Constitutive c-jun N-terminal kinase activity in acute myeloid leukemia derives from Flt3 and affects survival and proliferation

Experimental Hematology

Volumn 34, Issue 10, 2006, Pages 1360-1376

  Hartman, Amy D ^a   Wilson Weekes, Annique ^b   Suvannasankha, Attaya ^b   Burgess, Gem S ^b   Phillips, Carissa A ^b   Hincher, Katie J ^b   Cripe, Larry D ^b   Boswell, H Scott ^a,b,c  

^a WALTHER CANCER INSTITUTE   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c RICHARD L ROUDEBUSH VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRACYCLINE; ARF PROTEIN; BCR ABL PROTEIN; CBL PROTEIN; CRK LIKE PROTEIN; DAUNORUBICIN; FLT3 LIGAND; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P14; PROTEIN P53; PROTEIN P85; PROTEIN SH3; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; TUMOR SUPPRESSOR PROTEIN;

ACUTE GRANULOCYTIC LEUKEMIA; APOPTOSIS; ARTICLE; BLAST CELL; CELL LYSATE; CELL PROLIFERATION; CELL SURVIVAL; COHORT ANALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SUBSTRATE; FEMALE; GENE LOCUS; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MALE; ONCOGENE; PRIORITY JOURNAL; PROTEIN TARGETING; SENSITIZATION; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; ENZYME ACTIVATION; FMS-LIKE TYROSINE KINASE 3; FUSION PROTEINS, BCR-ABL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, LEUKEMIC; HUMANS; LEUKEMIA, MYELOCYTIC, ACUTE; MITOGEN-ACTIVATED PROTEIN KINASE 8; MUTATION; PROTO-ONCOGENE PROTEINS C-CBL; QUANTITATIVE TRAIT LOCI; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P14ARF; TUMOR SUPPRESSOR PROTEIN P53;

EID: 33748543646     PISSN: 0301472X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exphem.2006.05.019     Document Type: Article

References (56)

1. Grimwade D., Walker H., Oliver F., et al. The importance of diagnostic cytogenetics on outcome in AML: analysis of 1612 patients entered into the MRC AML 10 trial. Blood 92 (1998) 2322-2333
2. Harris N.L., Jaffe E.S., Diebold J., et al. World Health Organization classification of neoplastic diseases of the hematopoietic and lymphoid tissues: report of the clinical advisory committee meeting- Airlie House, Virginia, November, 1997. J Clin Oncol 17 (1999) 3835-3849
3. Slovak M.L., Kopecky K.J., Cassileth P.A., et al. Karyotypic analysis predicts outcome of preremission and postremission therapy in adult acute myeloid leukemia: a Southwest Oncology Group/Eastern Cooperative Oncology Group Study. Blood 96 (2000) 4075-4083
4. Fenaux P., Chastang C., Chevret S., et al. A randomized comparison of all-trans retinoic acid (ATRA) followed by chemotherapy and ATRA plus chemotherapy and the role of maintenance therapy in newly diagnosed acute promyelocytic leukemia. The European APL group. Blood 94 (1999) 1192-1200
5. Giles FJ, Keating A, Goldstone AH, Avivi I, Willman CL, Kantarjian HM. Acute myeloid leukemia. Hematology 2002. American Society of Hematology education program book. Available at: http://www.asheducationbook.org/cgi/content/full/2002/1/73.
6. Leith C.P., Kopecky K.J., Godwin J., et al. Acute myeloid leukemia in the elderly: assessment of multidrug resistance (MDR1) and cytogenetics distinguishes biologic subgroups with remarkably distinct responses to standard chemotherapy. A Southwest Oncology Group study. Blood 89 (1997) 3323-3329
7. LeGrand O., Simonin G., Perrot J.Y., Zittoun R., and Marie J.P. Pgp and MRP activities using calcein AM are prognostic factors in adult acute myeloid leukemia patients. Blood 91 (1998) 4480-4488
8. Legrand O., Simonin G., Beauchamp-Nicoud A., Zittoun R., and Marie J.P. Simultaneous activity of MRP1 and Pgp is correlated with in vitro resistance to daunorubicin and with in vivo resistance in adult acute myeloid leukemia. Blood 94 (1999) 1046-1056
9. Leith C.P., Kopecky K.J., Chen I.M., et al. Frequency and clinical significance of the expression of the multidrug resistance proteins MDR1/p-glycoprotein, MRP1, and LRP in acute myeloid leukemia: a SWOG study. Blood 94 (1999) 1086-1099
10. Konopleva M., Tari A.M., Estrov Z., et al. Liposomal Bcl-2 antisense oligonucleotides enhance proliferation, sensitize acute myeloid leukemia to cytosine-arabinoside, and induce apoptosis independent of other antiapoptotic proteins. Blood 95 (2000) 3929-3938
11. Estrov Z., Thall P.F., Talpaz M., et al. Caspase 2 and caspase 3 protein levels as predictors of survival in acute myelogenous leukemia. Blood 92 (1998) 3090-3097
12. Kiyoi H., Naoe T., Nakano Y., et al. Prognostic implication of Flt3 and N-ras mutations in acute myeloid leukemia. Blood 93 (1999) 3074-3080
13. Kottaridis P.D., Gale R.E., Frew M.E., et al. The presence of a FLT3 internal tandem duplication in patients with acute myeloid leukemia (AML) add important prognostic information to cytogenetic risk group and response to the first cycle of chemotherapy: analysis of 854 patients from the United Kingdom Medical Research Council AML 10 and 12 trials. Blood 98 (2001) 1752-1759
14. Ozeki K., Kiyoi H., Hirose Y., et al. Biologic and clinical significance of the FLT3 transcript level in acute myeloid leukemia. Blood 103 (2004) 1901-1908
15. Cripe L.D., Gelfanov V.M., Smith E.A., et al. Role for c-jun N-terminal kinase in treatment-refractory acute myeloid leukemia (AML): signaling to multidrug-efflux and hyperproliferation. Leukemia 16 (2002) 799-812
16. Lavagna-Sevenier C., Marchetto S., Birnbaum D., and Rosnet O. Flt3 signaling in hematopoietic cells involves cbl, shc, and unknown p115 as prominent tyrosine phosphorylated substrates. Leukemia 12 (1998) 301-310
17. Odero M.D., Zeleznik-Le N., Chinwalla V., and Rowley J.D. Cytogenetic and molecular analysis of the acute monocytic leukemia cell line, THP-1, exhibiting t(9;11) (11q23) with MLL-AF9 translocation. Genes Chromosomes Cancer 29 (2000) 333-338
18. Kevin W.H., Yee A.M., O'Farrell B.D., Smolich J.M., et al. SU5416 and SU5614 inhibit kinase activity of wild-type and mutant FLT3 receptor tyrosine kinase. Blood 100 (2002) 2941-2949
19. Manning A.M., and Davis R.J. Targeting JNK for therapeutic benefit: from junk to gold?. Nat Rev Drug Discov 2 (2003) 554-565
20. 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
21. Abu-Dubier F.M., Goodeve A.C., Wilson A., et al. Identification of novel Flt3 Asp 835 mutations in adult acute myeloid leukemia. Br J Haematol 113 (2001) 983-988
22. Walters D.K., Stoffregen E.P., Heinrich M.C., Deininger M.W., and Druker B.J. RNAi-induced down-regulation of FLT3 expression in AML cell lines increases sensitivity to MLN518. Blood 105 (2005) 2952-2954
23. Burgess G.S., Williamson E.A., Cripe L.D., et al. Regulation of the c-jun gene in P210 BCR-ABL transformed cells corresponds with activity of JNK, the c-jun N-terminal kinase. Blood 92 (1998) 2450-2460
24. Armstrong S.A., Staunton J.E., Silverman L.B., et al. MLL translocations specify a distinct gene expression profile that distinguishes a unique leukemia. Nat Genet 30 (2002) 41-47
25. Zheng R., Levis M., Piloto O., et al. FLT3 ligand causes autocrine signaling in acute myeloid leukemia cells. Blood 103 (2004) 267-274
26. Girardin S.E., and Yaniv M. A direct interaction between JNK1 and CrkII is critical for Rac1-induced JNK activation. EMBO J 20 (2001) 3437-3446
27. Salameh A., Galvagni F., Bardelli M., Bussolino F., and Oliviero S. Direct recruitment of CRK and GRB2 to VEGFR-3 induces proliferation, migration, and survival of endothelial cells through the activation of ERK, AKT, and JNK pathways. Blood 106 (2005) 3423-3431
28. Morrison D.K., and Davis R.J. Regulation of MAP kinase signaling modules by scaffold proteins in mammals. Ann Rev Cell Dev Biol 19 (2003) 91-1118
29. Adler V., Yizi Z., Fuchs S.Y., et al. Regulation of JNK signaling by GSTp. EMBO J 18 (1999) 1321-1334
30. Berenbaum M.C. Criteria for analyzing interactions between biologically active agents. Adv Cancer Res 35 (1981) 269-332
31. Libura M., Asnafi V., Tu A., et al. FLT3 and MLL intragenic abnormalities in AML reflect a common category of genotoxic stress. Blood 102 (2003) 2198-2204
32. Morrow C.S., Goldsmith M.E., and Cowan K.H. Regulation of human glutathione-S-transferase gene transcription: influence of 5′ flanking sequences and trans activating factors which recognize AP-1 binding sites. Gene 88 (1990) 215-225
33. 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
34. Beitz L.O., Fruman D.A., Kurosaki T., Cantley L.C., and Scharenberg A.M. SYK is upstream of phosphoinositide 3-kinase in B cell receptor signaling. J Biol Chem 274 (1999) 32662-32666
35. Grossman A.H., Kolibaba K.S., Willis S.G., et al. Catalytic domains of tyrosine kinases determine the phosphorylation sites within c-Cbl. FEBS Lett 577 (2004) 555-562
36. Sattler M., and Salgia R. Role of the adapter protein CRKL in signal transduction of normal hematopoietic and BCR/ABL-transformed cells. Leukemia 12 (1998) 637-644
37. Gelkop S., Babichev Y., and Isakov N. T cell activation induces direct binding of the Crk adapter protein to the regulatory subunit of phosphatidylinositol 3-kinase (p85) via a complex mechanism involving the Cbl protein. J Biol Chem 276 (2001) 36174-36182
38. Scheijen B., Ngo H.T., Kang H., and Griffin J.D. FLT3 receptors with internal tandem duplications promote cell viability and proliferation by signaling through Foxo proteins. Oncogene 23 (2004) 3338-3349
39. Levis M., Allebach J., Tse K.F., et al. A FLT3-targeted tyrosine kinase inhibitor is cytotoxic to leukemia cells in vitro and in vivo. Blood 99 (2002) 3885-3891
40. Choudhary C., Schwable J., Brandts C., et al. AML-associated Flt3 kinase domain mutations show signal transduction differences in comparison to Flt3 ITD mutations. Blood 106 (2005) 265-273
41. Robinson L.J., Xue J., and Corey S.J. Src family tyrosine kinases are activated by Flt3 and are involved in the proliferative effects of leukemia-associated Flt3 mutations. Exp Hematol 33 (2005) 469-479
42. Kim K.T., Baird K., Ahn J.Y., et al. Pim-1 is up-regulated by constitutively activated FLT3 and plays a role in FLT3-mediated cell survival. Blood 105 (2005) 1759-1767
43. Raitano A.B., Halpern J.R., Hambruch T.M., and Sawyers C.L. The Bcr-Abl leukemia oncogene activates jun kinase and requires jun for transformation. Proc Natl Acad Sci U S A 92 (1995) 11746-11750
44. Smeal T., Binetruy B., Mercola D.A., Birrer M., and Karin M. Oncogenic and transcriptional cooperation with Ha-Ras requires phosphorylation of c-Jun on serines 63 and 73. Nature 354 (1991) 494-496
45. Eferl R., Ricci R., Kenner L., et al. Liver tumor development. c-Jun antagonizes the proapoptotic activity of p53. Cell 112 (2003) 181-192
46. Angel P., Hattori K., Smeal T., and Karin M. The c-jun protooncogene is positively autoregulated by its product, c-jun/AP-1. Cell 55 (1988) 875-885
47. Schreiber M., Kolbus A., Piu F., et al. Control of cell cycle progression by c-jun is p53-dependent. Genes Dev 13 (1999) 607-619
48. Shaulian E., Schreiber M., Piu F., Beecher M., Wagner E.F., and Karin M. The mammalian UV response: c-jun induction is required for exit from p53-imposed growth arrest. Cell 103 (2000) 897-907
49. Dickins R.A., Hemann M.T., Zilfou J.T., et al. Probing tumor phenotypes using stable and regulated synthetic microRNA precursors. Nat Genet 37 (2005) 1289-1295
50. Bulavin D.V., Kovalsky O., Hollander M.C., and Fornace Jr. A.J. Loss of oncogenic H-ras-induced cell cycle arrest and p38 mitogen-activated protein kinase activation by disruption of Gadd45a. Mol Cell Biol 23 (2003) 3859-3871
51. Bulavin D.V., Phillips C., Nannenga B., et al. Inactivation of the Wip1 phosphatase inhibits mammary tumorigenesis through p38 MAPK-mediated activation of the p16(Ink4a)-p19(Arf) pathway. Nat Genet 36 (2004) 343-350
52. Edlund S., Bu S., Schuster N., et al. Transforming growth factor-beta1 (TGF-beta)-induced apoptosis of prostate cancer cells involves Smad7-dependent activation of p38 by TGF-beta-activated kinase 1 and mitogen-activated protein kinase kinase 3. Mol Biol Cell 14 (2003) 529-544
53. Li Y., Sassano A., Majchrzak B., et al. Role of p38alpha map kinase in type I interferon signaling. J Biol Chem 279 (2004) 970-979
54. Parmar S., Katsoulidis E., Verma A., et al. Role of the p38 mitogen-activated protein kinase pathway in the generation of the effects of imatinib mesylate (STI571) in BCR-ABL-expressing cells. J Biol Chem 279 (2004) 25345-25352
55. Irish J.M., Hovland R., Krutzik P.O., et al. Single cell profiling of potentiated phospho-protein networks in cancer cells. Cell 118 (2004) 217-228
56. Hess P., Pihan G., Sawyers C.L., Flavell R.A., and Davis R.J. Survival signaling mediated by c-jun (NH2) terminal kinase in transformed B lymphoblasts. Nat Genet 32 (2002) 201-205