Mechanisms of thrombogenesis in polycythemia vera

Blood Reviews

Volumn 29, Issue 4, 2015, Pages 215-221

  Kroll, Michael H ^a   Michaelis, Laura C ^b   Verstovsek, Srdan ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b FROEDTERT MEMORIAL LUTHERAN HOSPITAL   (United States)

Author keywords

Janus kinase 2; Polycythemia vera; Thrombosis

Indexed keywords

ACETYLSALICYLIC ACID; ANTITHROMBOCYTIC AGENT; C REACTIVE PROTEIN; HYDROXYUREA; JANUS KINASE 2; MOMELOTINIB; PEGINTERFERON ALPHA2A; PEGINTERFERON ALPHA2B; RECOMBINANT GAMMA INTERFERON; RUXOLITINIB; STAT PROTEIN;

ALLELE; ARTERY THROMBOSIS; BLOOD CLOTTING; CANCER CHEMOTHERAPY; CANCER MORTALITY; CANCER SURGERY; CELL ACTIVATION; CELL ADHESION; DRUG EFFICACY; ENDOTHELIUM CELL; ERYTHROCYTE; ERYTHROCYTOSIS; GENE MUTATION; HEMATOCRIT; HUMAN; INFLAMMATION; JAK2 GENE; LEUKOCYTE ACTIVATION; LEUKOCYTOSIS; MEDICAL HISTORY; MEMBRANE MICROPARTICLE; MORBIDITY; MYELOFIBROSIS; MYELOPROLIFERATIVE DISORDER; PHASE 2 CLINICAL TRIAL (TOPIC); PHLEBOTOMY; POLYCYTHEMIA VERA; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; RISK FACTOR; RISK REDUCTION; SIGNAL TRANSDUCTION; THROMBOCYTE ACTIVATION; THROMBOCYTHEMIA; VEIN THROMBOSIS; PATHOPHYSIOLOGY; THROMBOSIS;

HUMANS; POLYCYTHEMIA VERA; RISK FACTORS; THROMBOSIS;

EID: 84937164094     PISSN: 0268960X     EISSN: 15321681     Source Type: Journal    
DOI: 10.1016/j.blre.2014.12.002     Document Type: Article

References (66)

1. Gruppo Italiano Studio Policitemia Polycythemia vera: the natural history of 1213 patients followed for 20years. Gruppo Italiano Studio Policitemia. Ann Intern Med 1995, 123:656-664.
2. Tefferi A., Rumi E., Finazzi G., Gisslinger H., Vannucchi A.M., Rodeghiero F., et al. Survival and prognosis among 1545 patients with contemporary polycythemia vera: an international study. Leukemia 2013, 27:1874-1881.
3. Kiladjian J.J., Chevret S., Dosquet C., Chomienne C., Rain J.D. Treatment of polycythemia vera with hydroxyurea and pipobroman: final results of a randomized trial initiated in 1980. J Clin Oncol 2011, 29:3907-3913.
4. Hultcrantz M., Kristinsson S.Y., Andersson T.M., Landgren O., Eloranta S., Derolf A.R., et al. Patterns of survival among patients with myeloproliferative neoplasms diagnosed in Sweden from 1973 to 2008: a population-based study. J Clin Oncol 2012, 30:2995-3001.
5. Mehta J., Wang H., Fryzek J.P., Iqbal S.U., Mesa R. Health resource utilization and cost associated with myeloproliferative neoplasms in a large United States health plan. Leuk Lymphoma 2014, 55:2368-2374.
6. Tefferi A. Polycythemia vera and essential thrombocythemia: 2013 update on diagnosis, risk-stratification, and management. Am J Hematol 2013, 88:507-516.
7. Passamonti F. How I treat polycythemia vera. Blood 2012, 120:275-284.
8. Alvarez-Larran A., Pereira A., Cervantes F., Arellano-Rodrigo E., Hernandez-Boluda J.C., Ferrer-Marin F., et al. Assessment and prognostic value of the European LeukemiaNet criteria for clinicohematologic response, resistance, and intolerance to hydroxyurea in polycythemia vera. Blood 2012, 119:1363-1369.
9. Barbui T., Finazzi M.C., Finazzi G. Front-line therapy in polycythemia vera and essential thrombocythemia. Blood Rev 2012, 26:205-211.
10. Levine R.L., Wadleigh M., Cools J., Ebert B.L., Wernig G., Huntly B.J., 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.
11. Kralovics R., Passamonti F., Buser A.S., Teo S.S., Tiedt R., Passweg J.R., et al. A gain-of-function mutation of JAK2 in myeloproliferative disorders. N Engl J Med 2005, 352:1779-1790.
12. James C., Ugo V., Le Couedic J.P., 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.
13. Baxter E.J., Scott L.M., Campbell P.J., East C., Fourouclas N., Swanton S., et al. Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders. Lancet 2005, 365:1054-1061.
14. Passamonti F., Rumi E., Pietra D., Elena C., Boveri E., Arcaini L., et al. A prospective study of 338 patients with polycythemia vera: the impact of JAK2 (V617F) allele burden and leukocytosis on fibrotic or leukemic disease transformation and vascular complications. Leukemia 2010, 24:1574-1579.
15. Quintas-Cardama A., Kantarjian H., Cortes J., Verstovsek S. Janus kinase inhibitors for the treatment of myeloproliferative neoplasias and beyond. Nat Rev Drug Discov 2011, 10:127-140.
16. Barbui T., Carobbio A., Finazzi G., Vannucchi A.M., Barosi G., Antonioli E., et al. Inflammation and thrombosis in essential thrombocythemia and polycythemia vera: different role of C-reactive protein and pentraxin 3. Haematologica 2011, 96:315-318.
17. Chung I., Lip G.Y. Virchow's triad revisited: blood constituents. Pathophysiol Haemost Thromb 2003, 33:449-454.
18. Virchow R. Thrombosis and emboli (1846-1856) 1998, Science History Publications, Canton, Mass.
19. Nieswandt B., Pleines I., Bender M. Platelet adhesion and activation mechanisms in arterial thrombosis and ischaemic stroke. J Thromb Haemost 2011, 9(Suppl. 1):92-104.
20. Wakefield T.W., Myers D.D., Henke P.K. Mechanisms of venous thrombosis and resolution. Arterioscler Thromb Vasc Biol 2008, 28:387-391.
21. Mackman N. New insights into the mechanisms of venous thrombosis. J Clin Invest 2012, 122:2331-2336.
22. Rumbaut R.E., Thiagarajan P. Arterial, venous, and microvascular hemostasis/thrombosis. Platelet-vessel wall interactions in hemostasis and thrombosis 2010, Morgan & Claypool Life Sciences, San Rafael (CA).
23. Marchioli R., Finazzi G., Landolfi R., Kutti J., Gisslinger H., Patrono C., et al. Vascular and neoplastic risk in a large cohort of patients with polycythemia vera. J Clin Oncol 2005, 23:2224-2232.
24. Smalberg J.H., Arends L.R., Valla D.C., Kiladjian J.J., Janssen H.L., Leebeek F.W. Myeloproliferative neoplasms in Budd-Chiari syndrome and portal vein thrombosis: a meta-analysis. Blood 2012, 120:4921-4928.
25. Previtali E., Bucciarelli P., Passamonti S.M., Martinelli I. Risk factors for venous and arterial thrombosis. Blood Transfus 2011, 9:120-138.
26. Landolfi R., Di Gennaro L., Barbui T., De Stefano V., Finazzi G., Marfisi R., et al. Leukocytosis as a major thrombotic risk factor in patients with polycythemia vera. Blood 2007, 109:2446-2452.
27. Gangat N., Strand J., Li C.Y., Wu W., Pardanani A., Tefferi A. Leucocytosis in polycythaemia vera predicts both inferior survival and leukaemic transformation. Br J Haematol 2007, 138:354-358.
28. Marchioli R., Finazzi G., Specchia G., Cacciola R., Cavazzina R., Cilloni D., et al. Cardiovascular events and intensity of treatment in polycythemia vera. N Engl J Med 2013, 368:22-33.
29. Di Nisio M., Barbui T., Di Gennaro L., Borrelli G., Finazzi G., Landolfi R., et al. The haematocrit and platelet target in polycythemia vera. Br J Haematol 2007, 136:249-259.
30. Cinar Y., Demir G., Pac M., Cinar A.B. Effect of hematocrit on blood pressure via hyperviscosity. Am J Hypertens 1999, 12:739-743.
31. De Grandis M., Cambot M., Wautier M.P., Cassinat B., Chomienne C., Colin Y., et al. JAK2V617F activates Lu/BCAM-mediated red cell adhesion in polycythemia vera through an EpoR-independent Rap1/Akt pathway. Blood 2013, 121:658-665.
32. Caramazza D., Caracciolo C., Barone R., Malato A., Saccullo G., Cigna V., et al. Correlation between leukocytosis and thrombosis in Philadelphia-negative chronic myeloproliferative neoplasms. Ann Hematol 2009, 88:967-971.
33. De Stefano V., Za T., Rossi E., Vannucchi A.M., Ruggeri M., Elli E., et al. Recurrent thrombosis in patients with polycythemia vera and essential thrombocythemia: incidence, risk factors, and effect of treatments. Haematologica 2008, 93:372-380.
34. Vannucchi A.M., Antonioli E., Guglielmelli P., Longo G., Pancrazzi A., Ponziani V., et al. Prospective identification of high-risk polycythemia vera patients based on JAK2(V617F) allele burden. Leukemia 2007, 21:1952-1959.
35. Levine R.L., Belisle C., Wadleigh M., Zahrieh D., Lee S., Chagnon P., et al. X-inactivation-based clonality analysis and quantitative JAK2V617F assessment reveal a strong association between clonality and JAK2V617F in PV but not ET/MMM, and identifies a subset of JAK2V617F-negative ET and MMM patients with clonal hematopoiesis. Blood 2006, 107:4139-4141.
36. Harlan J.M., Killen P.D., Harker L.A., Striker G.E., Wright D.G. Neutrophil-mediated endothelial injury in vitro mechanisms of cell detachment. J Clin Invest 1981, 68:1394-1403.
37. Weksler B.B., Jaffe E.A., Brower M.S., Cole O.F. Human leukocyte cathepsin G and elastase specifically suppress thrombin-induced prostacyclin production in human endothelial cells. Blood 1989, 74:1627-1634.
38. Celi A., Pellegrini G., Lorenzet R., De Blasi A., Ready N., Furie B.C., et al. P-selectin induces the expression of tissue factor on monocytes. Proc Natl Acad Sci U S A 1994, 91:8767-8771.
39. Falanga A., Marchetti M., Evangelista V., Manarini S., Oldani E., Giovanelli S., et al. Neutrophil activation and hemostatic changes in healthy donors receiving granulocyte colony-stimulating factor. Blood 1999, 93:2506-2514.
40. Lip G.Y., von Blann A. Willebrand factor: a marker of endothelial dysfunction in vascular disorders?. Cardiovasc Res 1997, 34:255-265.
41. Evangelista V., Rajtar G., de Gaetano G., White J.G., Cerletti C. Platelet activation by fMLP-stimulated polymorphonuclear leukocytes: the activity of cathepsin G is not prevented by antiproteinases. Blood 1991, 77:2379-2388.
42. Falanga A., Marchetti M., Evangelista V., Vignoli A., Licini M., Balicco M., et al. Polymorphonuclear leukocyte activation and hemostasis in patients with essential thrombocythemia and polycythemia vera. Blood 2000, 96:4261-4266.
43. Falanga A., Marchetti M., Vignoli A., Balducci D., Barbui T. Leukocyte-platelet interaction in patients with essential thrombocythemia and polycythemia vera. Exp Hematol 2005, 33:523-530.
44. Cerletti C., Tamburrelli C., Izzi B., Gianfagna F., de Gaetano G. Platelet-leukocyte interactions in thrombosis. Thromb Res 2012, 129:263-266.
45. Hobbs C.M., Manning H., Bennett C., Vasquez L., Severin S., Brain L., et al. JAK2V617F leads to intrinsic changes in platelet formation and reactivity in a knock-in mouse model of essential thrombocythemia. Blood 2013, 122:3787-3797.
46. Owens A.P., Mackman N. Microparticles in hemostasis and thrombosis. Circ Res 2011, 108:1284-1297.
47. Tan X., Shi J., Fu Y., Gao C., Yang X., Li J., et al. Role of erythrocytes and platelets in the hypercoagulable status in polycythemia vera through phosphatidylserine exposure and microparticle generation. Thromb Haemost 2013, 109:1025-1032.
48. Han Y., Zhao S., Zhang W., Cen J., Zhang W., Qiu H., et al. Clinical significance of circulating microparticles in Ph-myeloproliferative neoplasms (MPN). Blood (ASH Annual Meeting Abstracts) 2013, 122. [abstract 2368].
49. Chen H., Angerer J.I., Napoleone M., Reininger A.J., Schneider S.W., Wixforth A., et al. Hematocrit and flow rate regulate the adhesion of platelets to von Willebrand factor. Biomicrofluidics 2013, 7:64113.
50. Nuyttens B.P., Thijs T., Deckmyn H., Broos K. Platelet adhesion to collagen. Thromb Res 2011, 127(Suppl. 2):S26-S29.
51. Holme P.A., Orvim U., Hamers M.J., Solum N.O., Brosstad F.R., Barstad R.M., et al. Shear-induced platelet activation and platelet microparticle formation at blood flow conditions as in arteries with a severe stenosis. Arterioscler Thromb Vasc Biol 1997, 17:646-653.
52. Evangelista V., Piccardoni P., White J.G., de Gaetano G., Cerletti C. Cathepsin G-dependent platelet stimulation by activated polymorphonuclear leukocytes and its inhibition by antiproteinases: role of P-selectin-mediated cell-cell adhesion. Blood 1993, 81:2947-2957.
53. Lu W.J., Lin K.C., Huang S.Y., Thomas P.A., Wu Y.H., Wu H.C., et al. Role of a Janus kinase 2-dependent signaling pathway in platelet activation. Thromb Res 2014, 133:1088-1096.
54. Passamonti F., Rumi E., Pietra D., Della Porta M.G., Boveri E., Pascutto C., et al. Relation between JAK2 (V617F) mutation status, granulocyte activation, and constitutive mobilization of CD34+ cells into peripheral blood in myeloproliferative disorders. Blood 2006, 107:3676-3682.
55. Henn V., Slupsky J.R., Grafe M., Anagnostopoulos I., Forster R., Muller-Berghaus G., et al. CD40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells. Nature 1998, 391:591-594.
56. Dole V.S., Bergmeier W., Mitchell H.A., Eichenberger S.C., Wagner D.D. Activated platelets induce Weibel-Palade-body secretion and leukocyte rolling in vivo: role of P-selectin. Blood 2005, 106:2334-2339.
57. Slupsky J.R., Kalbas M., Willuweit A., Henn V., Kroczek R.A., Muller-Berghaus G. Activated platelets induce tissue factor expression on human umbilical vein endothelial cells by ligation of CD40. Thromb Haemost 1998, 80:1008-1014.
58. De Caterina R., Husted S., Wallentin L., Andreotti F., Arnesen H., Bachmann F., et al. General mechanisms of coagulation and targets of anticoagulants (Section I). Position Paper of the ESC Working Group on Thrombosis-Task Force on Anticoagulants in Heart Disease. Thromb Haemost 2013, 109:569-579.
59. Aksu K., Donmez A., Keser G. Inflammation-induced thrombosis: mechanisms, disease associations and management. Curr Pharm Des 2012, 18:1478-1493.
60. Barbui T., Barosi G., Birgegard G., Cervantes F., Finazzi G., Griesshammer M., et al. Philadelphia-negative classical myeloproliferative neoplasms: critical concepts and management recommendations from European LeukemiaNet. J Clin Oncol 2011, 29:761-770.
61. Berk P.D., Goldberg J.D., Silverstein M.N., Weinfeld A., Donovan P.B., Ellis J.T., et al. Increased incidence of acute leukemia in polycythemia vera associated with chlorambucil therapy. N Engl J Med 1981, 304:441-447.
62. Haanen C., Mathé G., Hayat M., Peetermans N., Cauchie C., Michel J., et al. Treatment of polycythaemia vera by radiophosphorus or busulphan: a randomized trial. "Leukemia and Hematosarcoma" Cooperative Group, European Organization for Research on Treatment of Cancer (E.O.R.T.C.). Br J Cancer 1981, 44:75-80.
63. Verstovsek S., Kiladjian J.J., Griesshammer M., Masszi T., Durrant S., Passamonti F., et al. Results of a prospective, randomized, open-label phase 3 study of ruxolitinib (RUX) in polycythemia vera (PV) patients resistant to or intolerant of hydroxyurea (HU): the RESPONSE trial. J Clin Oncol 2014, 32. [abstract 7026].
64. Kiladjian J.J., Cassinat B., Chevret S., Turlure P., Cambier N., Roussel M., et al. Pegylated interferon-alfa-2a induces complete hematologic and molecular responses with low toxicity in polycythemia vera. Blood 2008, 112:3065-3072.
65. Quintas-Cardama A., Kantarjian H., Manshouri T., Luthra R., Estrov Z., Pierce S., et al. Pegylated interferon alfa-2a yields high rates of hematologic and molecular response in patients with advanced essential thrombocythemia and polycythemia vera. J Clin Oncol 2009, 27:5418-5424.
66. Quintas-Cardama A., Abdel-Wahab O., Manshouri T., Kilpivaara O., Cortes J., Roupie A.L., et al. Molecular analysis of patients with polycythemia vera or essential thrombocythemia receiving pegylated interferon alpha-2a. Blood 2013, 122:893-901.