A role for reactive oxygen species in JAK2 V617F myeloproliferative neoplasm progression

Leukemia

Volumn 27, Issue 11, 2013, Pages 2187-2195

  Marty, C ^a,b   Lacout, C ^a,b   Droin, N ^a,b   Le Couedic J P ^a,b   Ribrag, V ^a,b   Solary, E ^a,b   Vainchenker, W ^a,b   Villeval, J L ^a,b   Plo, I ^a,b  

^a Universite Paris Sud   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

DNA damages; JAK2V617F; knock in mouse model; myeloproliferative neoplasms; N acetylcysteine; reactive oxygen species

Indexed keywords

ACETYLCYSTEINE; CATALASE; DOUBLE STRANDED DNA; GENOMIC DNA; HISTONE H2AX; JANUS KINASE 2; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; CANCER GROWTH; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; FLOW CYTOMETRY; GAIN OF FUNCTION MUTATION; HEMATOPOIETIC STEM CELL; HETEROZYGOSITY LOSS; HUMAN; HUMAN CELL; INTRACELLULAR SPACE; MITOTIC RECOMBINATION; MOLECULAR PATHOLOGY; MOUSE; MYELOID PROGENITOR CELL; MYELOPROLIFERATIVE NEOPLASM; NONHUMAN; OXIDATIVE STRESS; POLYCYTHEMIA VERA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPLENOMEGALY;

EID: 84887320216     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2013.102     Document Type: Article

References (41)

1. Baxter EJ, Scott LM, Campbell PJ, East C, Fourouclas N, Swanton S et al. Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders. Lancet 2005; 365: 1054-1061. (Pubitemid 40386783)
2. James C, Ugo V, Le Couedic JP, Staerk J, Delhommeau F, Lacout C et al. A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature 2005; 434: 1144-1148. (Pubitemid 40663494)
3. Kralovics R, Passamonti F, Buser AS, Teo SS, Tiedt R, Passweg JR et al. A gain-offunction mutation of JAK2 in myeloproliferative disorders. N Engl J Med 2005; 352: 1779-1790. (Pubitemid 40570926)
4. Levine RL, Wadleigh M, Cools J, Ebert BL, Wernig G, Huntly BJ 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. (Pubitemid 40544655)
5. 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: 1652-1660. (Pubitemid 44316134)
6. Marty C, Lacout C, Martin A, Hasan S, Jacquot S, Birling MC et al. Myeloproliferative neoplasm induced by constitutive expression of JAK2V617F in knock-in mice. Blood 2010; 116: 783-787.
7. Shide K, Shimoda HK, Kumano T, Karube K, Kameda T, Takenaka K et al. Development of ET, primary myelofibrosis and PV in mice expressing JAK2 V617F. Leukemia 2008; 22: 87-95.
8. Tiedt R, Coers J, Ziegler S, Wiestner A, Hao-Shen H, Bornmann C et al. Pronounced thrombocytosis in transgenic mice expressing reduced levels of Mpl in platelets and terminally differentiated megakaryocytes. Blood 2009; 113: 1768-1777.
9. 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. (Pubitemid 43801351)
10. Dupont S, Masse A, James C, Teyssandier I, Lecluse Y, Larbret F et al. The JAK2 617V4F mutation triggers erythropoietin hypersensitivity and terminal erythroid amplification in primary cells from patients with polycythemia vera. Blood 2007; 110: 1013-1021. (Pubitemid 47267441)
11. Godfrey AL, Chen E, Pagano F, Ortmann CA, Silber Y, Bellosillo B et al. JAK2V617F homozygosity arises commonly and recurrently in PV and ET, but PV is characterized by expansion of a dominant homozygous subclone. Blood 2012; 120: 2704-2707.
12. Tiedt R, Hao-Shen H, Sobas MA, Looser R, Dirnhofer S, Schwaller J et al. Ratio of mutant JAK2-V617F to wild-type Jak2 determines the MPD phenotypes in transgenic mice. Blood 2008; 111: 3931-3940.
13. Gelsi-Boyer V, Trouplin V, Adelaide J, Bonansea J, Cervera N, Carbuccia N et al. Mutations of polycomb-associated gene ASXL1 in myelodysplastic syndromes and chronic myelomonocytic leukaemia. Br J Haematol 2009; 145: 788-800.
14. Lasho TL, Jimma T, Finke CM, Patnaik M, Hanson CA, Ketterling RP et al. SRSF2 mutations in primary myelofibrosis: significant clustering with IDH mutations and independent association with inferior overall and leukemia-free survival. Blood 2012; 120: 4168-4171.
15. Shih AH, Abdel-Wahab O, Patel JP, Levine RL. The role of mutations in epigenetic regulators in myeloid malignancies. Nat Rev Cancer 2012; 12: 599-612.
16. Vainchenker W, Delhommeau F, Constantinescu SN, Bernard OA. New mutations and pathogenesis of myeloproliferative neoplasms. Blood 2011; 118: 1723-1735.
17. Koptyra M, Falinski R, Nowicki MO, Stoklosa T, Majsterek I, Nieborowska-Skorska M et al. BCR/ABL kinase induces self-mutagenesis via reactive oxygen species to encode imatinib resistance. Blood 2006; 108: 319-327. (Pubitemid 43990645)
18. Sallmyr A, Tomkinson AE, Rassool FV. Up-regulation of WRN and DNA ligase IIIalpha in chronic myeloid leukemia: consequences for the repair of DNA doublestrand breaks. Blood 2008; 112: 1413-1423.
19. Walz C, Crowley BJ, Hudon HE, Gramlich JL, Neuberg DS, Podar K et al. Activated Jak2 with the V617F point mutation promotes G1/S phase transition. J Biol Chem 2006; 281: 18177-18183. (Pubitemid 44035617)
20. Plo I, Nakatake M, Malivert L, de Villartay JP, Giraudier S, Villeval JL et al. JAK2 stimulates homologous recombination and genetic instability: potential implication in the heterogeneity of myeloproliferative disorders. Blood 2008; 112: 1402-1412.
21. Sallmyr A, Fan J, Rassool FV. Genomic instability in myeloid malignancies: increased reactive oxygen species (ROS), DNA double strand breaks (DSBs) and error-prone repair. Cancer Lett 2008; 270: 1-9.
22. Hasan S, Lacout C, Marty C, Cuingnet M, Solary E, Vainchenker W et al. JAK2V617F expression in mice amplifies hematopoietic stem cells and gives them a competitive advantage that is hampered by IFNa. Blood, submitted 2013.
23. Ito K, Hirao A, Arai F, Matsuoka S, Takubo K, Hamaguchi I et al. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 2004; 431: 997-1002. (Pubitemid 39434422)
24. Jang YY, Sharkis SJ. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood 2007; 110: 3056-3063. (Pubitemid 350006961)
25. Tefferi A, Vardiman JW. Classification and diagnosis of myeloproliferative neoplasms: the 2008 World Health Organization criteria and point-of-care diagnostic algorithms. Leukemia 2008; 22: 14-22.
26. Lukas J, Lukas C, Bartek J. More than just a focus: the chromatin response to DNA damage and its role in genome integrity maintenance. Nat Cell Biol 2011; 13: 1161-1169.
27. Barosi G, Bergamaschi G, Marchetti M, Vannucchi AM, Guglielmelli P, Antonioli E et al. JAK2 V617F mutational status predicts progression to large splenomegaly and leukemic transformation in primary myelofibrosis. Blood 2007; 110: 4030-4036. (Pubitemid 350248459)
28. Yalcin S, Marinkovic D, Mungamuri SK, Zhang X, Tong W, Sellers R et al. ROS-mediated amplification of AKT/mTOR signalling pathway leads to myeloproliferative syndrome in Foxo3(-/-) mice. EMBO J 2010; 29: 4118-4131.
29. Nieborowska-Skorska M, Kopinski PK, Ray R, Hoser G, Ngaba D, Flis S et al. Rac2-MRC-cIII-generated ROS cause genomic instability in chronic myeloid leukemia stem cells and primitive progenitors. Blood 2012; 119: 4253-4263.
30. Reddy MM, Fernandes MS, Salgia R, Levine RL, Griffin JD, Sattler M. NADPH oxidases regulate cell growth and migration in myeloid cells transformed by oncogenic tyrosine kinases. Leukemia 2011; 25: 281-289.
31. Nakatake M, Monte-Mor B, Debili N, Casadevall N, Ribrag V, Solary E et al. JAK2(V617F) negatively regulates p53 stabilization by enhancing MDM2 via La expression in myeloproliferative neoplasms. Oncogene 2012; 31: 1323-1333.
32. Zhao R, Follows GA, Beer PA, Scott LM, Huntly BJ, Green AR et al. Inhibition of the Bcl-xL deamidation pathway in myeloproliferative disorders. N Engl J Med 2008; 359: 2778-2789.
33. Cummings WJ, Yabuki M, Ordinario EC, Bednarski DW, Quay S, Maizels N. Chromatin structure regulates gene conversion. PLoS Biol 2007; 5: e246.
34. Dawson MA, Bannister AJ, Gottgens B, Foster SD, Bartke T, Green AR et al. JAK2 phosphorylates histone H3Y41 and excludes HP1alpha from chromatin. Nature 2009; 461: 819-822.
35. Tothova Z, Kollipara R, Huntly BJ, Lee BH, Castrillon DH, Cullen DE et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 2007; 128: 325-339. (Pubitemid 46137992)
36. Rhee SG. Cell signaling. H2O2, a necessary evil for cell signaling. Science 2006; 312: 1882-1883. (Pubitemid 43993698)
37. Tefferi A, Vaidya R, Caramazza D, Finke C, Lasho T, Pardanani A. Circulating interleukin (IL)-8, IL-2R, IL-12, and IL-15 levels are independently prognostic in primary myelofibrosis: a comprehensive cytokine profiling study. J Clin Oncol 2011; 29: 1356-1363.
38. Fleischman AG, Aichberger KJ, Luty SB, Bumm TG, Petersen CL, Doratotaj S et al. TNFalpha facilitates clonal expansion of JAK2V617F positive cells in myeloproliferative neoplasms. Blood 2011; 118: 6392-6398.
39. Pardanani A, Vannucchi AM, Passamonti F, Cervantes F, Barbui T, Tefferi A. JAK inhibitor therapy for myelofibrosis: critical assessment of value and limitations. Leukemia 2011; 25: 218-225.
40. Hole PS, Darley RL, Tonks A. Do reactive oxygen species play a role in myeloid leukemias? Blood 2011; 117: 5816-5826.
41. Naka K, Hoshii T, Muraguchi T, Tadokoro Y, Ooshio T, Kondo Y et al. TGF-beta-FOXO signalling maintains leukaemia-initiating cells in chronic myeloid leukaemia. Nature 2010; 463: 676-680.