The thrombopoietin receptor, MPL, is critical for development of a JAK2V617F-induced myeloproliferative neoplasm

Blood

Volumn 124, Issue 26, 2014, Pages 3956-3963

  Sangkhae, Veena ^a,b   Etheridge, S Leah ^a,b   Kaushansky, Kenneth ^a   Hitchcock, Ian S ^a,b  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITY OF YORK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

JANUS KINASE 2; MPL PROTEIN; THROMBOPOIETIN RECEPTOR; UNCLASSIFIED DRUG; CYTOKINE; JAK2 PROTEIN, HUMAN; JAK2 PROTEIN, MOUSE; MPL PROTEIN, HUMAN; MPL PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER STEM CELL; CARCINOGENESIS; CONTROLLED STUDY; DISEASE SEVERITY; HEMATOPOIESIS; MOUSE; MYELOPROLIFERATIVE NEOPLASM; NEUTROPHILIA; NONHUMAN; PHENOTYPE; SPLENOMEGALY; STEM CELL EXPANSION; THROMBOCYTHEMIA; THROMBOCYTOSIS; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CELL PROLIFERATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HEMATOPOIETIC STEM CELL; HETEROZYGOTE; HOMOZYGOTE; KNOCKOUT MOUSE; METABOLISM; MYELOPROLIFERATIVE DISORDER; PHYSIOLOGY; STEM CELL; TRANSGENIC MOUSE;

ANIMALS; BONE MARROW CELLS; CELL PROLIFERATION; CYTOKINES; GENE EXPRESSION REGULATION, NEOPLASTIC; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HETEROZYGOTE; HOMOZYGOTE; JANUS KINASE 2; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MYELOPROLIFERATIVE DISORDERS; RECEPTORS, THROMBOPOIETIN; STEM CELLS;

EID: 84919466830     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-07-587238     Document Type: Article

References (51)

1. Geddis AE, Linden HM, Kaushansky K. Thrombopoietin: a pan-hematopoietic cytokine. Cytokine Growth Factor Rev. 2002;13(1):61-73.
2. Lannutti BJ, Epp A, Roy J, Chen J, Josephson NC. Incomplete restoration of Mpl expression in the mpl-/- mouse produces partial correction of the stem cell-repopulating defect and paradoxical thrombocytosis. Blood. 2009;113(8):1778-1785.
3. Tiedt R, Coers J, Ziegler S, et al. Pronounced thrombocytosis in transgenic mice expressing reduced levels of Mpl in platelets and terminally differentiated megakaryocytes. Blood. 2009;113(8):1768-1777.
4. Kaushansky K. Thrombopoietin and the hematopoietic stem cell. Ann N Y Acad Sci. 2005;1044:139-141.
5. Ihara K, Ishii E, Eguchi M, et al. Identification of mutations in the c-mpl gene in congenital amegakaryocytic thrombocytopenia. Proc Natl Acad Sci USA. 1999;96(6):3132-3136.
6. Ballmaier M, Germeshausen M, Schulze H, et al. c-mpl mutations are the cause of congenital amegakaryocytic thrombocytopenia. Blood. 2001;97(1):139-146.
7. Pikman Y, Lee BH, Mercher T, et al. MPLW515L is a novel somatic activating mutation in myelofibrosis with myeloid metaplasia. PLoS Med. 2006;3(7):e270.
8. Pardanani AD, Levine RL, Lasho T, et al. MPL515 mutations in myeloproliferative and other myeloid disorders: a study of 1182 patients. Blood. 2006;108(10):3472-3476.
9. Liu K, Martini M, Rocca B, et al. Evidence for a founder effect of the MPL-S505N mutation in eight Italian pedigrees with hereditary thrombocythemia. Haematologica. 2009;94(10):1368-1374.
10. Chou FS, Mulloy JC. The thrombopoietin/MPL pathway in hematopoiesis and leukemogenesis. J Cell Biochem. 2011;112(6):1491-1498.
11. 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.
12. 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.
13. 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.
14. 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.
15. 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.
16. Wernig G, Gonneville JR, Crowley BJ, et al. The Jak2V617F oncogene associated with myeloproliferative diseases requires a functional FERM domain for transformation and for expression of the Myc and Pim proto-oncogenes. Blood. 2008;111(7):3751-3759.
17. Etheridge SL, Cosgrove ME, Sangkhae V, et al. A novel activating, germline JAK2 mutation, JAK2R564Q, causes familial essential thrombocytosis. Blood. 2014;123(7):1059-1068.
18. Vainchenker W, Delhommeau F, Constantinescu SN, Bernard OA. New mutations and pathogenesis of myeloproliferative neoplasms. Blood. 2011;118(7):1723-1735.
19. Klampfl T, Gisslinger H, Harutyunyan AS, et al. Somatic mutations of calreticulin in myeloproliferative neoplasms. N Engl J Med. 2013;369(25):2379-2390.
20. Nangalia J, Massie CE, Baxter EJ, et al. Somatic CALR mutations in myeloproliferative neoplasms with nonmutated JAK2. N Engl J Med. 2013;369(25):2391-2405.
21. 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.
22. Tefferi A, Lasho TL, Huang J, et al. Low JAK2V617F allele burden in primary myelofibrosis, compared to either a higher allele burden or unmutated status, is associated with inferior overall and leukemia-free survival. Leukemia. 2008;22(4):756-761.
23. Verstovsek S, Kantarjian H, Mesa RA, et al. Safety and efficacy of INCB018424, a JAK1 and JAK2 inhibitor, in myelofibrosis. N Engl J Med. 2010;363(12):1117-1127.
24. Tefferi A, Litzow MR, Pardanani A. Long-term outcome of treatment with ruxolitinib in myelofibrosis. N Engl J Med. 2011;365(15):1455-1457.
25. Li Y, Hetet G, Kiladjian JJ, Gardin C, Grandchamp B, Briere J. Proto-oncogene c-mpl is involved in spontaneous megakaryocytopoiesis in myeloproliferative disorders. Br J Haematol. 1996;92(1):60-66.
26. Cocault L, Bouscary D, Le Bousse Kerdiles C, et al. Ectopic expression of murine TPO receptor (c-mpl) in mice is pathogenic and induces erythroblastic proliferation. Blood. 1996;88(5):1656-1665.
27. Moliterno AR, Hankins WD, Spivak JL. Impaired expression of the thrombopoietin receptor by platelets from patients with polycythemia vera. N Engl J Med. 1998;338(9):572-580.
28. Etheridge SL, Roh ME, Cosgrove ME, et al. JAK2V617F-positive endothelial cells contribute to clotting abnormalities in myeloproliferative neoplasms. Proc Natl Acad Sci USA. 2014;111(6):2295-2300.
29. Constien R, Forde A, Liliensiek B, et al. Characterization of a novel EGFP reporter mouse to monitor Cre recombination as demonstrated by a Tie2 Cre mouse line. Genesis. 2001;30(1):36-44.
30. Alexander WS, Roberts AW, Nicola NA, Li R, Metcalf D. Deficiencies in progenitor cells of multiple hematopoietic lineages and defective megakaryocytopoiesis in mice lacking the thrombopoietic receptor c-Mpl. Blood. 1996;87(6):2162-2170.
31. Gurney AL, de Sauvage FJ. Dissection of c-Mpl and thrombopoietin function: studies of knockout mice and receptor signal transduction. Stem Cells. 1996;14(Suppl 1):116-123.
32. Cohen-Solal K, Vitrat N, Titeux M, Vainchenker W, Wendling F. High-level expression of Mpl in platelets and megakaryocytes is independent of thrombopoietin. Blood. 1999;93(9):2859-2866.
33. Petit-Cocault L, Volle-Challier C, Fleury M, Péault B, Souyri M. Dual role of Mpl receptor during the establishment of definitive hematopoiesis. Development. 2007;134(16):3031-3040.
34. Solar GP, Kerr WG, Zeigler FC, et al. Role of c-mpl in early hematopoiesis. Blood. 1998;92(1):4-10.
35. Kent DG, Copley MR, Benz C, et al. Prospective isolation and molecular characterization of hematopoietic stem cells with durable self-renewal potential. Blood. 2009;113(25):6342-6350.
36. Ku H, Yonemura Y, Kaushansky K, Ogawa M. Thrombopoietin, the ligand for the Mpl receptor, synergizes with steel factor and other early acting cytokines in supporting proliferation of primitive hematopoietic progenitors of mice. Blood. 1996; 87(11):4544-4551.
37. Sitnicka E, Lin N, Priestley GV, et al. The effect of thrombopoietin on the proliferation and differentiation of murine hematopoietic stem cells. Blood. 1996;87(12):4998-5005.
38. Fox N, Priestley G, Papayannopoulou T, Kaushansky K. Thrombopoietin expands hematopoietic stem cells after transplantation. J Clin Invest. 2002;110(3):389-394.
39. Bhagwat N, Koppikar P, Keller M, et al. Improved targeting of JAK2 leads to increased therapeutic efficacy in myeloproliferative neoplasms. Blood. 2014;123(13):2075-2083.
40. Drachman JG, Millett KM, Kaushansky K. Thrombopoietin signal transduction requires functional JAK2, not TYK2. J Biol Chem. 1999; 274(19):13480-13484.
41. Brizzi MF, Zini MG, Aronica MG, Blechman JM, Yarden Y, Pegoraro L. Convergence of signaling by interleukin-3, granulocyte-macrophage colony-stimulating factor, and mast cell growth factor on JAK2 tyrosine kinase. J Biol Chem. 1994;269(50):31680-31684.
42. Witthuhn BA, Quelle FW, Silvennoinen O, et al. JAK2 associates with the erythropoietin receptor and is tyrosine phosphorylated and activated following stimulation with erythropoietin. Cell. 1993;74(2):227-236.
43. Ng AP, Kauppi M, Metcalf D, et al. Mpl expression on megakaryocytes and platelets is dispensable for thrombopoiesis but essential to prevent myeloproliferation. Proc Natl Acad Sci USA. 2014; 111(16):5884-5889.
44. Meyer SC, Keller MD, Woods BA, et al. Genetic studies reveal an unexpected negative regulatory role for Jak2 in thrombopoiesis. Blood. 2014;124(14):2280-2284.
45. Besancenot R, Roos-Weil D, Tonetti C, et al. JAK2 and MPL protein levels determine TPO-induced megakaryocyte proliferation vs differentiation. Blood. 2014;124(13):2104-2115.
46. Yan D, Hutchison RE, Mohi G. Tyrosine 201 is required for constitutive activation of JAK2V617F and efficient induction of myeloproliferative disease in mice. Blood. 2012;120(9):1888-1898.
47. Pecquet C, Diaconu CC, Staerk J, et al. Thrombopoietin receptor down-modulation by JAK2 V617F: restoration of receptor levels by inhibitors of pathologic JAK2 signaling and of proteasomes. Blood. 2012;119(20):4625-4635.
48. 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.
49. Staerk J, Constantinescu SN. The JAK-STAT pathway and hematopoietic stem cells from the JAK2 V617F perspective. JAKSTAT. 2012;1(3):184-190.
50. 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.
51. Li J, Kent DG, Chen E, Green AR. Mouse models of myeloproliferative neoplasms: JAK of all grades. Dis Model Mech. 2011;4(3):311-317.