A truncation mutant of Csf3r cooperates with PML-RARα to induce acute myeloid leukemia in mice

Experimental Hematology

Volumn 39, Issue 12, 2011, Pages 1136-1143

  Kunter, Ghada ^a   Woloszynek, Jill R ^a   Link, Daniel C ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE COLONY STIMULATING FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MUTANT PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW SUPPRESSION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; LEUKEMOGENESIS; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; NONSENSE MUTATION; ONCOGENE; ONCOGENE PML RAR ALPHA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSGENIC MOUSE;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; CODON, NONSENSE; CROSSES, GENETIC; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE KNOCK-IN TECHNIQUES; GENOTYPE; GRANULOCYTE COLONY-STIMULATING FACTOR; HUMANS; LEUKEMIA, MYELOID, ACUTE; MICE; MICE, INBRED C57BL; ONCOGENE PROTEINS, FUSION; PHENOTYPE; POLYETHYLENE GLYCOLS; RECEPTORS, GRANULOCYTE COLONY-STIMULATING FACTOR; STAT TRANSCRIPTION FACTORS;

MUS;

EID: 81155135073     PISSN: 0301472X     EISSN: 18732399     Source Type: Journal    
DOI: 10.1016/j.exphem.2011.08.013     Document Type: Article

References (37)

1. Donadieu J., Leblanc T., Bader Meunier B., et al. Analysis of risk factors for myelodysplasias, leukemias and death from infection among patients with congenital neutropenia. Experience of the French Severe Chronic Neutropenia Study Group. Haematologica 2005, 90:45-53.
2. Rosenberg P.S., Alter B.P., Bolyard A.A., et al. The incidence of leukemia and mortality from sepsis in patients with severe congenital neutropenia receiving long-term G-CSF therapy. Blood 2006, 107:4628-4635.
3. Dale D.C., Bonilla M.A., Davis M.W., et al. A randomized controlled phase III trial of recombinant human granulocyte colony-stimulating factor (filgrastim) for treatment of severe chronic neutropenia. Blood 1993, 81:2496-2502.
4. Germeshausen M., Ballmaier M., Welte K. Incidence of CSF3R mutations in severe congenital neutropenia and relevance for leukemogenesis: results of a long-term survey. Blood 2007, 109:93-99.
5. Dong F., Brynes R.K., Tidow N., Welte K., Lowenberg B., Touw I.P. Mutations in the gene for the granulocyte colony-stimulating-factor receptor in patients with acute myeloid leukemia preceded by severe congenital neutropenia [see comments]. N Engl J Med 1995, 333:487-493.
6. Hermans M.H., Ward A.C., Antonissen C., Karis A., Lowenberg B., Touw I.P. Perturbed granulopoiesis in mice with a targeted mutation in the granulocyte colony-stimulating factor receptor gene associated with severe chronic neutropenia. Blood 1998, 92:32-39.
7. McLemore M.L., Poursine-Laurent J., Link D.C. Increased granulocyte colony-stimulating factor responsiveness but normal resting granulopoiesis in mice carrying a targeted granulocyte colony-stimulating factor receptor mutation derived from a patient with severe congenital neutropenia. J Clin Invest 1998, 102:483-492.
8. Liu F., Kunter G., Krem M.M., et al. Csf3r mutations in mice confer a strong clonal HSC advantage via activation of Stat5. J Clin Invest 2008, 118:946-955.
9. Hermans M.H., Antonissen C., Ward A.C., Mayen A.E., Ploemacher R.E., Touw I.P. Sustained receptor activation and hyperproliferation in response to granulocyte colony-stimulating factor (G-CSF) in mice with a severe congenital neutropenia/acute myeloid leukemia-derived mutation in the G-CSF receptor gene. J Exp Med 1999, 189:683-692.
10. McLemore M.L., Grewal S., Liu F., et al. STAT-3 activation is required for normal G-CSF-dependent proliferation and granulocytic differentiation. Immunity 2001, 14:193-204.
11. Sexl V., Piekorz R., Moriggl R., et al. Stat5a/b contribute to interleukin 7-induced B-cell precursor expansion, but abl- and bcr/abl-induced transformation are independent of stat5. Blood 2000, 96:2277-2283.
12. Akada H., Yan D., Zou H., Fiering S., Hutchison R.E., Mohi M.G. Conditional expression of heterozygous or homozygous Jak2V617F from its endogenous promoter induces a polycythemia vera-like disease. Blood 2010, 115:3589-3597.
13. Hayakawa F., Towatari M., Kiyoi H., et al. 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.
14. 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 2000, 96:3907-3914.
15. Schepers H., van Gosliga D., Wierenga A.T., Eggen B.J., Schuringa J.J., Vellenga E. STAT5 is required for long-term maintenance of normal and leukemic human stem/progenitor cells. Blood 2007, 110:2880-2888.
16. Kato Y., Iwama A., Tadokoro Y., et al. Selective activation of STAT5 unveils its role in stem cell self-renewal in normal and leukemic hematopoiesis. J Exp Med 2005, 202:169-179.
17. Schwaller J., Parganas E., Wang D., et al. Stat5 is essential for the myelo- and lymphoproliferative disease induced by TEL/JAK2. Mol Cell 2000, 6:693.
18. Moriggl R., Sexl V., Kenner L., et al. Stat5 tetramer formation is associated with leukemogenesis. Cancer Cell 2005, 7:87-99.
19. Link D.C., Kunter G., Kasai Y., et al. Distinct patterns of mutations occurring in de novo AML versus AML arising in the setting of severe congenital neutropenia. Blood 2007, 110:1648-1655.
20. Freedman M.H., Bonilla M.A., Fier C., et al. Myelodysplasia syndrome and acute myeloid leukemia in patients with congenital neutropenia receiving G-CSF therapy. Blood 2000, 96:429-436.
21. Chan I.T., Kutok J.L., Williams I.R., et al. Oncogenic K-ras cooperates with PML-RAR alpha to induce an acute promyelocytic leukemia-like disease. Blood 2006, 108:1708-1715.
22. Kelly L.M., Kutok J.L., Williams I.R., et al. PML/RARalpha and FLT3-ITD induce an APL-like disease in a mouse model. Proc Natl Acad Sci 2002, 99:8283.
23. Westervelt P., Lane A.A., Pollock J.L., et al. High-penetrance mouse model of acute promyelocytic leukemia with very low levels of PML-RARalpha expression. Blood 2003, 102:1857-1865.
24. Benekli M., Xia Z., Donohue K.A., et al. Constitutive activity of signal transducer and activator of transcription 3 protein in acute myeloid leukemia blasts is associated with short disease-free survival. Blood 2002, 99:252-257.
25. Irish J.M., Hovland R., Krutzik P.O., et al. Single cell profiling of potentiated phospho-protein networks in cancer cells. Cell 2004, 118:217-228.
26. Redell M.S., Ruiz M.J., Alonzo T.A., Gerbing R.B., Tweardy D.J. Stat3 signaling in acute myeloid leukemia: ligand-dependent and -independent activation and induction of apoptosis by a novel small-molecule Stat3 inhibitor. Blood 2011, 117:5701-5709.
27. Gits J., van Leeuwen D., Carroll H.P., Touw I.P., Ward A.C. Multiple pathways contribute to the hyperproliferative responses from truncated granulocyte colony-stimulating factor receptors. Leukemia 2006, 20:2111-2118.
28. Ancliff P.J., Gale R.E., Liesner R., Hann I., Linch D.C. Long-term follow-up of granulocyte colony-stimulating factor receptor mutations in patients with severe congenital neutropenia: implications for leukaemogenesis and therapy. Br J Haematol 2003, 120:685-690.
29. Germeshausen M., Welte K., Ballmaier M. In vivo expansion of cells expressing acquired CSF3R mutations in patients with severe congenital neutropenia. Blood 2009, 113:668-670.
30. Xiang Z., Kreisel F., Cain J., Colson A., Tomasson M.H. Neoplasia driven by mutant c-KIT is mediated by intracellular, not plasma membrane, receptor signaling. Mol Cell Biol 2007, 27:267-282.
31. van de Geijn G.J., Gits J., Aarts L.H., Heijmans-Antonissen C., Touw I.P. G-CSF receptor truncations found in SCN/AML relieve SOCS3-controlled inhibition of STAT5 but leave suppression of STAT3 intact. Blood 2004, 104:667-674.
32. Hermans M.H., Antonissen C., Ward A.C., Mayen A.E., Ploemacher R.E., Touw I.P. Sustained receptor activation and hyperproliferation in response to granulocyte colony-stimulating factor (G-CSF) in mice with a severe congenital neutropenia/acute myeloid leukemia-derived mutation in the G-CSF receptor gene. J Exp Med 1999, 189:683-692.
33. Spiekermann K., Pau M., Schwab R., Schmieja K., Franzrahe S., Hiddemann W. Constitutive activation of STAT3 and STAT5 is induced by leukemic fusion proteins with protein tyrosine kinase activity and is sufficient for transformation of hematopoietic precursor cells. Exp Hematol 2002, 30:262-271.
34. Steensma D.P., McClure R.F., Karp J.E., et al. JAK2 V617F is a rare finding in de novo acute myeloid leukemia, but STAT3 activation is common and remains unexplained. Leukemia 2006, 20:971-978.
35. Xia Z., Baer M.R., Block A.W., Baumann H., Wetzler M. Expression of signal transducers and activators of transcription proteins in acute myeloid leukemia blasts. Cancer Res 1998, 58:3173-3180.
36. Zhu Q.S., Xia L., Mills G.B., Lowell C.A., Touw I.P., Corey S.J. G-CSF induced reactive oxygen species involves Lyn-PI3-kinase-Akt and contributes to myeloid cell growth. Blood 2006, 107:1847-1856.
37. Mills K.D., Ferguson D.O., Alt F.W. The role of DNA breaks in genomic instability and tumorigenesis. Immunol Rev 2003, 194:77-95.