JAK2V617F+ myeloproliferative neoplasm clones evoke paracrine DNA damage to adjacent normal cells through secretion of lipocalin-2

Blood

Volumn 124, Issue 19, 2014, Pages 2996-3006

  Kagoya, Yuki ^a   Yoshimi, Akihide ^a   Tsuruta Kishino, Takako ^a   Arai, Shunya ^a   Satoh, Takashi ^b,c   Akira, Shizuo ^b,c   Kurokawa, Mineo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b Immunology Frontier Research Center   (Japan)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

IRON; JANUS KINASE 2; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PROTEIN P53; REACTIVE OXYGEN METABOLITE; SHORT HAIRPIN RNA; ACUTE PHASE PROTEIN; JAK2 PROTEIN, MOUSE; LCN2 PROTEIN, MOUSE; LIPOCALIN; ONCOPROTEIN; PYRAZOLE DERIVATIVE; RUXOLITINIB;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CLONE; CONTROLLED STUDY; DNA DAMAGE; FEMALE; GROWTH INHIBITION; HEMATOPOIETIC CELL; IRON OVERLOAD; MOUSE; MYELOPROLIFERATIVE NEOPLASM; NONHUMAN; NUCLEOTIDE SEQUENCE; PARACRINE DNA DAMAGE; PARACRINE SIGNALING; PATHOGENESIS; PROTEIN SECRETION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL TRANSFORMATION; DRUG EFFECTS; GENETICS; HEMATOPOIESIS; KNOCKOUT MOUSE; METABOLISM; MYELOPROLIFERATIVE DISORDER; OXIDATIVE STRESS; PHYSIOLOGY; SECRETION (PROCESS);

ACUTE-PHASE PROTEINS; ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; DNA DAMAGE; FEMALE; HEMATOPOIESIS; IRON OVERLOAD; JANUS KINASE 2; LIPOCALINS; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOPROLIFERATIVE DISORDERS; ONCOGENE PROTEINS; OXIDATIVE STRESS; PARACRINE COMMUNICATION; PYRAZOLES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84909594302     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-04-570572     Document Type: Article

References (56)

1. Baxter EJ, Scott LM, Campbell PJ, et al; Cancer Genome Project. Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders. Lancet. 2005;365(9464):1054-1061.
2. James C, Ugo V, Le Couédic JP, et al. A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature. 2005;434(7037):1144-1148.
3. Jones AV, Kreil S, Zoi K, et al. Widespread occurrence of the JAK2 V617F mutation in chronic myeloproliferative disorders. Blood. 2005;106(6):2162-2168.
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(17):1779-1790.
5. 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(4):387-397.
6. Najean Y, Rain JD. The very long-term evolution of polycythemia vera: an analysis of 318 patients initially treated by phlebotomy or 32P between 1969 and 1981. Semin Hematol. 1997;34(1):6-16.
7. Abdel-Wahab O, Manshouri T, Patel J, et al. Genetic analysis of transforming events that convert chronic myeloproliferative neoplasms to leukemias. Cancer Res. 2010;70(2):447-452.
8. Wolanskyj AP, Schwager SM, McClure RF, Larson DR, Tefferi A. Essential thrombocythemia beyond the first decade: life expectancy, longterm complication rates, and prognostic factors. Mayo Clin Proc. 2006;81(2):159-166.
9. Gaidano G, Guerrasio A, Serra A, Rege-Cambrin G, Saglio G. Molecular mechanisms of tumor progression in chronic myeloproliferative disorders. Leukemia. 1994;8(Suppl 1): S27-S29.
10. Mesa RA, Li CY, Ketterling RP, Schroeder GS, Knudson RA, Tefferi A. Leukemic transformation in myelofibrosis with myeloid metaplasia: a singleinstitution experience with 91 cases. Blood. 2005;105(3):973-977.
11. Bumm TG, Elsea C, Corbin AS, et al. Characterization of murine JAK2V617F-positive myeloproliferative disease. Cancer Res. 2006;66(23):11156-11165.
12. Lacout C, Pisani DF, Tulliez M, Gachelin FM, Vainchenker W, Villeval JL. JAK2V617F expression in murine hematopoietic cells leads to MPD mimicking human PV with secondary myelofibrosis. Blood. 2006;108(5):1652-1660.
13. 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(11):4274-4281.
14. Shide K, Shimoda HK, Kumano T, et al. Development of ET, primary myelofibrosis and PV in mice expressing JAK2 V617F. Leukemia. 2008;22(1):87-95.
15. Xing S, Wanting TH, Zhao W, et al. Transgenic expression of JAK2V617F causes myeloproliferative disorders in mice. Blood. 2008;111(10):5109-5117.
16. Mullally A, Lane SW, Ball B, et al. Physiological Jak2V617F expression causes a lethal myeloproliferative neoplasm with differential effects on hematopoietic stem and progenitor cells. Cancer Cell. 2010;17(6):584-596.
17. Marty C, Lacout C, Martin A, et al. Myeloproliferative neoplasm induced by constitutive expression of JAK2V617F in knock-in mice. Blood. 2010;116(5):783-787.
18. Akada H, Yan D, Zou H, Fiering S, Hutchison RE, Mohi MG. Conditional expression of heterozygous or homozygous Jak2V617F from its endogenous promoter induces a polycythemia vera-like disease. Blood. 2010;115(17):3589-3597.
19. Lundberg P, Karow A, Nienhold R, et al. Clonal evolution and clinical correlates of somatic mutations in myeloproliferative neoplasms. Blood. 2014;123(14):2220-2228.
20. Klampfil T, Harutyunyan A, Berg T, et al. Genome integrity of myeloproliferative neoplasms in chronic phase and during disease progression. Blood. 2011;118(1):167-176.
21. Abdel-Wahab O, Pardanani A, Rampal R, Lasho TL, Levine RL, Tefferi A. DNMT3A mutational analysis in primary myelofibrosis, chronic myelomonocytic leukemia and advanced phases of myeloproliferative neoplasms. Leukemia. 2011;25(7):1219-1220.
22. Ding Y, Harada Y, Imagawa J, Kimura A, Harada H. AML1/RUNX1 point mutation possibly promotes leukemic transformation in myeloproliferative neoplasms. Blood. 2009;114(25):5201-5205.
23. Taketani T, Taki T, Takita J, et al. Mutation of the AML1/RUNX1 gene in a transient myeloproliferative disorder patient with Down syndrome. Leukemia. 2002;16(9):1866-1867.
24. Pardanani A, Lasho TL, Finke CM, Mai M, McClure RF, Tefferi A. IDH1 and IDH2 mutation analysis in chronic- and blast-phase myeloproliferative neoplasms. Leukemia. 2010;24(6):1146-1151.
25. Harutyunyan A, Klampfil T, Cazzola M, Kralovics R. p53 lesions in leukemic transformation. N Engl J Med. 2011;364(5):488-490.
26. Sterkers Y, Preudhomme C, Läi JL, et al. Acute myeloid leukemia and myelodysplastic syndromes following essential thrombocythemia treated with hydroxyurea: high proportion of cases with 17p deletion. Blood. 1998;91(2):616-622.
27. Burkitt MJ, Raafat A. Nitric oxide generation from hydroxyurea: significance and implications for leukemogenesis in the management of myeloproliferative disorders. Blood. 2006;107(6):2219-2222.
28. Campbell PJ, Baxter EJ, Beer PA, et al. Mutation of JAK2 in the myeloproliferative disorders: timing, clonality studies, cytogenetic associations, and role in leukemic transformation. Blood. 2006;108(10):3548-3555.
29. Theocharides A, Boissinot M, Girodon F, et al. Leukemic blasts in transformed JAK2-V617F-positive myeloproliferative disorders are frequently negative for the JAK2-V617F mutation. Blood. 2007;110(1):375-379.
30. Beer PA, Delhommeau F, LeCouédic JP, et al. Two routes to leukemic transformation after JAK2 mutation-positive myeloproliferative neoplasm. Blood. 2010;115(14):2891-2900.
31. Plo I, Nakatake M, Malivert L, et al. JAK2 stimulates homologous recombination and genetic instability: potential implication in the heterogeneity of myeloproliferative disorders. Blood. 2008;112(4):1402-1412.
32. Tsukada T, Tomooka Y, Takai S, et al. Enhanced proliferative potential in culture of cells from p53-deficient mice. Oncogene. 1993;8(12):3313-3322.
33. Flo TH, Smith KD, Sato S, et al. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature. 2004;432(7019):917-921.
34. Bersenev A, Wu C, Balcerek J, Tong W. Lnk controls mouse hematopoietic stem cell self-renewal and quiescence through direct interactions with JAK2. J Clin Invest. 2008;118(8):2832-2844.
35. Kagoya Y, Yoshimi A, Kataoka K, et al. Positive feedback between NF-kB and TNF-a promotes leukemia-initiating cell capacity. J Clin Invest. 2014;124(2):528-542.
36. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C (T) method. Nat Protoc. 2008;3(6):1101-1108.
37. Sheng Z, Wang SZ, Green MR. Transcription and signalling pathways involved in BCR-ABL-mediated misregulation of 24p3 and 24p3R. EMBO J. 2009;28(7):866-876.
38. 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(52):18962-18967.
39. Devireddy LR, Gazin C, Zhu X, Green MR. A cellsurface receptor for lipocalin 24p3 selectively mediates apoptosis and iron uptake. Cell. 2005;123(7):1293-1305.
40. Iannetti A, Pacifico F, Acquaviva R, et al. The neutrophil gelatinase-associated lipocalin (NGAL), a NF-kappaB-regulated gene, is a survival factor for thyroid neoplastic cells. Proc Natl Acad Sci USA. 2008;105(37):14058-14063.
41. McCord JM. Iron, free radicals, and oxidative injury. J Nutr. 2004;134(11):3171S-3172S.
42. Nakatake M, Monte-Mor B, Debili N, et al. JAK2 (V617F) negatively regulates p53 stabilization by enhancing MDM2 via La expression in myeloproliferative neoplasms. Oncogene. 2012;31(10):1323-1333.
43. Couronné L, Lippert E, Andrieux J, et al. Analyses of TET2 mutations in post-myeloproliferative neoplasm acute myeloid leukemias. Leukemia. 2010;24(1):201-203.
44. Schaub FX, Looser R, Li S, et al. Clonal analysis of TET2 and JAK2 mutations suggests that TET2 can be a late event in the progression of myeloproliferative neoplasms. Blood. 2010;115(10):2003-2007.
45. Ghoti H, Fibach E, Merkel D, Perez-Avraham G, Grisariu S, Rachmilewitz EA. Changes in parameters of oxidative stress and free iron biomarkers during treatment with deferasirox in iron-overloaded patients with myelodysplastic syndromes. Haematologica. 2010;95(8):1433-1434.
46. Law IK, Xu A, Lam KS, et al. Lipocalin-2 deficiency attenuates insulin resistance associated with aging and obesity. Diabetes. 2010;59(4):872-882.
47. Jang E, Kim JH, Lee S, et al. Phenotypic polarization of activated astrocytes: the critical role of lipocalin-2 in the classical inflammatory activation of astrocytes. J Immunol. 2013;191(10):5204-5219.
48. Klampfil T, Gisslinger H, Harutyunyan AS, et al. Somatic mutations of calreticulin in myeloproliferative neoplasms. N Engl J Med. 2013;369(25):2379-2390.
49. Beer PA, Ortmann CA, Campbell PJ, Green AR. Independently acquired biallelic JAK2 mutations are present in a minority of patients with essential thrombocythemia. Blood. 2010;116(6):1013-1014.
50. Haferlach C, Dicker F, Herholz H, Schnittger S, Kern W, Haferlach T. Mutations of the TP53 gene in acute myeloid leukemia are strongly associated with a complex aberrant karyotype. Leukemia. 2008;22(8):1539-1541.
51. Mohrin M, Bourke E, Alexander D, et al. Hematopoietic stem cell quiescence promotes error-prone DNA repair and mutagenesis. Cell Stem Cell. 2010;7(2):174-185.
52. Lin H, Monaco G, Sun T, et al. Bcr-Abl-mediated suppression of normal hematopoiesis in leukemia. Oncogene. 2005;24(20):3246-3256.
53. Leng X, Lin H, Ding T, et al. Lipocalin 2 is required for BCR-ABL-induced tumorigenesis. Oncogene. 2008;27(47):6110-6119.
54. Li J, Spensberger D, Ahn JS, et al. JAK2 V617F impairs hematopoietic stem cell function in a conditional knock-in mouse model of JAK2 V617F-positive essential thrombocythemia. Blood. 2010;116(9):1528-1538.
55. Lee HJ, Daver N, Kantarjian HM, Verstovsek S, Ravandi F. The role of JAK pathway dysregulation in the pathogenesis and treatment of acute myeloid leukemia. Clin Cancer Res. 2013;19(2):327-335.
56. Vainchenker W, Constantinescu SN. JAK/STAT signaling in hematological malignancies. Oncogene. 2013;32(21):2601-2613.