JAK2 V617F impairs hematopoietic stem cell function in a conditional knock-in mouse model of JAK2 V617F-positive essential thrombocythemia

Blood

Volumn 116, Issue 9, 2010, Pages 1528-1538

  Li, Juan ^a   Spensberger, Dominik ^a   Ahn, Jong Sook ^a   Anand, Shubha ^a   Beer, Philip A ^a,b   Ghevaert, Cedric ^c   Chen, Edwin ^a   Forrai, Ariel ^a   Scott, Linda M ^a,d   Ferreira, Rita ^a   Campbell, Peter J ^e   Watson, Steve P ^c   Liu, Pentao ^e   Erber, Wendy N ^b   Huntly, Brian J P ^a,b   Ottersbach, Katrin ^a   Green, Anthony R ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b ADDENBROOKE S HOSPITAL   (United Kingdom)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d Mays Cancer Center at UT Health San Antonio   (United States)

^e WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; INTEGRASE; JANUS KINASE 2; MESSENGER RNA;

ANIMAL; APOPTOSIS; BONE MARROW TRANSPLANTATION; CELL CYCLE; CELL PROLIFERATION; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE TARGETING; GENETICS; HEMATOPOIETIC STEM CELL; HUMAN; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; POINT MUTATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THROMBOCYTHEMIA; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; BONE MARROW TRANSPLANTATION; CELL CYCLE; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE KNOCK-IN TECHNIQUES; HEMATOPOIETIC STEM CELLS; HUMANS; INTEGRASES; JANUS KINASE 2; MICE; POINT MUTATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; THROMBOCYTHEMIA, ESSENTIAL;

EID: 77956578342     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-12-259747     Document Type: Article

References (46)

1. James C, Ugo V, Le Couedic JP, et al. A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature. 2005;434(7037):1144-1148. (Pubitemid 40663494)
2. Baxter EJ, Scott LM, Campbell PJ, et al. Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders. Lancet. 2005;365(9464):1054-1061. (Pubitemid 40386783)
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, Teo SS, et al. A gain of function mutation in Jak2 is frequently found in patients with myeloproliferative disorders. N Engl J Med. 2005;352(17):1779-1790.
5. Fialkow P, Gartler SM, Yoshida A. Clonal origin of chronic myelocytic leukemia in man. Proc Natl Acad Sci U S A. 1967;58(4):1468-1471.
6. Fialkow JP, Faguet GB, Jacobson RJ, Vaidya K, Murphy S. Evidence that essential thrombocythemia is a clonal disorder with origin in a multipotent stem cell. Blood. 1981;58(5):916-919.
7. Jamieson CH, Gotlib J, Durocher JA, et al. The JAK2 V617F mutation occurs in hematopoietic stem cells in polycythemia vera and predisposes toward erythroid differentiation. Proc Natl Acad Sci U S A. 2006;103(16):6224-6229.
8. 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.
9. Schaub FX, Jager R, Looser R, et al. Clonal analysis of deletions on chromosome 20q and JAK2-V617F in MPD suggests that del20q acts independently and is not one of the predisposing mutations for JAK2-V617F. Blood. 2009;113(9):2022-2027.
10. Delhommeau F, Dupont S, Della Valle V, et al. Mutation in TET2 in myeloid cancers. N Engl J Med. 2009;360(22):2289-2301.
11. Campbell PJ, Scott LM, Buck G, et al. Definition of subtypes of essential thrombocythaemia and relation to polycythaemia vera based on JAK2 V617F mutation status: a prospective study. Lancet. 2005;366(9501):1945-1953.
12. Scott LM, Scott MA, Campbell PJ, Green AR. Progenitors homozygous for the V617F mutation occur in most patients with polycythemia vera, but not essential thrombocythemia. Blood. 2006;108(7):2435-2437.
13. Dupont S, Masse 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. (Pubitemid 47267441)
14. Scott LM, Tong W, Levine RL, et al. JAK2 exon 12 mutations in polycythemia vera and idiopathic erythrocytosis. N Engl J Med. 2007;356(5):459-468.
15. 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.
16. 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. (Pubitemid 44316134)
17. Bumm TG, Elsea C, Corbin AS, et al. Characterization of murine JAK2V617F-positive myeloproliferative disease. Cancer Res. 2006;66(23):11156- 11165.
18. Zaleskas VM, Krause DS, Lazarides K, et al. Molecular pathogenesis and therapy of polycythemia induced in mice by JAK2 V617F. PLoS One. 2006;1:e18.
19. Tiedt R, Hao-Shen H, Sobas MA, et al. Ratio of mutant JAK2-V617F to wild-type Jak2 determines the MPD phenotypes in transgenic mice. Blood. 2008;111(8):3931-3940.
20. Xing S, Wanting TH, Zhao W, et al. Transgenic expression of JAK2V617F causes myeloproliferative disorders in mice. Blood. 2008;111(10):5109-5117.
21. 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.
22. Liu P, Jenkins NA, Copeland NG. A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res. 2003;13(3):476-484.
23. Kuhn R, Schwenk F, Aguet M, Rajewsky K. Inducible gene targeting in mice. Science. 1995;269(5229):1427-1429.
24. Hall MA, Curtis DJ, Metcalf D, et al. The critical regulator of embryonic hematopoiesis, SCL, is vital in the adult for megakaryopoiesis, erythropoiesis, and lineage choice in CFU-S12. Proc Natl Acad Sci U S A. 2003;100(3):992-997.
25. Laubach JP, Fu P, Jiang X, Salter KH, Potti A, Arcasoy MO. Polycythemia vera erythroid precursors exhibit increased proliferation and apoptosis resistance associated with abnormal RAS and PI3K pathway activation. Exp Hematol. 2009;37(12):1411-1422.
26. Heller PG, Lev PR, Salim JP, et al. JAK2V617F mutation in platelets from essential thrombocythemia patients: correlation with clinical features and analysis of STAT5 phosphorylation status. Eur J Haematol. 2006;77(3):210-216.
27. Mason KD, Carpinelli MR, Fletcher JI, et al. Programmed anuclear cell death delimits platelet life span. Cell. 2007;128(6):1173-1186.
28. Johnson GR, Metcalf D. Pure and mixed erythroid colony formation in vitro stimulated by spleen conditioned medium with no detectable erythropoietin. Proc Natl Acad Sci U S A. 1977;74(9):3879-3882. (Pubitemid 8193527)
29. Sato T, Maekawa T, Watanabe S, Tsuji K, Nakahata T. Erythroid progenitors differentiate and mature in response to endogenous erythropoietin. J Clin Invest. 2000;106(2):263-270.
30. 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.
31. Cramer K, Nieborowska-Skorska M, Koptyra M, et al. BCR/ABL and other kinases from chronic myeloproliferative disorders stimulate single-strand annealing, an unfaithful DNA double-strand break repair. Cancer Res. 2008;68(17):6884-6888.
32. Rossi DJ, Bryder D, Seita J, Nussenzweig A, Hoeijmakers J, Weissman IL. Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature. 2007;447(7145):725-729. (Pubitemid 46889729)
33. Nijnik A, Woodbine L, Marchetti C, et al. DNA repair is limiting for haematopoietic stem cells during ageing. Nature. 2007;447(7145):686-690.
34. Zhao R, Follows GA, Beer PA, et al. Inhibition of the Bcl-xL deamidation pathway in myeloproliferative disorders. N Engl J Med. 2008;359(26):2778-2789.
35. Lacout C, Pisani DF, Tulliez M, Moreau Gachelin F, 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.
36. 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.
37. Antonioli E, Guglielmelli P, Pancrazzi A, et al. Clinical implications of the JAK2 V617F mutation in essential thrombocythemia. Leukemia. 2005;19(10):1847-1849. (Pubitemid 41486170)
38. Wolanskyj AP, Lasho TL, Schwager SM, et al. JAK2 mutation in essential thrombocythaemia: clinical associations and long-term prognostic relevance. Br J Haematol. 2005;131(2):208-213.
39. Strobbe L, Lestrade P, Hermans MH, Fijnheer R. Detection of the JAK2V617F mutation in patients with slightly elevated platelets or hemoglobin without a secondary cause. Ann Hematol. 2007;86(11):801-803.
40. Warren LA, Rossi DJ. Stem cells and aging in the hematopoietic system. Mech Ageing Dev. 2009;130(1):46-53.
41. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell. 1997;88(5):593-602.
42. Lin AW, Barradas M, Stone JC, van Aelst L, Serrano M, Lowe SW. Premature senescence involving p53 and p16 is activated in response to constitutive MEK/MAPK mitogenic signaling. Genes Dev. 1998;12(19):3008-3019. (Pubitemid 28469303)
43. Mallette FA, Gaumont-Leclerc MF, Ferbeyre G. The DNA damage signaling pathway is a critical mediator of oncogene-induced senescence. Genes Dev. 2007;21(1):43-48. (Pubitemid 46089705)
44. Michaloglou C, Vredeveld LC, Soengas MS, et al. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature. 2005;436(7051):720- 724.
45. Theocharides A, Passweg JR, Medinger M, et al. The allele burden of JAK2 mutations remains stable over several years in patients with myeloproliferative disorders. Haematologica. 2008;93(12):1890-1893.
46. Van Pelt K, Nollet F, Selleslag D, et al. The JAK2V617F mutation can occur in a hematopoietic stem cell that exhibits no proliferative advantage: a case of human allogeneic transplantation. Blood. 2008;112(3):921-922.