JAK2V617F leads to intrinsic changes in platelet formation and reactivity in a knock-in mouse model of essential thrombocythemia

Blood

Volumn 122, Issue 23, 2013, Pages 3787-3797

  Hobbs, Catherine M ^a   Manning, Harrie ^a   Bennett, Cavan ^a   Vasquez, Louella ^b   Severin, Sonia ^c   Brain, Lauren ^c   Mazharian, Alexandra ^c   Guerrero, Jose A ^a   Li, Juan ^a   Soranzo, Nicole ^a,b   Green, Anthony R ^a   Watson, Steve P ^c   Ghevaert, Cedric ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; C REACTIVE PROTEIN; FIBRINOGEN; JANUS KINASE 2; PADGEM PROTEIN; STAT3 PROTEIN; THROMBIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CLOTTING; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENE MUTATION; IN VITRO STUDY; IN VIVO STUDY; JAK2V617F GENE; MEGAKARYOCYTE; MEGAKARYOPOIESIS; MOUSE; NONHUMAN; PLATELET REACTIVITY; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; THROMBOCYTE AGGREGATION; THROMBOCYTE FUNCTION; THROMBOCYTHEMIA; THROMBOCYTOPOIESIS;

EID: 84891127265     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-06-501452     Document Type: Article

References (59)

1. 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
2. James C, Ugo V, Le Cou'edic JP, et al. A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature. 2005;434(7037):1144-1148
3. 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
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. Landolfi R, Marchioli R, Kutti J, et al European Collaboration on Low-Dose Aspirin in Polycythemia Vera Investigators. Efficacy and safety of low-dose aspirin in polycythemia vera. N Engl J Med. 2004;350(2):114-124
6. Cortelazzo S, Finazzi G, Ruggeri M, et al. Hydroxyurea for patients with essential thrombocythemia and a high risk of thrombosis. N Engl J Med. 1995;332(17):1132-1136
7. Harrison CN, Campbell PJ, Buck G, et al; United Kingdom Medical Research Council PrimaryThrombocythemia 1 Study. Hydroxyurea compared with anagrelide in high-risk ssential thrombocythemia. N Engl J Med. 2005;353(1): 33-45
8. Elliott MA, Tefferi A. Thrombosis and haemorrhage in polycythaemia vera and essential thrombocythaemia. Br J Haematol. 2005;128(3): 275-290
9. Tefferi A, Elliott M. Thrombosis in myeloproliferative disorders: prevalence, prognostic factors, and the role of leukocytes and JAK2V617F. Semin Thromb Hemost. 2007;33(4): 313-320
10. Campbell PJ, Scott LM, Buck G, et al United Kingdom Myeloproliferative Disorders Study Group; Medical Research Council Adult Leukaemia Working Party; Australasian Leukaemia and Lymphoma Group. 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
11. Vannucchi AM, Antonioli E, Guglielmelli P, et al. Clinical profile of homozygous JAK2 617V>.F mutation in patients with polycythemia vera or essential thrombocythemia. Blood. 2007;110(3): 840-846
12. Lussana F, Caberlon S, Pagani C, Kamphuisen PW, Büller HR, Cattaneo M. Association of V617F Jak2 mutation with the risk of thrombosis among patients with essential thrombocythaemia or idiopathic myelofibrosis: a systematic review. Thromb Res. 2009; 124(4):409-417
13. Dahabreh IJ, Zoi K, Giannouli S, Zoi C, Loukopoulos D, Voulgarelis M. Is JAK2 V617F mutation more than a diagnostic index? A meta-analysis of clinical outcomes in ssential thrombocythemia. Leuk Res. 2009;33(1):67-73
14. Patel RK, Lea NC, Heneghan MA, et al. Prevalence of the activating JAK2 tyrosine kinase mutation V617F in the Budd-Chiari syndrome. Gastroenterology. 2006;130(7):2031-2038
15. Boissinot M, Lippert E, Girodon F, et al. Latent myeloproliferative disorder revealed by the JAK2- V617F mutation and endogenous megakaryocytic colonies in patients with splanchnic vein thrombosis. Blood. 2006;108(9):3223-3224
16. Wehmeier A, Südhoff T, Meierkord F. Relation of platelet abnormalities to thrombosis and hemorrhage in chronic myeloproliferative disorders. Semin Thromb Hemost. 1997;23(4): 391-402
17. Landolfi R, Rocca B, Patrono C. Bleeding andthrombosis in myeloproliferative disorders: mechanisms and treatment. Crit Rev Oncol Hematol. 1995;20(3):203-222
18. Michiels JJ, Berneman Z, Schroyens W, Finazzi G, Budde U, van Vliet HH. The paradox of platelet activation and impaired function: platelet-von Willebrand factor interactions, and the etiology of thrombotic and hemorrhagic manifestations in essential thrombocythemia and polycythemia vera. Semin Thromb Hemost. 2006;32(6): 589-604
19. Arellano-Rodrigo E, Alvarez-Larr'an A, Reverter JC, Villamor N, Colomer D, Cervantes F. Increased platelet and leukocyte activation as contributing mechanisms for thrombosis in essential thrombocythemia and correlation with the JAK2 mutational status. Haematologica. 2006; 91(2):169-175
20. Robertson B, Urquhart C, Ford I, et al. Platelet and coagulation activation markers in myeloproliferative diseases: relationships with JAK2 V6I7 F status, clonality, and antiphospholipid antibodies. J Thromb Haemost. 2007;5(8):1679-1685
21. Panova-Noeva M, Marchetti M, Spronk HM, et al. Platelet-induced thrombin generation by the calibrated automated thrombogram assay is increased in patients with essential thrombocythemia and polycythemia vera [published correction appears in Am J Hematol.2011;86(5):466]. Am J Hematol. 2011;86(4): 337-342
22. Randi ML, Brunati AM, Scapin M, et al. Src tyrosine kinase preactivation is associated with platelet hypersensitivity in essential thrombocythemia and polycythemia vera. Blood. 2010;115(3):667-676
23. Moore SF, Hunter RW, Harper MT, et al. Dysfunction of the PI3 kinase/Rap1/integrin (IIb)b(3) pathway underlies ex vivo platelet hypoactivity in essential thrombocythemia. Blood. 2013;121(7):1209-121
24. Adamson JW, Fialkow PJ, Murphy S, Prchal JF, Steinmann L. Polycythemia vera: stem-cell and probable clonal origin of the disease. N Engl J Med. 1976;295(17):913- 916
25. Harrison CN, Gale RE, Machin SJ, Linch DC. A large proportion of patients with a diagnosis of essential thrombocythemia do not have a clonal disorder and may be at lower risk of thrombotic complications. Blood. 1999;93(2):417-424
26. Jones CI, Garner SF, Angenent W, et al Bloodomics Consortium. Mapping the platelet profile for functional genomic studies and emonstration of the effect size of the P6 locus. J Thromb Haemost. 2007;5(8):1756-1765
27. 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 hrombocythemia. Blood. 2010;116(9):1528-1538
28. Lecine P, Blank V, Shivdasani R. Characterization of the hematopoietic transcription factor NF-E2 in primary murine megakaryocytes. J Biol Chem. 1998;273(13):7572-7578
29. Dumon S, Heath VL, Tomlinson MG, Göttgens B, Frampton J. Differentiation of murine committed megakaryocytic progenitors isolated by a novel strategy reveals the omplexity of GATA and Ets factor involvement in megakaryocytopoiesis and an unexpected potential role for GATA-6. Exp Hematol. 2006;34(5):654-663
30. Mazharian A, Thomas SG, Dhanjal TS, Buckley CD, Watson SP. Critical role of Src-Syk- PLCgamma2 signaling in megakaryocyte migration and thrombopoiesis. Blood. 2010; 116(5):793-800
31. Mazharian A, Watson SP, Severin S. Critical role for ERK1/2 in bone marrow and fetal liver-derived primary megakaryocyte differentiation, motility, and proplatelet ormation. Exp Hematol. 2009; 37(10):1238-1249
32. Dhanjal TS, Pendaries C, Ross EA, et al. A novel role for PECAM-1 in megakaryocytokinesis and recovery of platelet counts in thrombocytopenic mice. Blood. 2007;109(10):4237-4244
33. Unsworth AJ, Finney BA, Navarro-Nunez L, Severin S, Watson SP, Pears CJ. Protein kinase Ce and protein kinase Cu double-deficient mice have a bleeding diathesis. J Thromb Haemost. 2012;10(9):1887-1894
34. Auger JM, Kuijpers MJ, Senis YA, Watson SP, Heemskerk JW. Adhesion of human and mouse platelets to collagen under shear: a unifying model. FASEB J. 2005;19(7):825-827
35. McCarty OJ, Zhao Y, Andrew N, et al. Evaluation of the role of platelet integrins in fibronectindependent spreading and adhesion. J Thromb Haemost. 2004;2(10):1823- 1833
36. Dawson MA, Bannister AJ, Göttgens B, et al. JAK2 phosphorylates histone H3Y41 and excludes HP1alpha from chromatin. Nature. 2009; 461(7265):819-822
37. Balduini A, Badalucco S, Pugliano MT, et al. In vitro megakaryocyte differentiation and proplatelet formation in Ph-negative classical myeloproliferative neoplasms: distinct patterns in the different clinical phenotypes. PLoS ONE. 2011;6(6):e21015
38. Mazharian A, Ghevaert C, Zhang L, Massberg S, Watson SP. Dasatinib enhances megakaryocyte differentiation but inhibits platelet formation. Blood. 2011;117(19):5198- 5206
39. Goodall AH, Burns P, Salles I, et al Bloodomics Consortium. Transcription profiling in human platelets reveals LRRFIP1 as a novel protein regulating platelet function. Blood. 010;116(22): 4646-4656
40. Jones CI, Bray S, Garner SF, et al Bloodomics Consortium. A functional genomics approach reveals novel quantitative trait loci associated with platelet signaling pathways. Blood. 2009;114(7): 1405-1416
41. Rodríguez-Liñares B, Watson SP. Thrombopoietin potentiates activation of human platelets in association with JAK2 and TYK2 phosphorylation. Biochem J. 1996;316(pt 1): 93-98
42. Kubota Y, Arai T, Tanaka T, et al. Thrombopoietin modulates platelet activation in vitro through protein-tyrosine phosphorylation. Stem Cells. 1996;14(4):439-444
43. Oda A, Miyakawa Y, Druker BJ, et al. Thrombopoietin primes human platelet aggregation induced by shear stress and by multiple agonists. Blood. 1996;87(11): 4664-4670
44. Montrucchio G, Brizzi MF, Calosso G, Marengo S, Pegoraro L, Camussi G. Effects of recombinant human megakaryocyte growth and development factor on platelet activation. Blood. 1996;87(7): 2762-2768
45. Lupia E, Bosco O, Bergerone S, et al. Thrombopoietin contributes to enhanced platelet activation in patients with unstable angina. J Am Coll Cardiol. 2006;48(11):2195- 2203
46. Kubota Y, Tanaka T, Ohnishi H, et al. Constitutively activated hosphatidylinositol 3- kinase primes platelets from patients with chronic myelogenous leukemia for thrombopoietin-induced aggregation. Leukemia. 2004;18(6):1127-1137
47. Oda A, Miyakawa Y, Druker BJ, et al. Thrombopoietin-induced signal transduction and potentiation of platelet activation. Thromb Haemost. 1999;82(2):377-384
48. Pasquet JM, Gross BS, Gratacap MP, et al. Thrombopoietin potentiates collagen receptor signaling in platelets through a phosphatidylinositol 3-kinase-dependent pathway. Blood. 2000;95(11):3429-3434
49. Patel-Hett S, Wang H, Begonja AJ, et al. The spectrin-based membrane skeleton stabilizes mouse megakaryocyte membrane systems and is essential for proplatelet and platelet formation. Blood. 2011;118(6):1641-1652
50. Thon JN, Montalvo A, Patel-Hett S, et al. Cytoskeletal mechanics of proplatelet maturation and platelet release. J Cell Biol. 2010;191(4): 861-874
51. Zhang L, Orban M, Lorenz M, et al. A novel role of sphingosine 1-phosphate receptor S1pr1 in mouse thrombopoiesis. J Exp Med. 2012;209(12): 2165-2181
52. Zhang L, Urtz N, Gaertner F, et al. Sphingosine kinase 2 (Sphk2) regulates platelet biogenesis by providing intracellular sphingosine 1-phosphate (S1P). Blood. 2013;122(5):791-802
53. Wu Y, Welte T, Michaud M, Madri JA. PECAM-1: a multifaceted regulator of megakaryocytopoiesis. Blood. 2007;110(3):851-859
54. Geddis AE. The regulation of proplatelet production. Haematologica. 2009;94(6): 756-759
55. White MJ, Kile BT. Apoptotic processes in megakaryocytes and platelets. Semin Hematol. 2010;47(3):227-234
56. Khan I, Huang Z, Wen Q, et al. AKT is a therapeutic target in myeloproliferative neoplasms. Leukemia. 2013;27(9): 1882-1890
57. Chagraoui H, Komura E, Tulliez M, Giraudier S,Vainchenker W, Wendling F. Prominent role of TGF-beta 1 in thrombopoietin-induced myelofibrosis in mice. Blood. 2002;100(10): 3495-3503
58. Randrianarison-Huetz V, Laurent B, Bardet V, Blobe GC, Huetz F, Duḿ enil D. Gfi-1B controls human erythroid and megakaryocytic differentiation by regulating TGF-beta signaling at the bipotent erythro-megakaryocytic progenitor stage. Blood. 2010;115(14):2784-2795
59. Gnatenko DV, Zhu W, Xu X, et al. Class prediction models of thrombocytosis using genetic biomarkers. Blood. 2010;115(1):7-14