JAK2V617F expression in mice amplifies early hematopoietic cells and gives them a competitive advantage that is hampered by IFNa

Blood

Volumn 122, Issue 8, 2013, Pages 1464-1477

  Hasan, Salma ^a,b,c   Lacout, Catherine ^a,b,c   Marty, Caroline ^a,b,c   Cuingnet, Marie ^a,b,c   Solary, Eric ^a,b,c   Vainchenker, William ^a,b,c   Villeval, Jean Luc ^a,b,c  

^a INSERM   (France)

^b Universite Paris Sud   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CRE RECOMBINASE; HEMOGLOBIN; JANUS KINASE 2; MESSENGER RNA; STEM CELL ANTIGEN 1;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; ERYTHROBLAST; HEMATOCRIT; HEMATOPOIESIS; HEMATOPOIETIC CELL; HEMOGLOBIN BLOOD LEVEL; LEUKOCYTE COUNT; MOUSE; MYELOFIBROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETICULOCYTE COUNT; THROMBOCYTE COUNT; UPREGULATION; ANIMAL; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; C57BL MOUSE; CELL CYCLE; CROSS BREEDING; CYTOLOGY; DISEASE MODEL; GENETICS; HEMATOPOIETIC STEM CELL; HUMAN; LYMPHOCYTE; METABOLISM; MUTATION; MYELOID METAPLASIA; MYELOPROLIFERATIVE DISORDER; PHENOTYPE; POLYCYTHEMIA VERA; STEM CELL; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; CELL CYCLE; CROSSES, GENETIC; DISEASE MODELS, ANIMAL; HEMATOPOIETIC STEM CELLS; HUMANS; INTERFERON-ALPHA; JANUS KINASE 2; LYMPHOCYTES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; MYELOPROLIFERATIVE DISORDERS; PHENOTYPE; POLYCYTHEMIA VERA; PRIMARY MYELOFIBROSIS; STEM CELLS;

EID: 84886850069     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-04-498956     Document Type: Article

References (50)

1. 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.
2. 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.
3. 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.
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. 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.
6. 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.
7. Zaleskas VM, Krause DS, Lazarides K, et al. Molecular pathogenesis and therapy of polycythemia induced in mice by JAK2 V617F. PLoS One. 2006;1e18.
8. Tiedt R, Hao-Shen H, Sobas MA, Looser R, Dirnhofer S, Schwaller J, Skoda RC. Ratio of mutant JAK2-V617F to wild-type Jak2 determines the MPD phenotypes in transgenic mice. Blood. 2008;111(8):3931-3940.
9. 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.
10. 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.
11. 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.
12. 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.
13. Vainchenker W, Delhommeau F, Constantinescu SN, Bernard OA. New mutations and pathogenesis of myeloproliferative neoplasms. Blood. 2011;118(7):1723-1735.
14. Quivoron C, Couronné L, Della Valle V, et al. TET2 inactivation results in pleiotropic hematopoietic abnormalities in mouse and is a recurrent event during human lymphomagenesis. Cancer Cell. 2011;20(1):25-38.
15. Moran-Crusio K, Reavie L, Shih A, et al. Tet2 loss leads to increased hematopoietic stem cell selfrenewal and myeloid transformation. Cancer Cell. 2011;20(1):11-24.
16. Challen GA, Sun D, Jeong M, et al. Dnmt3a is essential for hematopoietic stem cell differentiation. Nat Genet. 2012;44(1):23-31.
17. Skoda RC. JAK2 impairs stem cell function?. Blood. 2010;116(9):1392-1393.
18. Dupont S, Massé A, James C, et al. The JAK2 617V.F mutation triggers erythropoietin hypersensitivity and terminal erythroid amplification in primary cells from patients with polycythemia vera. Blood. 2007;110(3): 1013-1021.
19. Delhommeau F, Dupont S, Della Valle V, et al. Mutation in TET2 in myeloid cancers. N Engl J Med. 2009;360(22):2289-2301.
20. Sato T, Onai N, Yoshihara H, Arai F, Suda T, Ohteki T. Interferon regulatory factor-2 protects quiescent hematopoietic stem cells from type I interferon-dependent exhaustion. Nat Med. 2009; 15(6):696-700.
21. Essers MA, Offner S, Blanco-Bose WE, et al. IFNalpha activates dormant haematopoietic stem cells in vivo. Nature. 2009;458(7240):904-908.
22. Kiladjian JJ, Mesa RA, Hoffman R. The renaissance of interferon therapy for the treatment of myeloid malignancies. Blood. 2011; 117(18):4706-4715.
23. Croker BA, Metcalf D, Robb L, et al. SOCS3 is a critical physiological negative regulator of G-CSF signaling and emergency granulopoiesis. Immunity. 2004;20(2):153-165.
24. Georgiades P, Ogilvy S, Duval H, Licence DR, Charnock-Jones DS, Smith SK, Print CG. VavCre transgenic mice: A tool for mutagenesis in hematopoietic and endothelial lineages. Genesis. 2002;34(4):251-256.
25. Schnütgen F, Ghyselinck NB. Adopting the good reFLEXes when generating conditional alterations in the mouse genome. Transgenic Res. 2007; 16(4):405-413.
26. Ogilvy S, Elefanty AG, Visvader J, Bath ML, Harris AW, Adams JM. Transcriptional regulation of vav, a gene expressed throughout the hematopoietic compartment. Blood. 1998;91(2): 419-430.
27. Almarza E, Segovia JC, Guenechea G, Gómez SG, Ramírez A, Bueren JA. Regulatory elements of the vav gene drive transgene expression in hematopoietic stem cells from adult mice. Exp Hematol. 2004;32(4):360-364.
28. Villeval JL, Cohen-Solal K, Tulliez M, et al. High thrombopoietin production by hematopoietic cells induces a fatal myeloproliferative syndrome in mice. Blood. 1997;90(11):4369-4383.
29. Kiel MJ, Yilmaz OH, Iwashita T, Yilmaz OH, Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 2005;121(7):1109-1121.
30. Kiladjian JJ, Cassinat B, Chevret S, et al. Pegylated interferon-alfa-2a induces complete hematologic and molecular responses with low toxicity in polycythemia vera. Blood. 2008;112(8): 3065-3072.
31. de Bruin AM, Demirel O, Hooibrink B, Brandts CH, Nolte MA. Interferon-g impairs proliferation of hematopoietic stem cells in mice. Blood. 2013; 121(18):3578-3585.
32. Ogilvy S, Metcalf D, Gibson L, Bath ML, Harris AW, Adams JM. Promoter elements of vav drive transgene expression in vivo throughout the hematopoietic compartment. Blood. 1999;94(6): 1855-1863.
33. Anand S, Stedham F, Beer P, et al. Effects of the JAK2 mutation on the hematopoietic stem and progenitor compartment in human myeloproliferative neoplasms. Blood. 2011; 118(1):177-181.
34. Yan D, Hutchison RE, Mohi G. Critical requirement for Stat5 in a mouse model of polycythemia vera. Blood. 2012;119(15): 3539-3549.
35. Mullally A, Poveromo L, Schneider RK, Al-Shahrour F, Lane SW, Ebert BL. Distinct roles for long-term hematopoietic stem cells and erythroid precursor cells in a murine model of Jak2V617F-mediated polycythemia vera. Blood. 2012;120(1):166-172.
36. Catlin SN, Guttorp P, Abkowitz JL. The kinetics of clonal dominance in myeloproliferative disorders. Blood. 2005;106(8):2688-2692.
37. Solar GP, Kerr WG, Zeigler FC, et al. Role of c-mpl in early hematopoiesis. Blood. 1998;92(1):4-10.
38. Qian H, Buza-Vidas N, Hyland CD, et al. Critical role of thrombopoietin in maintaining adult quiescent hematopoietic stem cells. Cell Stem Cell. 2007;1(6):671-684.
39. Richards MK, Liu F, Iwasaki H, Akashi K, Link DC. Pivotal role of granulocyte colony-stimulating factor in the development of progenitors in the common myeloid pathway. Blood. 2003;102(10): 3562-3568.
40. Muller-Sieburg CE, Sieburg HB. The GOD of hematopoietic stem cells: A clonal diversity model of the stem cell compartment. Cell Cycle. 2006; 5(4):394-398.
41. Mullally A, Bruedigam C, Poveromo L, et al. Depletion of Jak2V617F MPN-propagating stem cells by interferon-alpha in a murine model of polycythemia vera. Blood. 2013;121(18): 3692-3702.
42. James C, Mazurier F, Dupont S, et al. The hematopoietic stem cell compartment of JAK2V617F-positive myeloproliferative disorders is a reflection of disease heterogeneity. Blood. 2008;112(6):2429-2438.
43. Tefferi A. JAK inhibitors for myeloproliferative neoplasms: Clarifying facts from myths. Blood. 2012;119(12):2721-2730.
44. Shide K, Kameda T, Markovtsov V, et al. R723, a selective JAK2 inhibitor, effectively treats JAK2V617F-induced murine myeloproliferative neoplasm. Blood. 2011;117(25):6866-6875.
45. Lin Q, Dong C, Cooper MD. Impairment of T and B cell development by treatment with a type I interferon. J Exp Med. 1998;187(1): 79-87.
46. Rosenthal GJ, Stranahan RP III, Thompson M, et al. Organ-specific hematopoietic changes induced by a recombinant human interferon-alpha in mice. Fundam Appl Toxicol. 1990;14(4): 666-675.
47. Yamane A, Nakamura T, Suzuki H, et al. Interferon-alpha 2b-induced thrombocytopenia is caused by inhibition of platelet production but not proliferation and endomitosis in human megakaryocytes. Blood. 2008;112(3):542-550.
48. Rizza P, Moretti F, Belardelli F. Recent advances on the immunomodulatory effects of IFN-alpha: Implications for cancer immunotherapy and autoimmunity. Autoimmunity. 2010;43(3): 204-209.
49. Huber JP, Farrar JD. Regulation of effector and memory T-cell functions by type I interferon. Immunology. 2011;132(4):466-474.
50. Kiladjian JJ, Massé A, Cassinat B, et al; French Intergroup of Myeloproliferative Neoplasms (FIM). Clonal analysis of erythroid progenitors suggests that pegylated interferon alpha-2a treatment targets JAK2V617F clones without affecting TET2 mutant cells. Leukemia. 2010;24(8):1519-1523.