Bcr-Abl is a "molecular switch" for the decision for growth and differentiation in hematopoietic stem cells

International Journal of Hematology

Volumn 76, Issue 1, 2002, Pages 35-43

  Era, Takumi ^a  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

Bcr Abl; Chronic myeloid leukemia; Hematopoietic stem cell; In vitro ES cell differentiation system; Tetracycline regulatory system

Indexed keywords

BCR ABL PROTEIN; TETRACYCLINE;

CELL DIFFERENTIATION; CELL GROWTH; CHRONIC MYELOID LEUKEMIA; EMBRYONIC STEM CELL; HEMATOPOIETIC STEM CELL; IN VITRO STUDY; MYELOID PROGENITOR CELL; REVIEW; ANIMAL; BIOSYNTHESIS; CELL DIVISION; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM;

ANIMALS; CELL DIFFERENTIATION; CELL DIVISION; FUSION PROTEINS, BCR-ABL; GENE EXPRESSION REGULATION; HEMATOPOIETIC STEM CELLS; HUMANS; LEUKEMIA, MYELOID, CHRONIC; TETRACYCLINE;

EID: 0036632548     PISSN: 09255710     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF02982716     Document Type: Review

References (93)

1. Rowley JD. A new consistent chromosomal abnormality in chronic myelogenous leukemia identified by quinacrine fluorescence and Giemsa staining. Nature. 1973;243:290-293.
2. Groffen J, Stephenson JR, Heisterkamp N, de Klein A, Bartram CR, Grosveld G. Philadelphia chromosomal breakpoints are clustered within a limited region, bcr, on chromosome 22. Cell. 1984;36:93-99.
3. Konopka JB, Watanabe SM, Witte ON. An alteration of the human c-abl protein in K562 leukemia cells unmasks associated tyrosine kinase activity. Cell. 1984;37:1035-1042.
4. Shtivelman E, Lifshitz B, Gale RP, Roe BA, Canaani E. Fused transcript of abl and bcr genes in chronic myelogenous leukaemia. Nature. 1985;315:550-554.
5. Sawyers CL. Chronic myeloid leukemia. N Engl J Med. 1999;340:1330-1340.
6. Bernstein R. Cytogenetics of chronic myelogenous leukemia. Semin Hematol. 1988;25:20-34.
7. Faderl S, Talpaz M, Estrov Z, O'Brien S, Kurzrock R, Kantarjian HM. The biology of chronic myeloid leukemia. N Engl J Med. 1999;341:164-172.
8. McLaughlin J, Chianese E, Witte ON. In vitro transformation of immature hematopoietic cells by the P210 BCR/ABL oncogene product of the Philadelphia chromosome. Proc Natl Acad Sci U S A. 1987;84:6558-6562.
9. Lugo TG, Pendergast A, Muller AJ, Witte ON. Tyrosine kinase activity and transformation potency of bcr-abl oncogene products. Science. 1990;247:1079-1082.
10. McWhirter JR, Wang JYJ. An actin-binding function contributes to transformation by the bcr-abl oncoprotein of Philadelphia chromosome-positive human leukemias. EMBO J. 1993;12:1533-1546.
11. Wang JY. Abl tyrosine kinase in signal transduction and cell-cycle regulation. Curr Opin Genet Dev. 1993;3:35-43.
12. Pendergast AM, Quilliam LA, Cripe LD, et al. BCR-ABL-induced oncogenesis is mediated by direct interaction with the SH2 domain of the GRB-2 adaptor protein. Cell. 1993;75:175-185.
13. Heaney C, Kolibaba K, Bhat A, et al. Direct binding of CRKL to BCR-ABL is not required for BCR-ABL transformation. Blood. 1997;89:297-306.
14. Salgia R, Brunkhorst B, Pisick E, et al. Increased tyrosine phosphorylation of focal adhesion proteins in myeloid cell lines expressing p210BCR/ABL. Oncogene. 1995;11:1149-1155.
15. Tauchi T, Boswell HS, Leibowitz D, Broxmeyer HE. Coupling between p210bcr-abl and She and Grb2 adaptor proteins in hematopoietic cells permits growth factor receptor-independent link to Ras activation pathway. J Exp Med. 1994;179:167-175.
16. Yamanashi Y, Baltimore D. Identification of the Abl- and rasGAP-associated 62 kDa protein as a docking protein, Dok. Cell. 1997;88:205-211.
17. dok: a constitutively tyrosine-phosphorylated, GAP-associated protein in chronic myelogenous leukemia progenitor cells. Cell. 1997;88:197-204.
18. Mandanas RA, Leibowitz DS, Gharehbaghi K, et al. Role of p21 RAS in p210 bcr-abl transformation of murine myeloid cells. Blood. 1993;82:1838-1847.
19. Raitano AB, Halpern JR, Hambuch TM, Sawyers CL.The Bcr-Abl leukemia oncogene activates Jun kinase and requires Jun for transformation. Proc Natl Acad Sci U S A. 1995;92:11746-11750.
20. Shuai K, Halpern J, ten Hoeve J, Rao X, Sawyers CL. Constitutive activation of STAT5 by the BCR-ABL oncogene in chronic myelogenous leukemia. Oncogene. 1996;13:247-254.
21. Carlesso N, Frank DA, Griffin JD. Tyrosyl phosphorylation and DNA binding activity of signal transducers and activators of transcription (STAT) proteins in hematopoietic cell lines transformed by Bcr/Abl. J Exp Med. 1996;183:811-820.
22. Skorski T, Kanakaraj P, Nieborowska-Skorska M, et al. Phosphatidylinositol-3 kinase activity is regulated by BCR/ABL and is required for the growth of Philadelphia chromosome-positive cells. Blood. 1995;86:726-736.
23. Reuther JY, Reuther GW, Cortez D, Pendergast AM, Baldwin AS Jr. A requirement for NF-kappaB activation in Bcr-Abl-mediated transformation. Genes Dev. 1998;12:968-981.
24. Ron D, Zannini M, Lewis M, et al. A region of proto-dbl essential for its transforming activity shows sequence similarity to a yeast cell cycle gene, CDC 24, and the human breakpoint cluster gene, bcr. New Biol. 1991;3:372-379.
25. Afar DEH, Goga A, Cohen L, et al. Genetic approaches to defining signaling by the CML-associated tyrosine kinase BCR-ABL. Cold Spring Harb Symp Quant Biol. 1994;59:589-594.
26. McWhirter JR, Galasso DL, Wang JYJ. A coiled-coil oligomerization domain of Bcr is essential for the transforming function of Bcr-Abl oncoproteins. Mol Cell Dial. 1993;13:7587-7595.
27. Pendergast AM, Muller AJ, Havlik MH, Maru Y, Witte ON. BCR sequences essential for transformation by the BCR/ABL oncogene bind to the ABL SH2 regulatory domain in a non-phosphotyrosine-dependent manner. Cell. 1991;66:161-171.
28. Maru YM, Witte ON. The BCR gene encodes a novel serine/threonine kinase activity within a single exon. Cell. 1991;67:459-468.
29. Pendergast AM, Gishizky ML, Havlik MH, Witte ON. SH1 domain autophosphorylation of P210 BCR/ABL is required for transformation but not growth factor-independence. Mol Cell Biol. 1993;13:1728-1736.
30. Sawyers CL. Molecular studies in chronic myeloid leukemia patients treated with tyrosine kinase inhibitors. Semin Hematol. 2001;38:15-21.
31. Afar DEH, Goga A, McLaughlin J, Witte O, Sawyers CL. Differential rescue of BCR-ABL point mutants with c-MYC. Science. 1994;264:424-426.
32. Gaiger A, Henn T, Horth E, et al. Increase of bcr-abl chimeric mRNA expression in tumor cells of patients with chronic myeloid leukemia precedes disease progression. Blood. 1995;86:2371-2378.
33. Wong S, Witte O. Modeling Philadelphia chromosome positive leukemias. Oncogene. 2001;20:5644-5659.
34. Heisterkamp N, Jenster G, ten Hoeve J, Zovich D, Pattengale PK, Groffen J. Acute leukaemia in bcr/abl transgenic mice. Nature. 1990;344:251-253.
35. Voncken JW, Karrtinen V, Pattengale PK, Germeraad WTV, Groffen J, Heisterkamp N. BCR/ABL P210 and P190 cause distinct leukemia in transgenic mice. Blood. 1995;86:4603-4611.
36. Honda H, Oda H, Suzuki T, et al. Development of acute lymphoblastic leukemia and myeloproliferative disorder in transgenic mice expressing p210bcr/abl: a novel transgenic model for human Phi-positive leukemias. Blood. 1998;91:2067-2075.
37. bcr/abl gene of the Philadelphia chromosome. Science. 1990;247:824-830.
38. 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;9:1069-1078.
39. Gishizky ML, Johnson-White J, Witte ON. Efficient transplantation of BCR/ABL induced chronic myelogenous leukemia-like syndrome in mice. Proc Natl Acad Sci U S A. 1993;90:3755-3759.
40. Zhang X, Ren R. Bcr-Abl efficiently induces a myeloproliferative disease and production of excess interleukin-3 and granulocyte-macrophage colony-stimulating factor in mice: a novel model for chronic myelogenous leukemia. Blood. 1998;92:3829-3840.
41. Pear WS, Miller JP, Xu L, et al. Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood. 1998;92:3780-3792.
42. Kabarowski JHS, Witte O. Consequences of BCR-ABL expression within the hematopoietic stem cell in chronic myeloid leukemia. Stem Cells. 2000;18:399-408.
43. Fialkow PJ, Jacobson RJ, Papayannopoulou T. Chronic myelocytic leukemia: clonal origin in a stem cell common to the granulocyte, erythrocyte, platelet and monocyte/macrophage. Am J Med. 1977;63:125-130.
44. Bedi A, Zehnbauer BA, Collector MI, et al. BCR-ABL gene rearrangement and expression of primitive hematopoietic progenitors in chronic myeloid leukemia. Blood. 1993;81:2898-2902.
45. Wetzler M, Talpaz M, Van Etten RA, Hirsh-Ginsberg C, Beran M, Kurzrock R. Subcellular localization of bcr, abl, and bcr-abl proteins in normal and leukemic cells and correlation of expression with myeloid differentiation. J Clin Invest. 1993;92:1925-1939.
46. + cells from patients with chronic myeloid leukemia. Blood. 1996;88:1796-1804.
47. Takahashi N, Miura I, Saitoh K, Miura AB. Lineage involvement of stem cells bearing the Philadelphia chromosome in chronic myeloid leukemia in the chronic phase as shown by a combination of fluorescence-activated cell sorting and fluorescence in situ hybridization. Blood. 1998;92:4758-4763.
48. Irving JA, Lennard A, Storey N, et al. Analysis of CD34 populations in mobilised peripheral blood stem cell harvests and in bone marrow by fluorescent in situ hybridisation for the bcr/abl gene fusion in patients with chronic granulocytic leukaemia. Leukemia. 1999;13:944-949.
49. Miyajima A, Ito Y, Kinoshita T. Cytokine signaling for proliferation, survival, and death in hematopoietic cells. Int J Hematol. 1999;69:137-146.
50. Domen J, Cheshier SH, Weissman IL. The role of apoptosis in the regulation of hematopoietic stem cells: overexpression of Bcl-2 increases both their number and repopulation potential. J Exp Med. 2000;191:253-264.
51. - progenitor cells in early chronic phase, but not in more advanced phases, of chronic myelogenous leukemia are polyclonal. Blood. 1999;93:284-292.
52. Gordon MY, Dazzi F, Marley SB, et al. Cell biology of CML cells. Leukemia. 1999;13(suppl):S65-S71.
53. Pierce A, Spooncer E, Wooley S, et al. Bcr-Abl protein tyrosine kinase activity induces a loss of p53 protein that mediates a delay in myeloid differentiation. Oncogene. 2000;19:5487-5497.
54. Gossen M, Bujard H. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc Natl Acad Sci U S A. 1992;89:5547-5551.
55. Era T, Witte ON. Regulated expression of P210 Bcr-Abl during embryonic stem cell differentiation stimulates multipotential progenitor expansion and myeloid cell fate. Proc Natl Acad Sci U S A. 2000;97:1737-1742.
56. Witte ON. The role of Bcr-Abl in chronic myeloid leukemia and stem cell biology. Sem Hematol. 2001;38:3-8.
57. Evans MJ, Kaufman M. Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981;292:154-156.
58. Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A. 1981;78:7634-7638.
59. Doetschman TC, Eistetter H, Katz M, Schmidt W, Kemler R. The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol. 1985;87:27-45.
60. Bradley A, Evans M, Kaufman MH, Robertson E. Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature. 1984;309:255-256.
61. Wiles MV, Keller G. Multiple hematopoietic lineages develop from embryonic stem (ES) cells in culture. Development. 1991;111:259-267.
62. Nakano T, Kodama H, Honjo T. Generation of lymphohematopoietic cells from embryonic stem cells in culture. Science. 1994;265:1098-1101.
63. Nishikawa SI, Nishikawa S, Hirashima M, Matsuyoshi N, Kodama H. Progressive lineage analysis by cell sorting and culture identifies FLK1+VE-cadherin+ cells at a diverging point of endothelial and hemopoietic lineages. Development. 1998;125:1747-1757.
64. Yoshida H, Hayashi SI, Kunisada T, et al. The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature. 1990;345:442-444.
65. Nakano T, Kodama HH. In vitro development of primitive and definitive erythrocytes from different precursors. Science. 1996;272:722-724.
66. Era T, Takagi T, Takahashi T, Bories JC, Nakano T. Characterization of hematopoietic lineage-specific gene expression by ES cell in vitro differentiation induction system. Blood. 2000;95:870-878.
67. Era T, Takahashi T, Sakai K, Kawamura K, Nakano T. Thrombopoietin enhances proliferation and differentiation of murine yolk sac erythroid progenitors. Blood. 1997;89:1207-1213.
68. Baron U, Gossen M, Bujard H. Tetracycline-controlled transcription in eukaryotes: novel transactivators with graded transactivation potential. Nucleic Acids Res. 1997;25:2723-2729.
69. Niwa H, Yamamura K, Miyazaki J. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene. 1991;108:193-199.
70. Moore MA, Metcalf D. Ontogeny of the haemopoietic system: yolk sac origin of in vivo and in vitro colony forming cells in the developing mouse embryo. Br J Haematol. 1970;18:279-296.
71. Godin I, Dieterlen-Lievre F, Cumano A. Emergence of multipotent hemopoietic cells in the yolk sac and paraaortic splanchnopleura in mouse embryos, beginning at 8.5 days postcoitus. Proc Natl Acad Sci U S A. 1995;92:773-777.
72. Medvinsky A, Dzierzak E. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell. 1996;86:897-906.
73. Yoder MC, Hiatt K, Dutt P, Mukherjee P, Bodine DM, Orlic D. Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac. Immunity. 1997;7:335-344.
74. Kennedy M, Firpo M, Choi K, et al. A common precursor for primitive erythropoiesis and definitive haematopoiesis. Nature. 1997;386:488-493.
75. Muller AM, Dzierzak EA. ES cells have only a limited lymphopoietic potential after adoptive transfer into mouse recipients. Development. 1993;118:1343-1351.
76. Matsuoka S, Tsuji K, Hisakawa H, et al. Generation of definitive hematopoietic stem cells from murine early yolk sac and paraaortic splanchnopleures by aorta-gonad-mesonephros region-derived stromal cells. Blood. 2001;98:6-12.
77. Perlingeiro RC, Kyba M, Daley GQ. Clonal analysis of differentiating embryonic stem cells reveals a hematopoietic progenitor with primitive erythroid and adult lymphoid-myeloid potential. Development. 2001;128:4597-4604.
78. Snow JW, Abraham N, Ma MC, Abbey NW, Herndier B, Goldsmith MA. STAT5 promotes multilineage hematolymphoid development in vivo through effects on early hematopoietic progenitor cells. Blood. 2002;99:95-101.
79. Klucher KM, Lopez DV, Daley GQ. Secondary mutation maintains the transformed state in BaF3 cells with inducible BCR/ABL expression. Blood. 1998;91:3927-3934.
80. Nieborowska-Skorska M, Wasik MA, Slupianek A, et al. Signal transducer and activator of transcription (STAT)5 activation by BCR/ABL is dependent on intact src homology (SH)3 and SH2 domains of BCR/ABL and is required for leukemogenesis. J Exp Med. 1999;189:1229-1242.
81. Gross AW, Zhang X, Ren R. Bcr-Abl with an SH3 deletion retains the ability to induce a myeloproliferative disease in mice, yet c-Abl activated by an SH3 deletion induces only lymphoid malignancy. Mol Cell Biol. 1999;19:6918-6928.
82. Palis J, Robertson S, Kennedy M, Wall C, Keller G. Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development. 1999;126:5073-5084.
83. Salgia R, Li J-L, Lo SH, et al. Molecular cloning of human paxillin, a focal adhesion protein phosphorylated by P210{+BCR/ABL}. J Biol Chem. 1995;270:5039-5047.
84. Bazzoni G, Carlesso N, Griffin JD, Hemler ME. Bcr/Abl expression stimulates integrin function in hematopoietic cell lines. J Clin Invest. 1996;98:521-528.
85. Williams DA, Rios M, Stephens C, Patel VP. Fibronectin and VLA-4 in haematopoietic stem cell-microenvironment interactions. Nature. 1991;352:438-441.
86. Craddock CF, Nakamoto B, Andrews RG, Priestley GV, Papayannopoulou T. Antibodies to VLA4 integrin mobilize long-term repopulating cells and augment cytokine-induced mobilization in primates and mice. Blood. 1997;90:4779-4788.
87. Maru Y. Molecular biology of chronic myeloid leukemia. Int J Hematol. 2001;73:308-322.
88. Clarkson B, Strife A. Linkage of proliferative and maturational abnormalities in chronic myelogenous leukemia and relevance to treatment. Leukemia. 1993;7:1683-1721.
89. Carroll M, Ohno-Jones S, Tamura S, et al. CPG 57148, a tyrosine kinase inhibitor, inhibits the growth of cells expressing BCR-ABL, TEL-ABL, and TEL-PDGFR fusion proteins. Blood. 1997;90:4947-4952.
90. Melo JV. BCR-ABL gene variants. Baillieres Clin Haematol. 1997;10:203-222.
91. Janssen JW, Ridge SA, Papadopoulos P, et al. The fusion of TEL and ABL in human acute lymphoblastic leukaemia is a rare event. Br J Haematol. 1995;90:222-224.
92. Hannemann JR, McManus DM, Kabarowski JH, Wiedemann LM. Haemopoietic transformation by the TEL/ABL oncogene. Br J Haematol. 1998;102:475-485.
93. Li S, Ilaria RL, Million RP, Daley GQ, Van Etten RA. The P190, P210, and P230 forms of the BCR/ABL oncogene induce a similar chronic myeloid leukemia-like syndrome in mice but have different lymphoid leukemogenic activity. J Exp Med. 1999;189:1399-1412.