The Jak2V617F oncogene associated with myeloproliferative diseases requires a functional FERM domain for transformation and for expression of the Myc and Pim proto-oncogenes

Blood

Volumn 111, Issue 7, 2008, Pages 3751-3759

  Wernig, Gerlinde ^a   Gonneville, Jeffrey R ^b   Crowley, Brian J ^b   Rodrigues, Margret S ^a,b   Reddy, Mamatha M ^a,b   Hudon, Heidi E ^b   Walz, Christoph ^b   Reiter, Andreas ^c   Podar, Klaus ^a,b   Royer, Yohan ^d   Constantinescu, Stefan N ^d   Tomasson, Michael H ^e   Griffin, James D ^a,b   Gilliland, D Gary ^a   Sattler, Martin ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d LUDWIG INSTITUTE FOR CANCER RESEARCH   (Belgium)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CYCLIN D2; ERYTHROPOIETIN RECEPTOR; GROWTH FACTOR RECEPTOR; JANUS KINASE 2; MUTANT PROTEIN; MYC PROTEIN; PROTEIN KINASE PIM 1; PROTEIN P27; PROTEIN PIM2; REACTIVE OXYGEN METABOLITE; STAT5 PROTEIN; UNCLASSIFIED DRUG; ERYTHROPOIETIN; JAK2 PROTEIN, HUMAN; JAK2 PROTEIN, MOUSE; MYC PROTEIN, HUMAN; MYC PROTEIN, MOUSE; ONCOPROTEIN; PIM1 PROTEIN, HUMAN; PIM1 PROTEIN, MOUSE; PIM2 PROTEIN, HUMAN; PIM2 PROTEIN, MOUSE; PROTEIN SERINE THREONINE KINASE;

ANIMAL CELL; ARTICLE; CELL TRANSFORMATION; CONTROLLED STUDY; FETUS; GENE ACTIVATION; GENE EXPRESSION; HEMATOPOIESIS; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; JAK2V617F ONCOGENE; MOUSE; MYELOPROLIFERATIVE DISORDER; NONHUMAN; ONCOGENE; ONCOGENE MYC; PHENOTYPE; PIM PROTO ONCOGENE; POINT MUTATION; PRIORITY JOURNAL; RECEPTOR BINDING; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; ENZYME ACTIVATION; EXTRAMEDULLARY HEMATOPOIESIS; GENE EXPRESSION REGULATION; GENETIC TRANSDUCTION; GENETICS; LIVER; METABOLISM; MISSENSE MUTATION; PATHOLOGY; PRENATAL DEVELOPMENT; PROTEIN TERTIARY STRUCTURE; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; ENZYME ACTIVATION; ERYTHROPOIETIN; GENE EXPRESSION REGULATION, NEOPLASTIC; HEMATOPOIESIS, EXTRAMEDULLARY; HUMANS; JANUS KINASE 2; LIVER; MICE; MUTATION, MISSENSE; MYELOPROLIFERATIVE DISORDERS; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MYC; PROTO-ONCOGENE PROTEINS C-PIM-1; REACTIVE OXYGEN SPECIES; RECEPTORS, ERYTHROPOIETIN; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; TRANSDUCTION, GENETIC;

EID: 43549109620     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2007-07-102186     Document Type: Article

References (44)

1. Levine RL, Wadleigh M, Cools J, et al. Activating mutation in the tyrosine kinase JAK2 in polycythemia vera, essential thrombocythemia, and myeloid metaplasia with myelofibrosis. Cancer Cell. 2005;7:387-397.
2. James C, Ugo V, Le Couedic JP, et al. A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature. 2005;434:1144-1148.
3. Baxter EJ, Scott LM, Campbell PJ, et al. Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders. Lancet. 2005;365:1054-1061.
4. Kralovics R, Passamonti F, Buser AS, et al. A gain-of-function mutation of JAK2 in myeloproliferative disorders. N Engl J Med. 2005;352:1779-1790.
5. Zhao R, Xing S, Li Z, et al. Identification of an acquired JAK2 mutation in polycythemia vera. J Biol Chem. 2005;280:22788-22792.
6. Jones AV, Kreil S, Zoi K, et al. Widespread occurrence of the JAK2 V617F mutation in chronic myeloproliferative disorders. Blood. 2005;106:2162-2168.
7. Steensma DP, Dewald GW, Lasho TL, et al. The JAK2 V617F activating tyrosine kinase mutation is an infrequent event in both "atypical" myeloproliferative disorders and the myelodysplastic syndrome. Blood. 2005;106:1207-1209.
8. Mercher T, Wernig G, Moore SA, et al. JAK2T875N is a novel activating mutation that results in myeloproliferative disease with features of megakaryoblastic leukemia in a murine bone marrow transplantation model. Blood. 2006;108:2770-2779.
9. Peeters P, Raynaud SD, Cools J, et al. 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.
10. Lacronique V, Boureux A, Valle VD, et al. ATEL-JAK2 fusion protein with constitutive kinase activity in human leukemia. Science. 1997;278:1309-1312.
11. Reiter A, Walz C, Watmore A, et al.The t(8;9)(p22;p24) is a recurrent abnormality in chronic and acute leukemia that fuses PCM1 to JAK2. Cancer Res. 2005;65:2662-2667.
12. Griesinger F, Hennig H, Hillmer F, et al. ABCR-JAK2 fusion gene as the result of a t(9;22)(p24;q11.2) translocation in a patient with a clinically typical chronic myeloid leukemia. Genes Chromosomes Cancer. 2005;44:329-333.
13. Onishi M, NosakaT, MisawaK, et al. Identification and characterization of a constitutively active STAT5 mutant that promotes cell proliferation. Mol Cell Biol. 1998;18:3871-3879.
14. Teglund S, McKay C, Schuetz E, et al. Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell. 1998;93:841-850.
15. Socolovsky M, Fallon AE, Wang S, Brugnara C, Lodish HF. Fet al anemia and apoptosis of red cell progenitors in Stat5a-/-5b-/-mice: a direct role for Stat5 in Bcl-X(L) induction. Cell. 1999;98:181-191.
16. Mui AL, Wakao H, KinoshitaT, KitamuraT, Miyajima A. Suppression of interleukin-3-induced gene expression by a C-terminal truncated Stat5: role of Stat5 in proliferation. Embo J. 1996;15:2425-2433.
17. Joneja B, Wojchowski DM. Mitogenic signaling and inhibition of apoptosis via the erythropoietin receptor Box-1 domain. J Biol Chem. 1997;272:11176-11184.
18. Yamaoka K, Saharinen P, Pesu M, Holt VE III. Silvennoinen O, O'Shea JJ. The Janus kinases (Jaks). Genome Biol. 2004;5:253.1-253.6.
19. Royer Y, Staerk J, Costuleanu M, Courtoy PJ, Constantinescu SN. Janus kinases affect thrombopoietin receptor cell surface localization and stability. J Biol Chem. 2005;280:27251-27261.
20. Gesbert F, Griffin JD. Bcr/Abl activates transcription of the Bcl-X gene through STAT5. Blood. 2000;96:2269-2276.
21. Wernig G, Mercher T, Okabe R, Levine RL, Lee BH, Gilliland DG. Expression of Jak2V617F causes a polycythemia vera-like disease with associated myelofibrosis in a murine bone marrow transplant model. Blood. 2006;107:4274-4281.
22. Walz C, Crowley BJ, Hudon HE, et al. Activated Jak2 with the V617F point mutation promotes G1/S phase transition. J Biol Chem. 2006;281:18177-18183.
23. Lu X, Levine R, Tong W, et al. Expression of a homodimeric type I cytokine receptor is required for JAK2V617F-mediated transformation. Proc Natl Acad Sci USA. 2005;102:18962-18967.
24. Funakoshi-Tago M, Pelletier S, MatsudaT, Parganas E, Ihle JN. Receptor specific downregulation of cytokine signaling by autophosphorylation in the FERM domain of Jak2. Embo J. 2006;25:4763-4772.
25. Goerttler PS, Kreutz C, Donauer J, et al. Gene expression profiling in polycythaemia vera: over-expression of transcription factor NF-E2. Br J Haematol. 2005;129:138-150.
26. Guglielmelli P, Zini R, Bogani C, et al. Molecular profiling of CD34+ cells in idiopathic myelofibrosis identifies a set of disease-associated genes and reveals the clinical significance of Wilms' tumor gene 1 (WT1). Stem Cells. 2007;25:165-173.
27. Adam M, Pogacic V, Bendit M, et al. Targeting PIM kinases impairs survival of hematopoietic cells transformed by kinase inhibitor-sensitive and kinase inhibitor-resistant forms of Fms-like tyrosine kinase 3 and BCR/ABL. Cancer Res. 2006;66:3828-3835.
28. Littlewood TD, Hancock DC, Danielian PS, Parker MG, Evan GI. Amodified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res. 1995;23:1686-1690.
29. Spivak JL. Polycythemia vera: myths, mechanisms, and management. Blood. 2002;100:4272-4290.
30. Lindauer K, Loerting T, Liedl KR, Kroemer RT. Prediction of the structure of human Janus kinase 2 (JAK2) comprising the two carboxy-terminal domains reveals a mechanism for autoregulation. Protein Eng. 2001;14:27-37.
31. Huang LJ, Constantinescu SN, Lodish HF. The N-terminal domain of Janus kinase 2 is required for Golgi processing and cell surface expression of erythropoietin receptor. Mol Cell. 2001;8:1327-1338.
32. Staerk J, Kallin A, Demoulin JB, Vainchenker W, Constantinescu SN. JAK1 and Tyk2 activation by the homologous polycythemia vera JAK2 V617F mutation: cross-talk with IGF1 receptor. J Biol Chem. 2005;280:41893-41899.
33. Pelletier S, Gingras S, Funakoshi-Tago M, Howell S, Ihle JN. Two domains of the erythropoietin receptor are sufficient for Jak2 binding/activation and function. Mol Cell Biol. 2006;26:8527-8538.
34. Sattler M, Pride YB, Quinnan LR, et al. Differential expression and signaling of CBL and CBL-B in BCR/ABL transformed cells. Oncogene. 2002;21:1423-1433.
35. Harir N, Pecquet C, Kerenyi M, et al. Constitutive activation of Stat5 promotes its cytoplasmic localization and association with PI3-kinase in myeloid leukemias. Blood. 2007;109:1678-1686.
36. Kim JH, Chu SC, Gramlich JL, et al. Activation of the PI3K/mTOR pathway by BCR-ABL contributes to increased production of reactive oxygen species. Blood. 2005;105:1717-1723.
37. Nieborowska-Skorska M, Hoser G, Kossev P, Wasik MA, Skorski T. Complementary functions of the antiapoptotic protein A1 and serine/threonine kinase pim-1 in the BCR/ABL-mediated leukemogenesis. Blood. 2002;99:4531-4539.
38. Mikkers H, Nawijn M, Allen J, et al. Mice deficient for all PIM kinases display reduced body size and impaired responses to hematopoietic growth factors. Mol Cell Biol. 2004;24:6104-6115.
39. Breuer M, Slebos R, Verbeek S, van Lohuizen M, Wientjens E, Berns A. Very high frequency of lymphoma induction by a chemical carcinogen in pim-1 transgenic mice. Nature. 1989;340:61-63.
40. van Lohuizen M, Verbeek S, Krimpenfort P, et al. Predisposition to lymphomagenesis in pim-1 transgenic mice: cooperation with c-myc and N-myc in murine leukemia virus-induced tumors. Cell. 1989;56:673-682.
41. Nosaka T, Kawashima T, Misawa K, Ikuta K, Mui AL, Kitamura T. STAT5 as a molecular regulator of proliferation, differentiation and apoptosis in hematopoietic cells. Embo J. 1999;18:4754-4765.
42. Roh M, Gary B, Song C, et al. Overexpression of the oncogenic kinase Pim-1 leads to genomic instability. Cancer Res. 2003;63:8079-8084.
43. Fest T, Mougey V, Dalstein V, et al. c-MYC overexpression in Ba/F3 cells simultaneously elicits genomic instability and apoptosis. Oncogene. 2002;21:2981-2990.
44. Walz C, Sattler M. Novel targeted therapies to overcome imatinib mesylate resistance in chronic myeloid leukemia (CML). Crit Rev Oncol Hematol. 2006;57:145-164.