Oncogenic Flt3 receptors display different specificity and kinetics of autophosphorylation

Experimental Hematology

Volumn 37, Issue 8, 2009, Pages 979-989

  Razumovskaya, Elena ^a   Masson, Kristina ^a   Khan, Rasheed ^a   Bengtsson, Susanne ^a   Rönnstrand, Lars ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; CD135 ANTIGEN; TYROSINE;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; CONTROLLED STUDY; GENE DUPLICATION; GENE MUTATION; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; WILD TYPE;

ANIMALS; BINDING SITES; CELL LINE; EPITOPE MAPPING; FMS-LIKE TYROSINE KINASE 3; KINETICS; LEUKEMIA, MYELOID, ACUTE; MICE; MUTANT PROTEINS; NEOPLASM PROTEINS; PHOSPHORYLATION; SUBSTRATE SPECIFICITY;

EID: 67650079715     PISSN: 0301472X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exphem.2009.05.008     Document Type: Article

References (60)

1. Nakao M., Yokota S., Iwai T., et al. Internal tandem duplication of the flt3 gene found in acute myeloid leukemia. Leukemia 10 (1996) 1911-1918
2. Gilliland D.G., and Griffin J.D. The roles of FLT3 in hematopoiesis and leukemia. Blood 100 (2002) 1532-1542
3. Small D., Levenstein M., Kim E., et al. 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 U S A 91 (1994) 459-463
4. Rosnet O., Marchetto S., deLapeyriere O., and Birnbaum D. Murine Flt3, a gene encoding a novel tyrosine kinase receptor of the PDGFR/CSF1R family. Oncogene 6 (1991) 1641-1650
5. Rosnet O., Mattei M.G., Marchetto S., and Birnbaum D. Isolation and chromosomal localization of a novel FMS-like tyrosine kinase gene. Genomics 9 (1991) 380-385
6. Turner A.M., Lin N.L., Issarachai S., Lyman S.D., and Broudy V.C. FLT3 receptor expression on the surface of normal and malignant human hematopoietic cells. Blood 88 (1996) 3383-3390
7. Brasel K., Escobar S., Anderberg R., de Vries P., Gruss H.J., and Lyman S.D. Expression of the flt3 receptor and its ligand on hematopoietic cells. Leukemia 9 (1995) 1212-1218
8. Kikushige Y., Yoshimoto G., Miyamoto T., et al. Human Flt3 is expressed at the hematopoietic stem cell and the granulocyte/macrophage progenitor stages to maintain cell survival. J Immunol 180 (2008) 7358-7367
9. Maroc N., Rottapel R., Rosnet O., et al. Biochemical characterization and analysis of the transforming potential of the FLT3/FLK2 receptor tyrosine kinase. Oncogene 8 (1993) 909-918
10. Maraskovsky E., Brasel K., Teepe M., et al. Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligand-treated mice: multiple dendritic cell subpopulations identified. J Exp Med 184 (1996) 1953-1962
11. Gilliland D.G., and Griffin J.D. Role of FLT3 in leukemia. Curr Opin Hematol 9 (2002) 274-281
12. Stirewalt D.L., and Radich J.P. The role of FLT3 in haematopoietic malignancies. Nat Rev Cancer 3 (2003) 650-665
13. Dosil M., Wang S., and Lemischka I.R. Mitogenic signalling and substrate specificity of the Flk2/Flt3 receptor tyrosine kinase in fibroblasts and interleukin 3-dependent hematopoietic cells. Mol Cell Biol 13 (1993) 6572-6585
14. Rosnet O., Bühring H.J., deLapeyriere O., et al. Expression and signal transduction of the FLT3 tyrosine kinase receptor. Acta Haematol 95 (1996) 218-223
15. Griffith J., Black J., Faerman C., et al. The structural basis for autoinhibition of FLT3 by the juxtamembrane domain. Mol Cell 13 (2004) 169-178
16. Kiyoi H., Ohno R., Ueda R., Saito H., and Naoe T. Mechanism of constitutive activation of FLT3 with internal tandem duplication in the juxtamembrane domain. Oncogene 21 (2002) 2555-2563
17. Yamamoto Y., Kiyoi H., Nakano Y., et al. Activating mutation of D835 within the activation loop of FLT3 in human hematologic malignancies. Blood 97 (2001) 2434-2439
18. Kiyoi H., Towatari M., Yokota S., et al. Internal tandem duplication of the FLT3 gene is a novel modality of elongation mutation which causes constitutive activation of the product. Leukemia 12 (1998) 1333-1337
19. Beghini A., Peterlongo P., Ripamonti C.B., et al. C-kit mutations in core binding factor leukemias. Blood 95 (2000) 726-727
20. Jeffers M., Schmidt L., Nakaigawa N., et al. Activating mutations for the met tyrosine kinase receptor in human cancer. Proc Natl Acad Sci U S A 94 (1997) 11445-11450
21. Liu X., Vega Q.C., Decker R.A., Pandey A., Worby C.A., and Dixon J.E. Oncogenic RET receptors display different autophosphorylation sites and substrate binding specificities. J Biol Chem 271 (1996) 5309-5312
22. Blume-Jensen P., Siegbahn A., Stabel S., Heldin C.H., and Rönnstrand L. Increased Kit/SCF receptor induced mitogenicity but abolished cell motility after inhibition of protein kinase C. EMBO J 12 (1993) 4199-4209
23. Voytyuk O., Lennartsson J., Mogi A., et al. Src family kinases are involved in the differential signaling from two splice forms of c-Kit. J Biol Chem 278 (2003) 9159-9166
24. Pumiglia K.M., Lau L.F., Huang C.K., Burroughs S., and Feinstein M.B. Activation of signal transduction in platelets by the tyrosine phosphatase inhibitor pervanadate (vanadyl hydroperoxide). Biochem J 286 Pt 2 (1992) 441-449
25. Lennartsson J., Blume-Jensen P., Hermanson M., Pontén E., Carlberg M., and Rönnstrand L. Phosphorylation of Shc by Src family kinases is necessary for stem cell factor receptor/c-kit mediated activation of the Ras/MAP kinase pathway and c-fos induction. Oncogene 18 (1999) 5546-5553
26. Heiss E., Masson K., Sundberg C., et al. Identification of Y589 and Y599 in the juxtamembrane domain of Flt3 as ligand-induced autophosphorylation sites involved in binding of Src family kinases and the protein tyrosine phosphatase SHP2. Blood 108 (2006) 1542-1550
27. Masson K, Liu T, Khan R, Sun J, Rönnstrand L. A role of Gab2 association in Flt3 ITD mediated STAT5 phosphorylation and cell survival. Br J Haematol. In press (2009).
28. Sweeney C., Lai C., Riese II D.J., Diamonti A.J., Cantley L.C., and Carraway III K.L. Ligand discrimination in signaling through an ErbB4 receptor homodimer. J Biol Chem 275 (2000) 19803-19807
29. Schmidt M.H., Furnari F.B., Cavenee W.K., and Bogler O. Epidermal growth factor receptor signaling intensity determines intracellular protein interactions, ubiquitination, and internalization. Proc Natl Acad Sci U S A 100 (2003) 6505-6510
30. Lundin L., Rönnstrand L., Cross M., Hellberg C., Lindahl U., and Claesson-Welsh L. Differential tyrosine phosphorylation of fibroblast growth factor (FGF) receptor-1 and receptor proximal signal transduction in response to FGF-2 and heparin. Exp Cell Res 287 (2003) 190-198
31. Horion J., Gloire G., El Mjiyad N., et al. Histone deacetylase inhibitor trichostatin A sustains sodium pervanadate-induced NF-kappaB activation by delaying IkappaBalpha mRNA resynthesis: comparison with tumor necrosis factor alpha. J Biol Chem 282 (2007) 15383-15393
32. Ishiko J., Mizuki M., Matsumura I., et al. Roles of tyrosine residues 845, 892 and 922 in constitutive activation of murine FLT3 kinase domain mutant. Oncogene 24 (2005) 8144-8153
33. Clark J.J., Cools J., Curley D.P., et al. Variable sensitivity of FLT3 activation loop mutations to the small molecule tyrosine kinase inhibitor MLN518. Blood 104 (2004) 2867-2872
34. Rocnik J.L., Okabe R., Yu J.C., et al. Roles of tyrosine 589 and 591 in STAT5 activation and transformation mediated by FLT3-ITD. Blood 108 (2006) 1339-1345
35. Heldin C.H., Östman A., and Rönnstrand L. Signal transduction via platelet-derived growth factor receptors. Biochim Biophys Acta 1378 (1998) F79-F113
36. Ronnstrand L. Signal transduction via the stem cell factor receptor/c-Kit. Cell Mol Life Sci 61 (2004) 2535-2548
37. Lennartsson J., Wernstedt C., Engström U., Hellman U., and Rönnstrand L. Identification of Tyr900 in the kinase domain of c-Kit as a Src-dependent phosphorylation site mediating interaction with c-Crk. Exp Cell Res 288 (2003) 110-118
38. Hansen K., Johnell M., Siegbahn A., et al. Mutation of a Src phosphorylation site in the PDGF beta-receptor leads to increased PDGF-stimulated chemotaxis but decreased mitogenesis. EMBO J 15 (1996) 5299-5313
39. Quentmeier H., Reinhardt J., Zaborski M., and Drexler H.G. FLT3 mutations in acute myeloid leukemia cell lines. Leukemia 17 (2003) 120-124
40. Zheng R., Levis M., Piloto O., et al. FLT3 ligand causes autocrine signaling in acute myeloid leukemia cells. Blood 103 (2004) 267-274
41. Kelly L.M., Liu Q., Kutok J.L., Williams I.R., Boulton C.L., and Gilliland D.G. FLT3 internal tandem duplication mutations associated with human acute myeloid leukemias induce myeloproliferative disease in a murine bone marrow transplant model. Blood 99 (2002) 310-318
42. Vempati S., Reindl C., Wolf U., et al. Transformation by oncogenic mutants and ligand-dependent activation of FLT3 wild-type requires the tyrosine residues 589 and 591. Clin Cancer Res 14 (2008) 4437-4445
43. Mizuki M., Schwäble J., Steur C., et al. Suppression of myeloid transcription factors and induction of STAT response genes by AML-specific Flt3 mutations. Blood 101 (2003) 3164-3173
44. Santoro M., Carlomagno F., Romano A., et al. Activation of RET as a dominant transforming gene by germline mutations of MEN2A and MEN2B. Science 267 (1995) 381-383
45. Miller M., Ginalski K., Lesyng B., Nakaigawa N., Schmidt L., and Zbar B. Structural basis of oncogenic activation caused by point mutations in the kinase domain of the MET proto-oncogene: modeling studies. Proteins 44 (2001) 32-43
46. Sun J., Pedersen M., and Rönnstrand L. The D816V mutation of c-Kit circumvents a requirement for Src family kinases in c-Kit signal transduction. J Biol Chem 24 284 (2009) 11039-11047
47. Schmidt-Arras D., Böhmer S.A., Koch S., et al. Anchoring of FLT3 in the endoplasmic reticulum alters signaling quality. Blood 113 (2009) 3568-3576
48. Choudhary C., Schwäble J., Brandts C., et al. AML-associated Flt3 kinase domain mutations show signal transduction differences compared with Flt3 ITD mutations. Blood 106 (2005) 265-273
49. Mizuki M., Fenski R., Halfter H., et al. Flt3 mutations from patients with acute myeloid leukemia induce transformation of 32D cells mediated by the Ras and STAT5 pathways. Blood 96 (2000) 3907-3914
50. Grundler R., Miething C., Thiede C., Peschel C., and Duyster J. FLT3-ITD and tyrosine kinase domain mutants induce 2 distinct phenotypes in a murine bone marrow transplantation model. Blood 105 (2005) 4792-4799
51. Levis M., and Small D. FLT3: ITDoes matter in leukemia. Leukemia 17 (2003) 1738-1752
52. Kato H., Faria T.N., Stannard B., Roberts Jr. C.T., and LeRoith D. Essential role of tyrosine residues 1131, 1135, and 1136 of the insulin-like growth factor-I (IGF-I) receptor in IGF-I action. Mol Endocrinol 8 (1994) 40-50
53. Mohammadi M., Schlessinger J., and Hubbard S.R. Structure of the FGF receptor tyrosine kinase domain reveals a novel autoinhibitory mechanism. Cell 86 (1996) 577-587
54. Longati P., Bardelli A., Ponzetto C., Naldini L., and Comoglio P.M. Tyrosines1234-1235 are critical for activation of the tyrosine kinase encoded by the MET proto-oncogene (HGF receptor). Oncogene 9 (1994) 49-57
55. Mol C.D., Lim K.B., Sridhar V., et al. Structure of a c-kit product complex reveals the basis for kinase transactivation. J Biol Chem 278 (2003) 31461-31464
56. Dong L.Q., Farris S., Christal J., and Liu F. Site-directed mutagenesis and yeast two-hybrid studies of the insulin and insulin-like growth factor-1 receptors: the Src homology-2 domain-containing protein hGrb10 binds to the autophosphorylated tyrosine residues in the kinase domain of the insulin receptor. Mol Endocrinol 11 (1997) 1757-1765
57. Moodie S.A., Alleman-Sposeto J., and Gustafson T.A. Identification of the APS protein as a novel insulin receptor substrate. J Biol Chem 274 (1999) 11186-11193
58. Kotani K., Wilden P., and Pillay T.S. SH2-Balpha is an insulin-receptor adapter protein and substrate that interacts with the activation loop of the insulin-receptor kinase. Biochem J 335 Pt 1 (1998) 103-109
59. Ungureanu D., Saharinen P., Junttila I., Hilton D.J., and Silvennoinen O. Regulation of Jak2 through the ubiquitin-proteasome pathway involves phosphorylation of Jak2 on Y1007 and interaction with SOCS-1. Mol Cell Biol 22 (2002) 3316-3326
60. Small D. FLT3 mutations: biology and treatment. Hematology Am Soc Hematol Educ Program (2006) 178-184