c-myb expression in K562 cells inhibits induced erythroid differentiation but not tetradecanoyl phorbol acetate-induced megakaryocytic differentiation. Mol Cell Biol 1995; 15:772-779.
191. Gewirtz AM, Calabretta B. A c-myb antisense oligodeoxynucleotide inhibits normal human hematopoieis in vitro. Science 1988; 242: 1003-1006.
192. Mucenski ML, McLain K, Bier AB, et al. A functional c-myb gene is required for normal mutine fetal hematopoiesis. Cell 1991; 65: 677-689.
193. Klemsz MJ, McKercher SR, Celada A, Van Beveren C, Maki RA. The macrophage and B cell-specific transcription factor PU.l is related to the ets oncogene. Cell 1990; 61: 113-124.
194. Moreau-Gachelin F, Tavitian A, Tambourin P. Spi-1 is a putative oncogene in virally induced murine erythroleukaemias. Nature 1988; 33: 277-280.
195. Paul R, Schuetze S, Kozak SL, Kozak CA, Rabat D. The Sfpi1 proviral integration site of Friend erythroleukemia encodes the ets-related transcription factor PU.l. J Virol. 1991; 65: 464-67.
196. Chen HM, Zhang P, Voso MT, et al. Neutrophils and monocytes express high levels of PU.l (Spi-1) but not Spi-B. Blood 1995; 85: 2918-2928.
197. Galson DL, Hensold JO, Bishop TR, et al. Mouse /3-globin DNA-binding protein BI is identical to aproto-oncogene, the transcription factor Spi-I/PU.l, and is restricted in expression to hematopoietic cells and the testis. Mol Cell Biol 1993; 13: 2929-2941.
198. Hromas R, Orazi A, Neiman RS, et al. Hematopoietic lineageand stage-restricted expression of the ETS oncogene family member PU.l. Blood 1993; 82: 2998-3004.
199. Pahl HL, Scheibe RJ, Zhang DE, et al. The proto-oncogene PU. 1 regulates expression of the myeloid-specific CD1 Ibpromoter. J Biol Chem 1993; 268: 5014-5020.
200. Zhang DE, Hetherington CJ, Chen HM, Tenen DG. The macrophage transcription factor PU.l directs tissue-specific expression of the macrophage colony-stimulating factor receptor. Mol Cell Biol 1994; 14: 373-381.
201. Schuetze S, Stenberg PE, Kabat D. The Ets-related transcription factor PU.l immortalizes erythroblasts. Mol Cell Biol 1993; 13: 5670-5678.
202. Voso MT, Burn TC, Wulf G, Lim B, Leone G, Tenen DG. Inhibition of hematopoiesis by competitive binding of transcription factor PU.l. Proc Natl Acad Sei USA 1994; 91: 7932-7936.
203. Lawrence HJ, Largman C. Homeobox genes in normal hematopoiesis and leukemia. Blood 1992; 80: 2445-2453.
204. Kongsuwan K, Webb E, Housiaux P, Adams JM. Expression of multiple homeobox genes within diverse mammalian haemopoietic lineages. EMBO J 1988; 7: 2131-2138.
205. Lowney P, Corral J, Detmer K, et al. A human Hox I homeobox gene exhibits myeloid-specific expression of alternative transcripts in human hematopoietic cells. Nucleic Acid Res 1991; 19:3443-3449.
206. Magli MC, Barba P, Celetti A, De Vita G, Cillo C, Boncinelli E. Coordinate regulation of HOX genes in human hematopoietic cells. Proc Natl Acad Sei USA 1991; 88: 6348-352.
207. Shen WF, Detmer K, Mathews CHE, et al. Modulation of Homeobox gene expression alters the phenotype of human hematopoietic cell lines. EMBO J. 1992; 11: 983-989.
208. Metcalf D. Hematopoietic regulators: redundancy or subtlety. Blood 1993; 82: 3515-3523.
209. Migliaccio G, Migliaccio AR, Valinsky J, Langley K, Zsebo K, Visser JWM. Stem cell factor (SCF) induces proliferation and differentiation of highly enriched murine hematopoietic cells. Proc Natl Acad Sei USA 1991; 88: 7420-7424.
210. Hirayama F, Shih JP, Awgulewitsch A, Warr GW, Clark SC, Ogawa M. Clonal proliferation of murine lymphohemopoietic progenitors in culture. Proc Natl Acad Sei USA 1992; 89: 5907-5911.
211. Brandt J, Briddell RA, Srour EF, Leemhuis TB, Hoffman R. Role of c-kit ligand in the expansion of human hematopoietic progenitor lls. Blood 1992; 79: 634-641.
212. Migliaccio G, Migliaccio AR, Druzin ML, Giardina PJV, Zsebo KM, Adamson JW. Long-term generation of colonyforming cells in liquid culture of CD34+ cord blood cells in the presence of recombinant human stem cell factor. Blood 1992; 79:2620-2627.
213. Sonoda Y, Yang YC, Wong GG, dark SC, Ogawa M. Analysis in serum-free culture of the targets of recombinant human hemopoietic growth factors: interleukin 3 and granulocyte/macrophage-colony stimulating factor are specific for early developmental stages. Proc Natl Acad Sei USA 1988; 85: 4360-4364.
214. Migliaccio G, Migliaccio AR, Adamson JW. In vitro differentiation of human granulocyte/macrophage and erythroid progenitors: comparative analysis of the influence of recombinant human erythropoietin, G-CSF, GM-CSF, and IL-3 in serum-supplemented and serum-deprived cultures. Blood 1988; 72: 248-256.
215. Dainiak N, Kreczko S. Interactions of insulin, insulin-like growth factor II, and platelet-derived growth factor in erythropoietic culture. J Clin Invest 1985; 76: 1237-1242.
216. Akahane K, Tojo A, Urabe A, Takaku F. Pure erythropoietic colony and burst formations in serum-free culture and their enhancement by insulin-like growth factor. Exp Hematol 1987; 15:797-802.
217. Merchav S, Tatarsky I, Hochberg Z. Enhancement of human granulopoiesis in vitro by biosynthetic insulin-like growth factor 1/somatomedin C and human growth hormone. J Clin Invest 1988; 81:791-797.
218. Migliaccio AR, Bruno M, Migliaccio G. Evidence for direct action of human biosynthetic (recombinant) GM-CSF on erythroid progenitors in serum-free culture. Blood 1987; 70: 1867-1871.
219. Iscove NN, Guilbert LJK, Weyman C. Complete replacement of serum in primary cultures of erythropoietin-dependent red cell precursors (CFU-E) by albumin, transferrin, iron, unsaturated fatty acid, lecithin and cholesterol. Exp Cell Res 1980; 126:121-126.
220. Migliaccio AR, Migliaccio G. Human embryonic hemopoiesis: control mechanisms underlying progenitor differentiation in vitro. Dev Biol 1988; 125: 127-134.
221. Migliaccio AR, Vannucchi AM, Migliaccio G. Molecular control of erythroid differentiation (review article) Int. J. Hemat. 1996; 64: 1-29.
222. Kelly LL, Green WF, Hicks GG, Bondurant MC, Koury MJ, Ruley HE. Apoptosis in erythroid progenitors deprived of erythropoietin occurs during the Gl and S phases of the cell cycle without growth arrest or stabilization of wild-type p53. Mol Cell Biol 1994; 14: 4183-4192.
223. Vannucchi A, Alespeiti G, Migliaccio G, Migliaccio AR. Differential expression of the GATAI family and growth factor receptors in purified stem cells (HSC) and multilineage progenitor cells. Blood 1995; 86: 303a.
224. Jiang, Y, Migliaccio G, Migliaccio AR, Adamson JW. Regulation of the expression of the Id gene during erythroid differentiation of 32D cells. Blood 1993; 82: lOOa.