Constitutive activation of FLT3 stimulates multiple intracellular signal transducers and results in transformation (original) (raw)

References

  1. D'Andrea A . Hematopoietic growth factors and the regulation of differentiative decisions Curr Opin Cell Biol 1994 6: 804–805
    Article CAS Google Scholar
  2. Miyajima A, Kitamura T, Haroda N, Yokota T, Arai K-I . Cytokine receptors and signal transduction Annu Rev Immunol 1992 10: 295–331
    Article CAS Google Scholar
  3. Metcalf D . Cellular hematopoiesis in the twentieth century Semin Hematol 1999 36: 5–12
    CAS PubMed Google Scholar
  4. Yarden Y, Ullrich A . Growth factor receptor tyrosine kinases Ann Rev Biochem 1988 57: 443–478
    Article CAS Google Scholar
  5. Hanks SK, Quinn AM, Hunter T . The protein kinase family conserved features and deduced phylogeny of the catalytic domains Science 1988 241: 42–52
    Article CAS Google Scholar
  6. Rosnet O, Birnbaum D . Hematopoietic receptors of class III receptor-type tyrosine kinases Crit Rev Oncog 1993 4: 595–613
    CAS PubMed Google Scholar
  7. Small D, Levenstein M, Kim E, Carow C, Amin S, Rockwell P, Witte L, Burrow C, Ratajczak M, Gewirtz AM, Civin C . STK-1, the human homolog of Flk-2/FLT-3, is selectively expressed in CD34+ human bone marrow cells and is involved in the proliferation of early progenitor/stem cells Proc Natl Acad Sci USA 1994 91: 459–463
    Article CAS Google Scholar
  8. Rappold I, Ziegler BL, Kohler I, Marchetto S, Rosnet O, Birnbaum D, Simmons PJ, Zannettino ACW, Hill B, Neu S, Knapp W, Alitalo R, Alitalo K, Ullrich A, Kanz L, Buhring H-J . Functional and phenotypic characterization of cord blood and bone marrow subsets expressing FLT3 (CD135) receptor tyrosine kinase Blood 1997 90: 111–1125
    CAS PubMed Google Scholar
  9. Brasel K, Escobar S, Anderberg R, de Vries P, Gruss H-J, Lyman SD . Expression of the Flt3 receptor and its ligand on hematopoietic cells Leukemia 1995 9: 1212–1218
    CAS PubMed Google Scholar
  10. Gotze KS, Ramirez M, Tabor K, Small D, Matthews W, Civin CI . Flt3high and Flt3low CD34+ progenitor cells isolated from human bone marrow are functionally distinct Blood 1997 91: 1947–1958.
    Google Scholar
  11. Gabbianelli M, Pelosi E, Montesoro E, Valtieri M, Luchetti L, Samoggia P, Vitelli L, Barberi T, Testa U, Lyman S . Multi-level effects of Flt3 ligand on human hematopoiesis: expansion of putative stem cells and proliferation of granulomonocytic progenitors/monocytic precursors Blood 1995 86: 1661–1670
    CAS PubMed Google Scholar
  12. Shah AJ, Smogorzewska EM, Hannum C, Crooks GM . Flt3 ligand induces proliferation of quiescent human bone marrow CD34+CD38− cells and maintains progenitor cells in vitro Blood 1996 87: 3563–3570
    CAS PubMed Google Scholar
  13. Hirayama F, Lyman SD, Clark SC, Ogawa M . The flt3 ligand supports proliferation of lymphohematopoietic progenitors and early B-lymphoid progenitors Blood 1995 85: 1762–1768
    CAS PubMed Google Scholar
  14. Hunte BE, Hudak S, Campbell D, Xu Y, Rennick D . Flk2/Flt3 ligand is a potent cofactor for the growth of primitive B cell progenitors J Immunol 1996 156: 489–496
    CAS PubMed Google Scholar
  15. Mackaretschian K, Hardin JD, Moore KA, Boast S, Goff SP, Lemischka IR . Targeted disruption of the Flk2/Flt3 gene leads to deficiencies in primitive hematopoietic progenitors Immunity 1995 3: 147–161
    Article Google Scholar
  16. Hannum C, Culpepper J, Campbell D, McClanahan T, Zurawski S, Bazan JF, Kastelein R, Hudak S, Wagner J, Mattson J, Luh J, Duda G, Martina N, Peterson D, Menon S, Shanafelt A, Muench M, Keiner G, Namikawa R, Rennick D, Roncarolo MG, Zlotnik A, Rosnet O, Dubreuil P, Birnbaum D, Lee F . Ligand for FLT3/FLK2 receptor tyrosine kinase regulates growth of haematopoietic stem cells and is encoded by variant RNAs Nature 1994 368: 643–648.
    Article CAS Google Scholar
  17. McKenna HJ, de Vries P, Brasel K, Lyman SD, Williams DE . Effect of Flt3 ligand on the ex vivo expansion of human CD34+ hematopoietic progenitor cells Blood 1995 86: 3413–3420
    CAS PubMed Google Scholar
  18. Lyman SD, Jacobsen SEW . c-kit ligand and Flt3 ligand: stem/progenitor cell factors with overlapping yet distinct activities Blood 1998 91: 1101–1134
    CAS PubMed Google Scholar
  19. van der Geer P, Hunter T, Lindberg R . Receptor protein-tyrosine kinases and their signal transduction pathways Annu Rev Cell Biol 1994 10: 251–337
    Article CAS Google Scholar
  20. Heldin C . Dimerization of cell surface receptors in signal transduction Cell 1995 80: 213–223
    Article CAS Google Scholar
  21. Dosil M, Wang S, Lemischka I . Mitogenic signalling and substrate specificity of the Flk2/Flt3 receptor tyrosine kinase in fibroblasts and interleukin 3-dependent hematopoietic cells Mol Cell Biol 1993 13: 6572–6585
    Article CAS Google Scholar
  22. Rottapel R, Turck, CW, Casteran N, Liu X, Birnbaum D, Pawson T, Dubreuil P . Substrate specificities and identification of a putative binding site for PI3K in the carboxy tail of the murine Flt3 receptor tyrosine kinase Oncogene 1994 9: 1755–1765
    CAS PubMed Google Scholar
  23. Casteran N, Rottapel R, Beslu N, Lecocq E, Birnbaum D, Dubreuil P . Analysis of the mitogenic pathway of the FLT3 receptor and characterization in its C terminal region of a specific binding site for the PI3′ kinase Cell Mol Biol 1994 40: 443–456
    CAS PubMed Google Scholar
  24. Lavagna-Sevenier C, Marchetto S, Birnbaum D, Rosnet O . FLT3 signaling in hematopoietic cells involves CBL, SHC and an unknown P115 as prominent tyrosine-phosphorylated substrates Leukemia 1998 12: 301–310
    Article CAS Google Scholar
  25. Zhang S, Mantel C, Broxmeyer HE . Flt3 signaling involves tyrosyl-phosphorylation of SHP-2 and SHIP and their association with Grb2 and Shc in Baf3/Flt3 cells J Leukoc Biol 1999 65: 372–380
    Article CAS Google Scholar
  26. Zhang S, Broxmeyer HE . p85 Subunit of P13 kinase does not bind to human Flt3 receptor, but associates with SHP2, SHIP, and a tyrosine-phosphorylated 100-kDa protein in Flt3 ligand-stimulated hematopoietic cells Biochem Biophys Res Commun 1999 254: 440–445
    Article CAS Google Scholar
  27. Hayakawa F, Towatari M, Kiyoi H, Tanimoto M, Kitamura T, Saito H, Naoe T . Tandem-duplicated Flt3 constitutively activates STAT5 and MAP kinase and introduces autonomous cell growth in IL-3-dependent cell lines Oncogene 2000 19: 624–631
    Article CAS Google Scholar
  28. Carow CE, Levenstein M, Kaufmann SH, Chen J, Amin S, Rockwell P, Witte L, Borowitz MJ, Civin CI, Small D . Expression of the hematopoietic growth factor receptor FLT3 (STK-1/Flk2) in human leukemias Blood 1996 87: 1089–1096
    CAS PubMed Google Scholar
  29. Birg F, Courcoul M, Rosnet O, Bardin F, Pebusque M, Marchetto S, Tabilio A, Mannoni P, Birnbaum D . Expression of the FMS/KIT-like gene FLT3 in human acute leukemias of the myeloid and lymphoid lineages Blood 1992 80: 2584–2593
    CAS PubMed Google Scholar
  30. Rosnet O, Buhring HJ, Marchetto S, Rappold I, Lavagna C, Sainty D, Arnoulet C, Chabannon C, Kanz L, Hannum C, Birnbaum D . Human FLT3/FLK2 receptor tyrosine kinase is expressed at the surface of normal and malignant hematopoietic cells Leukemia 1996 10: 238–248
    CAS PubMed Google Scholar
  31. Turner AM, Lin NL, Issarachai S, Lyman SD, Broudy VC . FLT3 receptor expression on the surface of normal and malignant human hematopoietic cells Blood 1996 88: 3383–3390
    CAS PubMed Google Scholar
  32. Dehmel U, Zaborski M, Meierhoff G, Rosnet O, Birnbaum D, Ludwig WD, Quentmeier H, Drexler HG . Effects of Flt3 ligand on human leukemia cells. I. Proliferative response of myeloid leukemia cells Leukemia 1996 10: 261–270
    CAS PubMed Google Scholar
  33. Lisovsky M, Estrov Z, Zhang X, Consoli U, Sanchez-Williams G, Snell V, Munker R, Goodacre A, Savchenko V, Andreeff M . Flt3 ligand stimulates proliferation and inhibits apoptosis of acute myeloid leukemia cells: regulation of Bcl-2 and Bax Blood 1996 88: 3987–3997
    CAS PubMed Google Scholar
  34. Meierhoff G, Dehmel U, Gruss H-J, Rosnet O, Birnbaum D, Quentmeier H, Dirks W, Drexler HG . Expression of FLT3 receptor and FLT3-ligand in human leukemia–lymphoma cell lines Leukemia 1995 9: 1368–1372
    CAS PubMed Google Scholar
  35. Lisovsky M, Braun M, Ge Y, Takahira H, Lu L, Savchenko VG, Lyman SD, Broxmeyer HE . Flt3-ligand production by human bone marrow stromal cells Leukemia 1996 10: 1012–1018
    CAS PubMed Google Scholar
  36. Solanilla AGC, Lemervier C, Dupouy M, Mahon FX, Schweitzer K, Reiffers J, Weksler B, Ripoche J . Expression of Flt3-ligand by the endothelial cell Leukemia 2000 14: 153–162
    Article CAS Google Scholar
  37. Pietsch T, Kyas U, Yakisan E, Hadam M, Ludwig W, Zsebo K, Welte K . Effects of human stem cell factor (c-kit ligand) on proliferation of myeloid leukemia cells: heterogeneity in response and synergy with other hematopoietic growth factors Blood 1992 80: 1199–1206
    CAS PubMed Google Scholar
  38. Torres H, Dubrueil P, Falzetti F, Courcoul M, Lopez M, Falcinelli F, Birg F, Tabilio A, Mannoni P . c-fms expression in acute leukemias with complex phenotypes Leukemia 1990 4: 673–677
    CAS PubMed Google Scholar
  39. Parwaresch MR, Kriepe H, Felgner J, Heidorn K, Jaquet K, Bodewadt-Radzun S, Radzun HJ . M-CSF and M-CSF receptor gene expression in acute myelomonocytic leukemias Leuk Res 1990 14: 27–37
    Article CAS Google Scholar
  40. Metcalf D . The roles of stem cell self-renewal and autocrine growth factor production in the biology of myeloid leukemia Cancer Res 1989 49: 2305–2311
    CAS PubMed Google Scholar
  41. Hawley R . Interleukin-6-type cytokines in myeloproliferativedisease Ann NY Acad Sci 1995 762: 294–307
    Article CAS Google Scholar
  42. Horiike S, Yokota S, Nakao M, Iwaai T, Sasai Y, Kaneko H, Taniwaki M, Kashima K, Fujii H, Abe T, Misawa S . Tandemduplications of the FLT3 receptor gene are associated with leukemic transformation of myelodysplasia Leukemia 1997 11: 1442–1446
    Article CAS Google Scholar
  43. Nakao M, Yokota S, Iwai T, Kaneko H, Horiike S, Kashima K, Sonoda Y, Fujimoto T, Misawa S . Internal tandem duplication of the Flt3 gene found in acute myeloid leukemia Leukemia 1996 10: 1911–1918
    CAS PubMed Google Scholar
  44. Iwai T, Yokota S, Nakao M, Okamoto T, Taniwaki M, Onodera N, Watanabe A, Kikuta A, Tanaka A, Asami K, Sekine I, Mugishima H, Nishimura Y, Koizumi S, Horikoski Y, Mimaya J, Ohta S, Nishikawa K, Iwai A, Shimokawa T, Nakayama M, Kawakami K, Gushiken T, Hyakuna N, Katano N, Tsurusawa M, Fujimoto T . Internal tandem duplication of the FLT3 gene and clinical evaluation in childhood acute myeloid leukemia Leukemia 1999 13: 38–43.
    Article CAS Google Scholar
  45. Xu F, Taki T, Yang HW, Hanada R, Hongo T, Ohnishi H, Kobayashi M, Bessho F, Yanagisawa M, Hayashi Y . Tandem duplication of the FLT3 gene is found in acute lymphoblastic leukaemia as well as acute myeloid leukaemia but not in myelodysplastic syndrome or juvenile chronic myelogenous leukaemia in children Br J Haematol 1999 105: 155–162
    Article CAS Google Scholar
  46. Kiyoi H, Towatari M, Yokota S, Hamaguchi M, Ohno R, Saito H, Naoe T . Internal tandem duplication of the FLT3 gene is a novel modality of elongation mutation which causes constitutive activation of the product Leukemia 1998 12: 1333–1337
    Article CAS Google Scholar
  47. Jousset C, Carron C, Oury C, Susanter-Fourt I, Charon M, Levin J, Bernard O, Ghysdael J . A domain of TEL conserved in a subset of ETS proteins defines a specific oligomerization interface essential to the mitogenic properties of the TEL-PDGFRB oncoprotein EMBO J 1997 16: 69–82
    Article CAS Google Scholar
  48. Golub T, Goga A, Barker G, Afar D, McLaughlin J . Oligomerization of the ABL tyrosine kinase by the Ets protein TEL in human leukemia Mol Cell Biol 1996 16: 4107–4116
    Article CAS Google Scholar
  49. Golub TR, Barker GF, Lovett M, Gilliland DG . Fusion of PDGF receptor β to a novel ets-like gene, tel, in chronic myelomonocytic leukemia with t(5;12) chromosomal translocation Cell 1994 77: 307–316
    Article CAS Google Scholar
  50. Golub TR, Barker GF, Stegmaier K, Gilliland DG . Involvement of the TEL gene in hematologic malignancy by diverse molecular genetic mechanisms Curr Top Microbiol Immunol 1996 211: 279–288
    CAS PubMed Google Scholar
  51. Carroll M, Tomasson MH, Barker GF, Golub TR, Gilliland DG . The TEL/platelet-derived growth factor β receptor (PDGFβR) fusion in chronic meylomonocytic leukemia is a transforming protein that self-associates and activates PDGFBR kinase-dependent signaling pathways Proc Natl Acad Sci USA 1996 93: 14845–14850.
    Article CAS Google Scholar
  52. Papadopoulos P, Ridge SA, Boucher CA, Stocking C, Wiedermann LM . The novel activation of ABL by fusion to an ets-related gene, TEL Cancer Res 1995 55: 34–38
    CAS PubMed Google Scholar
  53. Peeters P, Raynaud SD, Cools J, Wlodarska I, Grosgeorge J, Philip P, Monpoux F, Van Rompaey L, Baens M, Van den Gerghe H, Maryen P . Fusion of TEL, the ETS-variant gene 6 (ETV6), to the receptor-associated kinase JAK2 as a result of t(9;12) in a lymphoid and t(9;15;12) in a myeloid leukemia Blood 1997 90: 2535–2540.
    CAS PubMed Google Scholar
  54. Lacronique V, Boureux A, Valle VD, Poirel H, Quang CT, Mauchauffe M, Berthou C, Lessard M, Berger R, Ghysdael J, Bernard OA . A TEL-JAK2 fusion protein with constitutive kinase activity in human leukemia Science 1997 278: 1309–1312
    Article CAS Google Scholar
  55. Weiss A, Schlessinger J . Switching signals on or off by receptor dimerization Cell 1998 94: 277–280
    Article CAS Google Scholar
  56. Hara T, Miyajima A . Function and signal transduction mediated by the interleukin 3 receptor system in hematopoiesis Stem Cells 1996 14: 605–618
    Article CAS Google Scholar
  57. Darnell JE, Kerr IM, Stark G . Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins Science 1994 264: 1415–1420
    Article CAS Google Scholar
  58. Fukazawa T, Reedquist K, Trub T, Soltoff S, Panchamoorthy G, Druker B, Cantley L, Shoelson S, Band H . The SH3 domain-binding T cell tyrosyl phosphoprotein p120. Demonstration of its identity with the c-cbl protooncogene product and in vivo complexes with Fyn, Grb2, and phosphatidylinositol 3-kinase J Biol Chem 1995 270: 19141–19150
    Article CAS Google Scholar
  59. Donovan J, Wange R, Langdon W, Samelson L . The protein product of the c-cbl protooncogene is the 120-kDa tyrosine-phosphorylated protein in Jurkat cells activated via the T cell antigen receptor J Biol Chem 1994 269: 22921–22924
    CAS PubMed Google Scholar
  60. Langdon WY, Hartley JW, Klinken SP, Ruscetti SK, Morse HC . v-cbl, an oncogene from a dual-recombinant murine retrovirus that induces early B-lineage lymphomas Proc Natl Acad Sci USA 1989 86: 1168–1172
    Article CAS Google Scholar
  61. Barber DL, Mason JM, Fukazawa T, Reedquist KA, Druker BJ, Band H, D'Andrea AD . Erythropoietin and interleukin-3 activate tyrosine phosphorylation of CBL and association with CRK adaptor proteins Blood 1997 89: 3166–3174
    CAS PubMed Google Scholar
  62. Joazeiro CAWS, Huang H, Leverson JD, Hunter T, Liu YC . The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase Science 1999 286: 309–312
    Article CAS Google Scholar
  63. Hawley TS, Fong AZC, Griesser H, Lyman SD, Hawley RG . Leukemic predisposition of mice transplanted with gene-modified hematopoietic precursors expressing flt3 ligand Blood 1998 92: 2003–2011
    CAS PubMed Google Scholar
  64. Yokota S, Kiyoi H, Nakao M, Iwai T, Misawa S, Okuda T, Sonoda Y, Abe T, Kashima K, Matsuo Y, Naoe T . Internal tandem duplication of the FLT3 gene is preferentially seen in acute myeloid leukemia and myelodysplastic syndrome among various hematological malignancies. A study on a large series of patients and cell lines Leukemia 1997 11: 1605–1609
    Article CAS Google Scholar
  65. Zhong Z, Wen Z, Darnell J . Stat3: a STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6 Science 1994 264: 95–98
    Article CAS Google Scholar
  66. Sachsenmaier C, Sadowski HB, Cooper JA . STAT activation by the PDGF receptor requires juxtamembrane phosphorylation sites but not Src tyrosine kinase activation Oncogene 1999 18: 3583–3592
    Article CAS Google Scholar
  67. Novak U, Nice E, Hamilton JA, Paradiso L . Requirement for Y706 of the murine (or Y708 of the human) CSF-1 receptor for STAT1 activation in response to CSF-1 Oncogene 1996 13: 2607–2613
    CAS PubMed Google Scholar
  68. Novak U, Mui A, Miyajima A, Paradiso L . Formation of STAT5-containing DNA binding complexes in response to colony-stimulating factor-1 and platelet-derived growth factor J Biol Chem 1996 271: 18350–18354
    Article CAS Google Scholar
  69. Deberry C, Mou S, Linnekin K . Stat1 associates with c-kit and is activated in response to stem cell factor Biochem J 1997 327: 73–80
    Article CAS Google Scholar
  70. Ryan JJ, Huang H, McReynolds LJ, Shelburne C, Hu-Li J, Huff TF, Paul WE . Stem cell factor activates STAT-5 DNA binding in IL-3-derived bone marrow mast cells Exp Hematol 1997 25: 357–362
    CAS PubMed Google Scholar
  71. Wang Y, Yeung Y-G, Langdon WY, Stanley ER . c-cbl is transiently tyrosine-phosphorylated, ubiquininated, and membrane-targeted following CSF-1 stimulation of macrophages J Biol Chem 1996 271: 17–20
    Article CAS Google Scholar
  72. Odai H, Sasaki K, Iwamatsu A, Hanazono Y, Tanaka T, Mitani K, Yazaki Y, Hirai H . The proto-oncogene product c-Cbl becomes tyrosine phosphorylated by stimulation with GM-CSF or Epo and constitutively binds to the SH3 domain of Grb2/Ash in human hematopoietic cells J Biol Chem 1995 270: 10800–10805
    Article CAS Google Scholar
  73. Lavagna-Sevenier C, Marchetto S, Birnbaum D, Rosnet O . The CBL-related protein CBLB participates in FLT3 and interleukin-7 receptor signal transduction in pro-B cells J Biol Chem 1998 273: 14962–14967
    Article CAS Google Scholar
  74. Ribon V, Hubbell S, Herrera R, Saltiel AR . The product of the cbl oncogene forms stable complexes in vivo with endogenous Crk in a tyrosine phosphorylation-dependent manner Mol Cell Biol 1996 16: 45–52
    Article CAS Google Scholar
  75. Sattler M, Salgia R, Okuda K, Uemura N, Durstin MA, Pisick E, Xu G, Li J-L, Prasad KV, Griffin JD . The proto-oncogene product p120CBL and the adaptor proteins CRKL and c-CRK like c-ABL, p190 BCR/ABL and p210BCR/ABL to the phosphatidylinositol-3′ kinase pathway Oncogene 1996 12: 839–846
    CAS PubMed Google Scholar
  76. de Jong R, ten Hoeve J, Heisterkamp N, Groffen J . Crkl is complexed with tyrosine-phosphorylated Cbl in Ph-positive leukemia J Biol Chem 1995 270: 21468–21471
    Article CAS Google Scholar
  77. Zhao M, Kiyoi H, Yamamoto Y, Towatari M, Omura S, Kitamura T, Ueda R, Saito H, Naoe T . In vivo treatment of mutant FLT3-transformed murine leukemia with a tyrosine kinase inhibitor Leukemia 2000 14: 374–378
    Article CAS Google Scholar

Download references