The hypomorphic Gata1low mutation alters the proliferation/differentiation potential of the common megakaryocytic-erythroid progenitor

Blood

Volumn 109, Issue 4, 2007, Pages 1460-1471

  Ghinassi, Barbara ^a,b   Sanchez, Massimo ^a   Martelli, Fabrizio ^a   Amabile, Giovanni ^a   Vannucchi, Alessandro Maria ^c   Migliaccio, Giovanni ^a   Orkin, Stuart H ^d   Migliaccio, Anna Rita ^a,e  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b UNIVERSITY OF CHIETI   (Italy)

^c UNIVERSITY OF FLORENCE   (Italy)

^d HARVARD MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR GATA 1; GATA1 PROTEIN, HUMAN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL ISOLATION; CELL LINE; CELL PROLIFERATION; CLONING; CONTROLLED STUDY; ERYTHROBLAST; ERYTHROID CELL; ERYTHROID PRECURSOR CELL; GENE MUTATION; MAST CELL; MEGAKARYOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SPLEEN CELL; STEM CELL; ANIMAL; CYTOLOGY; GENETICS; MUTATION;

ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; ERYTHROID PROGENITOR CELLS; GATA1 TRANSCRIPTION FACTOR; MAST CELLS; MEGAKARYOCYTES; MICE; MUTATION;

EID: 33846917131     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-07-030726     Document Type: Article

References (62)

1. Orkin SH. Transcription factors that regulate lineage decisions. In: Stamatoyannopoulous G, ed. The Molecular Basis of Blood Diseases. Philadelphia, PA: Saunders. 2000:80-120.
2. 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;339:446-451.
3. Martin DI, Zon LI, Mutter G, Orkin SH. Expression of an erythroid transcription factor in megakaryocytic and mast cell lineages. Nature. 1990;344:444-447.
4. Romeo PH, Prandini MH, Joulin V, et al. Megakaryocytic and erythrocytic lineages share specific transcription factors. Nature. 1990;344:447-449.
5. Yu C, Cantor AB, Yang H, et al. Targeted deletion of a high-affinity GATA-binding site in the GATA-1 promoter leads to selective loss of the eosinophil lineage in vivo. J Exp Med. 2002;195:1387-1395.
6. Migliaccio AR, Rana RA, Sanchez M, et al. GATA-1 as a regulator of mast cell differentiation revealed by the phenotype of the GATA-1low mouse mutant. J Exp Med. 2003;197:281-296.
7. Nichols KE, Crispino JD, Poncz M, et al. Familial dyserythropoietic anaemia and thrombocytopenia due to an inherited mutation in GATA1. Nat Genet. 2000;24:266-270.
8. Freson K, Devriendt K, Matthijs G, et al. Platelet characteristics in patients with X-linked macrothrombocytopenia because of a novel GATA1 mutation. Blood. 2001;98:85-92.
9. Mehaffey MG, Newton AL, Gandhi MJ, Crossley M, Drachman JG. X-linked thrombocytopenia caused by a novel mutation of GATA-1. Blood. 2001;98:2681-2688.
10. Yu C, Niakan KK, Matsushita M, Stamatoyannopoulos G, Orkin SH, Raskind WH. X-linked thrombocytopenia with thalassemia from a mutation in the amino finger of GATA-1 affecting DNA binding rather than FOG-1 interaction. Blood. 2002;100:2040-2045.
11. Hollanda LM, Lima CSP, Cunha AF, et al. An inherited mutation leading to production of only the short isoform of GATA-1 is associated with impaired erythropoiesis. Nat Genet. 2006;38:807-812.
12. Mundschau G, Crispino JD. GATA1s goes germline. Nat Genet. 2006;38:741-742.
13. Wechsler J, Greene M, McDevitt MA, et al. Acquired mutations in GATA1 in the megakaryoblastic leukemia of Down syndrome. Nat Genet. 2002;32:148-152.
14. Xu G, Nagano M, Kanezaki R, et al. Frequent mutations in the GATA-1 gene in the transient myeloproliferative disorder of Down syndrome. Blood. 2003;102:2960-2968.
15. Ahmed M, Sternberg A, Hall G, et al. Natural history of GATA1 mutations in Down syndrome. Blood. 2004;103:2480-2489.
16. Harigae H, Xu G, Sugawara T, Ishikawa I, Toki T, Ito E. The GATA1 mutation in an adult patient with acute megakaryoblastic leukemia not accompanying Down syndrome. Blood. 2004;103:3242-3243.
17. Suda T, Suda J, Ogawa M. Single-cell origin of mouse hemopoietic colonies expressing multiple lineages in variable combinations. Proc Natl Acad Sci U S A. 1983;80:6689-6693.
18. Akashi K, Traver D, Miyamoto T, Weissman IL. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature. 2000;404:193-197.
19. Gurish MF, Austen KF. The diverse roles of mast cells. J Exp Med. 2001;194:F1-5.
20. Galli SJ, Nakae S, Tsai M. Mast cells in the development of adaptive immune responses. Nat Immunol. 2005;6:135-142.
21. Chen CC, Grimbaldeston MA, Tsai M, Weissman IL, Galli SJ. Identification of mast cell progenitors in adult mice. Proc Natl Acad Sci U S A. 2005;102:11408-11413.
22. Rodewald DS, Dessing M, Dvorak AM, Galli SJ. Identification of a committed precursor for the mast cell lineage. Science. 1996;271:818-822.
23. Reynolds DS, Stevens RL, Lane WS, Carr MH, Austen KF, Serafin WE. Different mouse mast cell populations express various combinations of at least six distinct mast cell serine proteases. Proc Natl Acad Sci U S A. 1990;87:3230-3234.
24. Stevens RL, Friend DS, McNeil HP, Schiller V, Ghildyal N, Austen KF. Strain-specific and tissue-specific expression of mouse mast cell secretory granule proteases. Proc Natl Acad Sci U S A. 1994;91:128-132.
25. Nocka K, Tan JC, Chiu E, et al. Molecular bases of dominant negative and loss of function mutations at the murine c-kit/white spotting locus: W37, Wv, W41 and W. EMBO J. 1990;9:1805-1813.
26. McDevitt MA, Shivdasani RA, Fujiwara Y, Yang H, Orkin SH. A "knockdown" mutation created by cis-element gene targeting reveals the dependence of erythroid cell maturation on the level of transcription factor GATA-1. Proc Natl Acad Sci U S A. 1997;94:6781-6785.
27. Li Q, Clegg C, Peterson K, Shaw S, Raich N, Stamatoyannopoulos G. Binary transgenic mouse model for studying the trans control of globin gene switching: evidence that GATA-1 is an in vivo repressor of human epsilon gene expression. Proc Natl Acad Sci U S A. 1997;94:2444-2448.
28. Li Q, Stamatoyannopoulos JA. Position independence and proper developmental control of gamma-globin gene expression require both a 5′ locus control region and a downstream sequence element. Mol Cell Biol. 1994;14:6087-6096.
29. Vannucchi AM, Bianchi L, Cellai C, et al. Development of myelofibrosis in mice genetically impaired for GATA-1 expression (GATA-1(low) mice). Blood. 2002;100:1123-1132.
30. Sanchez M, Weissman IL, Pallavicini M, et al. Differential amplification of murine bipotent megakaryocytic/erythroid progenitor and precursor cells during recovery from acute and chronic erythroid stress. Stem Cells. 2006;24:337-348.
31. Krause DS, Theise ND, Collector MI, et al. Multiorgan, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell. 2001;105:369-377.
32. Nocka K, Buck J, Levi E, Besmer P. Candidate ligand for the c-kit transmembrane kinase receptor: KL, a fibroblast derived growth factor stimulates mast cells and erythroid progenitors. EMBO J. 1990;9:3287-3294.
33. + cord blood cells stimulated with stem cell factor and interleukin-3. Blood. 1994;84:3667-3674.
34. Nakorn TN, Miyamoto T, Weissman IL. Characterization of mouse clonogenic megakaryocyte progenitors. Proc Natl Acad Sci U S A. 2003;100:205-210.
35. Greenberger JS, Sakakeeny MA, Humphries RK, Eaves CJ, Eckner RJ. Demonstration of permanent factor-dependent multipotential (erythroid/ neutrophil/basophil) hematopoietic progenitor cell lines. Proc Natl Acad Sci U S A. 1983;80:2931-2935.
36. Migliaccio G, Migliaccio AR, Kreider 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;109:833-841.
37. Sambrook J, Fritsch EF, ManiatisT. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1989.
38. McNeil HP, Reynolds DS, Schiller V, et al. Isolation, characterization, and transcription of the gene encoding mouse mast cell protease 7. Proc Natl Acad Sci U S A. 1992;89:11174-11178.
39. Reynolds DS, Stevens RL, Gurley DS, Lane WS, Austen KF, Serafin WE. Isolation and molecular cloning of mast cell carboxypeptidase A. A novel member of the carboxypeptidase gene family. J Biol Chem. 1989;264:20094-20099.
40. Lecine P, Shivdasani RA. Cellular and molecular biology of megakaryocyte differentiation in the absence of lineage-restricted transcription factors. Stem Cells. 1998;16(suppl 2):91-95.
41. Vannucchi AM, Linari S, Lin CS, Koury MJ, Bondurant MC, Migliaccio AR. Increased expression of the distal, but not of the proximal, Gata1 transcripts during differentiation of primary erythroid cells. J Cell Physiol. 1999;180:390-401.
42. Maeda K, Nishiyama C, Tokura T, et al. FOG-1 represses GATA-1-dependent FcepsilonRI beta-chain transcription: transcriptional mechanism of mast-cell-specific gene expression in mice. Blood. 2006;108:262-269.
43. + lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell. 2005;121:295-306.
44. Vannucchi AM, Paoletti F, Linari S, et al. Identification and characterization of a bipotent (erythroid and megakaryocytic) cell precursor from the spleen of phenylhydrazine-treated mice. Blood. 2000;95:2559-2568.
45. Kitajima K, Zheng J, Yen H, Sugiyama D, Nakano T. Multipotential differentiation ability of GATA-1-null erythroid-committed cells. Genes Dev. 2006;20:654-659.
46. McNagny K, Graf T. Making eosinophils through subtle shifts in transcription factor expression. J Exp Med. 2002;195:F43-47.
47. Cantor AB, Orkin SH. Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene. 2002;21:3368-3376.
48. Hu M, Krause D, Greaves M, et al. Multilineage gene expression precedes commitment in the hemopoietic system. Genes Dev. 1997;11:774-785.
49. Farina SF, Girard LJ, Vanin EF, Nienhuis AW, Bodine DM. Dysregulated expression of GATA-1 following retrovirus-mediated gene transfer into murine hematopoietic stem cells increases erythropoiesis. Blood. 1995;86:4124-4133.
50. Iwasaki H, Mizuno S, Wells RA, Cantor AB, Watanabe S, Akashi K. GATA-1 converts lymphoid and myelomonocytic progenitors into the megakaryocyte/ erythrocyte lineages. Immunity. 2003;19:451-462.
51. Galloway JL, Wingert RA, Thisse C, Thisse B, Zon LI. Loss of gata1 but not gata2 converts erythropoiesis to myelopoiesis in zebrafish embryos. Dev Cell. 2005;8:109-116.
52. Kulessa H, Frampton J, Graf T. GATA-1 reprograms avian myelomonocytic cell lines into eosinophils, thromboblasts, and erythroblasts. Genes Dev. 1995;9:1250-1262.
53. Pevny L, Simon MC, Robertson E, et al. Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1. Nature. 1991;349:257-260.
54. Pevny L, Lin CS, D'Agati V, Simon MC, Orkin SH, Costantini F. Development of hematopoietic cells lacking transcription factor GATA-1. Development. 1995;121:163-172.
55. 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;92:9623-9627.
56. Migliaccio AR, Rana RA, Vannucchi AM, Manzoli FA. Role of GATA-1 in normal and neoplastic hemopoiesis. Ann N Y Acad Sci. 2005;1044:142-158.
57. Li Z, Godinho FJ, Klusmann JH, Garriga-Canut M, Yu C, Orkin SH. Developmental stage-selective effect of somatically mutated leukemogenic transcription factor GATA1. Nat Genet. 2005;37:613-619.
58. Shimizu R, Kuroha T, Ohneda O, et al. Leukemogenesis caused by incapacitated GATA-1 function. Mol Cell Biol. 2004;24:10814-10825.
59. Stachura DL, Chou ST, Weiss MJ. Early block to erythromegakaryocytic development conferred by loss of transcription factor GATA-1. Blood. 2006;107:87-97.
60. Takahashi S, Onodera K, Motohashi H, et al. Arrest in primitive erythroid cell development caused by promoter-specific disruption of the GATA-1 gene. J Biol Chem. 1997;272:12611-12615.
61. low mutation in mice of different genetic backgrounds. Blood. 2005;106:4102-4113.
62. Hoffmann R, Ravandi-Kashani F. Idiopathic myelofibrosis. In: Hoffman R, Benz E Jr, Shattil S, et al, eds. Hematology: Basic Principles and Practise. 4th ed. New York, NY: Churchill Livingstone. In press.