The renaissance of interferon therapy for the treatment of myeloid malignancies

Blood

Volumn 117, Issue 18, 2011, Pages 4706-4715

  Kiladjian, Jean Jacques ^a,b,c   Mesa, Ruben A ^d   Hoffman, Ronald ^e  

^a SAINT LOUIS HOSPITAL   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c INSERM   (France)

^d MAYO CLINIC   (United States)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ALPHA INTERFERON RECEPTOR; ALPHA1 INTERFERON; ALPHA2 INTERFERON; ALPHA2A INTERFERON; ALPHA2B INTERFERON; ALPHA2C INTERFERON; BETA1 INTERFERON; CXCL11 CHEMOKINE; CXCL9 CHEMOKINE; CYTARABINE; DASATINIB; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GAMMA INTERFERON RECEPTOR 1; IMATINIB; INTERFERON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MYELOBLASTIN; NILOTINIB; PEGINTERFERON ALPHA2A; PEGINTERFERON ALPHA2B;

ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BONE MARROW TUMOR; CANCER IMMUNOTHERAPY; CANCER REGRESSION; CANCER SURVIVAL; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURFACE; CHRONIC MYELOID LEUKEMIA; CROSS PRESENTATION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DOWN REGULATION; DRUG RECEPTOR BINDING; DRUG RESPONSE; EFFECTOR CELL; ENDOTHELIUM CELL; HEMATOPOIETIC STEM CELL; HUMAN; HYPEREOSINOPHILIA; HYPEREOSINOPHILIC SYNDROME; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IMMUNOSURVEILLANCE; LEUKAPHERESIS; LYMPHOCYTE DIFFERENTIATION; LYMPHOMA CELL; MACROPHAGE; MAINTENANCE THERAPY; MAST CELL; MAST CELL DEGRANULATION; MASTOCYTOMA; MONOCYTE; MONONUCLEAR CELL; MYELOFIBROSIS; MYELOID LEUKEMIA; MYELOID METAPLASIA; MYELOPROLIFERATIVE DISORDER; NATURAL KILLER CELL; OUTCOME ASSESSMENT; PHILADELPHIA CHROMOSOME NEGATIVE CELL; POLYCYTHEMIA VERA; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; THROMBOCYTHEMIA; THROMBOCYTOPENIA; UPREGULATION;

EID: 79955947379     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-08-258772     Document Type: Review

References (119)

1. Borden EC, Sen GC, Uze G, et al. Interferons at age 50: past, current and future impact on biomedicine. Nat Rev Drug Discov. 2007;6(12):975-990. (Pubitemid 350201788)
2. le Coutre P, Schwarz M, Kim TD. New developments in tyrosine kinase inhibitor therapy for newly diagnosed chronic myeloid leukemia. Clin Cancer Res. 2010;16(6):1771-1780.
3. Ravandi F. Hairy cell leukemia. Clin Lymphoma Myeloma. 2009;9(suppl 3):S254-S259.
4. 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.
5. Shao YY, Lin CC, Yang CH. Gefitinib or erlotinib in the treatment of advanced non-small cell lung cancer. Discov Med. 2010;9(49):538-545.
6. Wozniak A, Floris G, Debiec-Rychter M, Sciot R, Schoffski P. Implications of mutational analysis for the management of patients with gastrointestinal stromal tumors and the application of targeted therapies. Cancer Invest. 2010;28(8):839-848.
7. Agrawal M, Garg RJ, Kantarjian H, Cortes J. Chronic myeloid leukemia in the tyrosine kinase inhibitor era: what is the "best" therapy? Curr Oncol Rep. 2010;12(5):302-313.
8. Allen M, Louise Jones J. Jekyll and Hyde: the role of the microenvironment on the progression of cancer. J Pathol. 2011;223(2):162-176.
9. La Rosee P, Deininger MW. Resistance to imatinib: mutations and beyond. Semin Hematol. 2010;47(4):335-343.
10. Mani S, Herceg Z. DNA demethylating agents and epigenetic therapy of cancer. Adv Genet. 2010;70:327-340.
11. Vu BT, Vassilev LT. Small-molecule inhibitors of the p53-MDM2 interaction. Curr Top Microbiol Immunol. 2011;348:151-172.
12. Borden EC. Review: Milstein Award lecture: interferons and cancer: where from here? J Interferon Cytokine Res. 2005;25(9):511-527. (Pubitemid 41395839)
13. Borden EC, Wadler S. Interferons as biochemical modulators. J Clin Oncol. 1996;14(10):2627-2630. (Pubitemid 26329645)
14. Potenza L, Volzone F, Riva G, et al. Interferonalpha may restore sensitivity to tyrosine-kinase inhibitors in Philadelphia chromosome positive acute lymphoblastic leukaemia with F317L mutation. Br J Haematol. 2009;146(2):227-230.
15. Pestka S. The interferons: 50 years after their discovery, there is much more to learn. J Biol Chem. 2007;282(28):20047-20051. (Pubitemid 47099975)
16. Platanias LC. Mechanisms of type-I- and type-IIinterferon- mediated signalling. Nat Rev Immunol. 2005;5(5):375-386. (Pubitemid 40685987)
17. Trinchieri G. Type I interferon: friend or foe? J Exp Med. 2010;207(10):2053-2063.
18. Uze G, Monneron D. IL-28 and IL-29: newcomers to the interferon family. Biochimie. 2007;89(6-7): 729-734. (Pubitemid 47001631)
19. Grouard G, Durand I, Filgueira L, Banchereau J, Liu YJ. Dendritic cells capable of stimulating T cells in germinal centres. Nature. 1996; 384(6607):364-367. (Pubitemid 26408519)
20. Samuel CE. Antiviral actions of interferons. Clin Microbiol Rev. 2001;14(4):778-809. (Pubitemid 32979631)
21. Errante PR, Frazao JB, Condino-Neto A. The use of interferon-gamma therapy in chronic granulomatous disease. Recent Pat Antiinfect Drug Discov. 2008;3(3):225-230.
22. Key LL Jr, Rodriguiz RM, Willi SM, et al. Longterm treatment of osteopetrosis with recombinant human interferon gamma. N Engl J Med. 1995; 332(24):1594-1599.
23. de Weerd NA, Samarajiwa SA, Hertzog PJ. Type I interferon receptors: biochemistry and biological functions. J Biol Chem. 2007;282(28): 20053-20057. (Pubitemid 47099976)
24. Decker T, Muller M, Stockinger S. The yin and yang of type I interferon activity in bacterial infection. Nat Rev Immunol. 2005;5(9):675-687. (Pubitemid 43086170)
25. Chawla-Sarkar M, Lindner DJ, Liu YF, et al. Apoptosis and interferons: role of interferonstimulated genes as mediators of apoptosis. Apoptosis. 2003;8(3):237-249. (Pubitemid 36749609)
26. Platanias LC, Uddin S, Bruno E, et al. CrkL and CrkII participate in the generation of the growth inhibitory effects of interferons on primary hematopoietic progenitors. Exp Hematol. 1999;27(8): 1315-1321. (Pubitemid 29347480)
27. Jaks E, Gavutis M, Uze G, Martal J, Piehler J. Differential receptor subunit affinities of type I interferons govern differential signal activation. J Mol Biol. 2007;366(2):525-539. (Pubitemid 46136210)
28. Biron CA. Interferons alpha and beta as immune regulators - a new look. Immunity. 2001;14(6): 661-664. (Pubitemid 32592413)
29. Tamura T, Yanai H, Savitsky D, Taniguchi T. The IRF family transcription factors in immunity and oncogenesis. Annu Rev Immunol. 2008;26:535-584. (Pubitemid 351600385)
30. Paquette RL, Hsu N, Said J, et al. Interferonalpha induces dendritic cell differentiation of CML mononuclear cells in vitro and in vivo. Leukemia. 2002;16(8):1484-1489.
31. 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.
32. Burchert A, Muller MC, Kostrewa P, et al. Sustained molecular response with interferon alfa maintenance after induction therapy with imatinib plus interferon alfa in patients with chronic myeloid leukemia. J Clin Oncol. 2010;28(8):1429-1435.
33. Kanodia S, Wieder E, Lu S, et al. PR1-specific T cells are associated with unmaintained cytogenetic remission of chronic myelogenous leukemia after interferon withdrawal. PLoS ONE. 2010; 5(7):e11770.
34. Seggewiss R, Price DA, Purbhoo MA. Immunomodulatory effects of imatinib and secondgeneration tyrosine kinase inhibitors on T cells and dendritic cells: an update. Cytotherapy. 2008; 10(6):633-641.
35. Chen X, Regn S, Raffegerst S, Kolb HJ, Roskrow M. Interferon alpha in combination with GM-CSF induces the differentiation of leukaemic antigen-presenting cells that have the capacity to stimulate a specific anti-leukaemic cytotoxic T-cell response from patients with chronic myeloid leukaemia. Br J Haematol. 2000;111(2):596-607.
36. Molldrem J, Dermime S, Parker K, et al. Targeted T-cell therapy for human leukemia: cytotoxic T lymphocytes specific for a peptide derived from proteinase 3 preferentially lyse human myeloid leukemia cells. Blood. 1996;88(7):2450-2457. (Pubitemid 26327493)
37. Molldrem JJ, Lee PP, Kant S, et al. Chronic myelogenous leukemia shapes host immunity by selective deletion of high-avidity leukemia-specific T cells. J Clin Invest. 2003;111(5):639-647. (Pubitemid 36278582)
38. Molldrem JJ, Lee PP, Wang C, et al. Evidence that specific T lymphocytes may participate in the elimination of chronic myelogenous leukemia. Nat Med. 2000;6(9):1018-1023.
39. Burchert A, Neubauer A. Interferon alpha and T-cell responses in chronic myeloid leukemia. Leuk Lymphoma. 2005;46(2):167-175. (Pubitemid 40185945)
40. Palandri F, Iacobucci I, Castagnetti F, et al. Frontline treatment of Philadelphia positive chronic myeloid leukemia with imatinib and interferon-alpha: 5-year outcome. Haematologica. 2008;93(5):770-774. (Pubitemid 351669320)
41. Preudhomme C, Guilhot J, Nicolini FE, et al. Imatinib plus peginterferon alfa-2a in chronic myeloid leukemia. N Engl J Med. 2010;363(26):2511-2521.
42. Xiong Z, Liu E, Yan Y, et al. An unconventional antigen translated by a novel internal ribosome entry site elicits antitumor humoral immune reactions. J Immunol. 2006;177(7):4907-4916. (Pubitemid 44469827)
43. Xiong Z, Yan Y, Liu E, et al. Novel tumor antigens elicit anti-tumor humoral immune reactions in a subset of patients with polycythemia vera. Clin Immunol. 2007;122(3):279-287. (Pubitemid 46216913)
44. Le Bon A, Schiavoni G, D'Agostino G, Gresser I, Belardelli F, Tough DF. Type i interferons potently enhance humoral immunity and can promote isotype switching by stimulating dendritic cells in vivo. Immunity. 2001;14(4):461-470. (Pubitemid 32441598)
45. Kiladjian JJ, Cassinat B, Turlure P, et al. High molecular response rate of polycythemia vera patients treated with pegylated interferon alpha-2a. Blood. 2006;108(6):2037-2040. (Pubitemid 44395018)
46. Quintas-Cardama A, Kantarjian H, Manshouri T, 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(32):5418-5424.
47. Bekisz J, Baron S, Balinsky C, Morrow A, Zoon KC. Antiproliferative properties of type I and type II interferon. Pharmaceuticals (Basel). 2010;3(4): 994-1015.
48. Indraccolo S. Interferon-alpha as angiogenesis inhibitor: learning from tumor models. Autoimmunity. 2010;43(3):244-247.
49. Lu M, Zhang W, Li Y, et al. Interferon-alpha targets JAK2V617F-positive hematopoietic progenitor cells and acts through the p38 MAPK pathway. Exp Hematol. 2010;38(6):472-480.
50. Mayer IA, Verma A, Grumbach IM, et al. The p38 MAPK pathway mediates the growth inhibitory effects of interferon-alpha in BCR-ABL-expressing cells. J Biol Chem. 2001;276(30): 28570-28577.
51. Raefsky EL, Platanias LC, Zoumbos NC, Young NS. Studies of interferon as a regulator of hematopoietic cell proliferation. J Immunol. 1985; 135(4):2507-2512. (Pubitemid 16215841)
52. Ito K, Tanaka H, Ito T, et al. Initial expression of interferon alpha receptor 2 (IFNAR2) on CD34- positive cells and its down-regulation correlate with clinical response to interferon therapy in chronic myelogenous leukemia. Eur J Haematol. 2004;73(3):191-205. (Pubitemid 39062243)
53. Aman MJ, Bug G, Aulitzky WE, Huber C, Peschel C. Inhibition of interleukin-11 by interferon-alpha in human bone marrow stromal cells. Exp Hematol. 1996;24(8):863-867. (Pubitemid 26255100)
54. Aman MJ, Keller U, Derigs G, Mohamadzadeh M, Huber C, Peschel C. Regulation of cytokine expression by interferon-alpha in human bone marrow stromal cells: inhibition of hematopoietic growth factors and induction of interleukin-1 receptor antagonist. Blood. 1994;84(12):4142-4150. (Pubitemid 24371916)
55. Grace MJ, Cutler DL, Bordens RW. Pegylated IFNs for chronic hepatitis C: an update. Expert Opin Drug Deliv. 2005;2(2):219-226. (Pubitemid 41130879)
56. Drachman JG, Sabath DF, Fox NE, Kaushansky K. Thrombopoietin signal transduction in purified murine megakaryocytes. Blood. 1997;89(2):483-492. (Pubitemid 27051683)
57. Wang Q, Miyakawa Y, Fox N, Kaushansky K. Interferon-alpha directly represses megakaryopoiesis by inhibiting thrombopoietin-induced signaling through induction of SOCS-1. Blood. 2000; 96(6):2093-2099.
58. 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.
59. Ludwig H, Cortelezzi A, Van Camp BG, et al. Treatment with recombinant interferon-alpha-2C: multiple myeloma and thrombocythaemia in myeloproliferative diseases. Oncology. 1985; 42(suppl 1):19-25. (Pubitemid 16208173)
60. Joshi S, Kaur S, Redig AJ, et al. Type I interferon (IFN)-dependent activation of Mnk1 and its role in the generation of growth inhibitory responses. Proc Natl Acad Sci U S A. 2009;106(29):12097-12102.
61. Katsoulidis E, Carayol N, Woodard J, et al. Role of Schlafen 2 (SLFN2) in the generation of interferon alpha-induced growth inhibitory responses. J Biol Chem. 2009;284(37):25051-25064.
62. Katsoulidis E, Li Y, Yoon P, et al. Role of the p38 mitogen-activated protein kinase pathway in cytokine-mediated hematopoietic suppression in myelodysplastic syndromes. Cancer Res. 2005; 65(19):9029-9037. (Pubitemid 41377395)
63. Kim BJ, Ryu SW, Song BJ. JNK- and p38 kinase-mediated phosphorylation of Bax leads to its activation and mitochondrial translocation and to apoptosis of human hepatoma HepG2 cells. J Biol Chem. 2006;281(30):21256-21265.
64. Lee WH, Liu FH, Lee YL, Huang HM. Interferonalpha induces the growth inhibition of human T-cell leukaemia line Jurkat through p38alpha and p38beta. J Biochem. 2010;147(5):645-650.
65. Uddin S, Lekmine F, Sharma N, et al. The Rac1/ p38 mitogen-activated protein kinase pathway is required for interferon alpha-dependent transcriptional activation but not serine phosphorylation of Stat proteins. J Biol Chem. 2000;275(36):27634-27640.
66. Essers MA, Offner S, Blanco-Bose WE, et al. IFNalpha activates dormant haematopoietic stem cells in vivo. Nature. 2009;458(7240):904-908.
67. 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.
68. Baldridge MT, King KY, Boles NC, Weksberg DC, Goodell MA. Quiescent haematopoietic stem cells are activated by IFN-gamma in response to chronic infection. Nature. 2010;465(7299):793-797.
69. Trumpp A, Essers M, Wilson A. Awakening dormant haematopoietic stem cells. Nat Rev Immunol. 2010;10(3):201-209.
70. Graham SM, Jorgensen HG, Allan E, et al. Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. Blood. 2002;99(1): 319-325.
71. Druker BJ, Talpaz M, Resta DJ, et al. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med. 2001;344(14):1031-1037. (Pubitemid 32267972)
72. Salmon SE, Crowley JJ, Grogan TM, Finley P, Pugh RP, Barlogie B. Combination chemotherapy, glucocorticoids, and interferon alfa in the treatment of multiple myeloma: a Southwest Oncology Group study. J Clin Oncol. 1994;12(11): 2405-2414. (Pubitemid 24346714)
73. Quesada JR, Alexanian R, Hawkins M, et al. Treatment of multiple myeloma with recombinant alpha-interferon. Blood. 1986;67(2):275-278. (Pubitemid 16164636)
74. Golomb HM, Jacobs A, Fefer A, et al. Alpha-2 interferon therapy of hairy-cell leukemia: a multicenter study of 64 patients. J Clin Oncol. 1986; 4(6):900-905. (Pubitemid 16080943)
75. Kluin-Nelemans HC, Jansen JH, Breukelman H, et al. Response to interferon alfa-2b in a patient with systemic mastocytosis. N Engl J Med. 1992; 326(9):619-623.
76. Lim KH, Pardanani A, Butterfield JH, Li CY, Tefferi A. Cytoreductive therapy in 108 adults with systemic mastocytosis: outcome analysis and response prediction during treatment with interferon-alpha, hydroxyurea, imatinib mesylate or 2-chlorodeoxyadenosine. Am J Hematol. 2009; 84(12):790-794.
77. Rousselot P, Huguet F, Vey N, et al. Maintenance therapy by Glivec(R) and Pegasys(R) in patients with Philadelphia positive acute lymphocytic leukemia not eligible for hematopoietic stem cell transplantation [abstract]. Blood (ASH Annual Meeting Abstracts). 2007;110(11): Abstract 2812.
78. 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.
79. Cools J, DeAngelo DJ, Gotlib J, et al. A tyrosine kinase created by fusion of the PDGFRA and FIP1L1 genes as a therapeutic target of imatinib in idiopathic hypereosinophilic syndrome. N Engl J Med. 2003;348(13):1201-1214. (Pubitemid 36359296)
80. Interferon alfa-2a as compared with conventional chemotherapy for the treatment of chronic myeloid leukemia: the Italian Cooperative Study Group on Chronic Myeloid Leukemia. N Engl J Med. 1994;330(12):820-825.
81. O'Brien SG, Guilhot F, Larson RA, et al. Imatinib compared with interferon and low-dose cytarabine for newly diagnosed chronic-phase chronic myeloid leukemia. N Engl J Med. 2003;348(11): 994-1004. (Pubitemid 36302244)
82. Talpaz M, Shah NP, Kantarjian H, et al. Dasatinib in imatinib-resistant Philadelphia chromosomepositive leukemias. N Engl J Med. 2006;354(24): 2531-2541. (Pubitemid 43882349)
83. Kantarjian H, Giles F, Wunderle L, et al. Nilotinib in imatinib-resistant CML and Philadelphia chromosome-positive ALL. N Engl J Med. 2006; 354(24):2542-2551. (Pubitemid 43882350)
84. Hochhaus A, O'Brien SG, Guilhot F, et al. Sixyear follow-up of patients receiving imatinib for the first-line treatment of chronic myeloid leukemia. Leukemia. 2009;23(6):1054-1061.
85. Saglio G, Kim DW, Issaragrisil S, et al. Nilotinib versus imatinib for newly diagnosed chronic myeloid leukemia. N Engl J Med. 2010;362(24): 2251-2259.
86. Mahon FX, Rea D, Guilhot J, et al. Discontinuation of imatinib in patients with chronic myeloid leukaemia who have maintained complete molecular remission for at least 2 years: the prospective, multicentre Stop Imatinib (STIM) trial. Lancet Oncol. 2010;11(11):1029-1035.
87. Saglio G, Kim D-W, Issaragrisil S, et al. Nilotinib demonstrates superior efficacy compared with imatinib in patients with newly diagnosed chronic myeloid leukemia in chronic phase: results from the International Randomized Phase III ENESTnd Trial [abstract]. Blood (ASH Annual Meeting Abstracts). 2009;114(22):LBA-1.
88. Visani G, Piccaluga P, Malagola M, Isidori A. Efficacy of dasatinib in conjunction with alphainterferon for the treatment of imatinib-resistant and dasatinib-resistant Ph+ acute lymphoblastic leukemia. Leukemia. 2009;23(9):1687-1688.
89. Pye SM, Cortes J, Ault P, et al. The effects of imatinib on pregnancy outcome. Blood. 2008; 111(12):5505-5508.
90. Apperley J. Issues of imatinib and pregnancy outcome. J Natl Compr Canc Netw. 2009;7(10): 1050-1058.
91. Griesshammer M, Struve S, Barbui T. Management of Philadelphia negative chronic myeloproliferative disorders in pregnancy. Blood Rev. 2008;22(5):235-245.
92. Kiladjian JJ, Chomienne C, Fenaux P. Interferonalpha therapy in bcr-abl-negative myeloproliferative neoplasms. Leukemia. 2008;22(11):1990-1998.
93. Vardiman JW, Thiele J, Arber DA, et al. The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: rationale and important changes. Blood. 2009;114(5):937-951.
94. Pardanani A, Ketterling RP, Brockman SR, et al. CHIC2 deletion, a surrogate for FIP1L1-PDGFRA fusion, occurs in systemic mastocytosis associated with eosinophilia and predicts response to imatinib mesylate therapy. Blood. 2003;102(9): 3093-3096. (Pubitemid 37314742)
95. Butterfield JH, Gleich GJ. Interferon-alpha treatment of six patients with the idiopathic hypereosinophilic syndrome. Ann Intern Med. 1994;121(9): 648-653.
96. Ceretelli S, Capochiani E, Petrini M. Interferonalpha in the idiopathic hypereosinophilic syndrome: consideration of five cases. Ann Hematol. 1998;77(4):161-164. (Pubitemid 28499837)
97. Silver RT. Recombinant interferon-alpha for treatment of polycythaemia vera. Lancet. 1988; 2(8607):403.
98. Bellucci S, Harousseau JL, Brice P, Tobelem G. Treatment of essential thrombocythaemia by alpha 2a interferon. Lancet. 1988;2(8617):960-961.
99. Hasselbalch HC, Larsen TS, Riley CH, Jensen MK, Kiladjian JJ. Interferon Alpha in the treatment of Philadelphia-negative chronic myeloproliferative neoplasms: status and perspectives. Curr Drug Targets. 2011;12(3):392-419.
100. Barosi G, Birgegard G, Finazzi G, et al. Response criteria for essential thrombocythemia and polycythemia vera: result of a European LeukemiaNet consensus conference. Blood. 2009;113(20):4829-4833.
101. Barosi G, Liberato LN, Costa A, Ascari E. Cytoreductive effect of recombinant alpha interferon in patients with myelofibrosis with myeloid metaplasia. Blut. 1989;58(6):271-274. (Pubitemid 19162782)
102. Ianotto JC, Kiladjian JJ, Demory JL, et al. PEGIFN- alpha-2a therapy in patients with myelofibrosis: a study of the French Groupe d'Etudes des Myelofibroses (GEM) and France Intergroupe des syndromes Myeloproliferatifs (FIM). Br J Haematol. 2009;146(2):223-225.
103. Hino M, Futami E, Okuno S, Miki T, Nishizawa Y, Morii H. Possible selective effects of interferon alpha-2b on a malignant clone in a case of polycythemia vera. Ann Hematol. 1993;66(3):161-162. (Pubitemid 23104737)
104. Liu E, Jelinek J, Pastore YD, Guan Y, Prchal JF, Prchal JT. Discrimination of polycythemias and thrombocytoses by novel, simple, accurate clonality assays and comparison with PRV-1 expression and BFU-E response to erythropoietin. Blood. 2003;101(8):3294-3301. (Pubitemid 36858027)
105. Massaro P, Foa P, Pomati M, et al. Polycythemia vera treated with recombinant interferon-alpha 2a: evidence of a selective effect on the malignant clone. Am J Hematol. 1997;56(2):126-128. (Pubitemid 27448844)
106. Messora C, Bensi L, Vecchi A, et al. Cytogenetic conversion in a case of polycythaemia vera treated with interferon-alpha. Br J Haematol. 1994;86(2):402-404. (Pubitemid 24199014)
107. Larsen TS, Moller MB, de Stricker K, et al. Minimal residual disease and normalization of the bone marrow after long-term treatment with alpha- interferon2b in polycythemia vera: a report on molecular response patterns in seven patients in sustained complete hematological remission. Hematology. 2009;14(6):331-334.
108. Gilbert HS. Long term treatment of myeloproliferative disease with interferon-alpha-2b: feasibility and efficacy. Cancer. 1998;83(6):1205-1213. (Pubitemid 28419075)
109. Ishii T, Xu M, Zhao Y, et al. Recurrence of clonal hematopoiesis after discontinuing pegylated recombinant interferon-alpha 2a in a patient with polycythemia vera. Leukemia. 2007;21(2):373-374. (Pubitemid 46158140)
110. Kiladjian JJ, Masse A, Cassinat B, et al. 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.
111. Silver RT, Vandris K. Recombinant interferon alpha (rIFN alpha-2b) may retard progression of early primary myelofibrosis. Leukemia. 2009; 23(7):1366-1369.
112. Lengfelder E, Berger U, Hehlmann R. Interferon alpha in the treatment of polycythemia vera. Ann Hematol. 2000;79(3):103-109. (Pubitemid 30195605)
113. Silver RT. Long-term effects of the treatment of polycythemia vera with recombinant interferonalpha. Cancer. 2006;107(3):451-458. (Pubitemid 44107203)
114. Marchioli R, Finazzi G, Landolfi R, et al. Vascular and neoplastic risk in a large cohort of patients with polycythemia vera. J Clin Oncol. 2005; 23(10):2224-2232. (Pubitemid 46218714)
115. McMullin MF, Bareford D, Campbell P, et al. Guidelines for the diagnosis, investigation and management of polycythaemia/erythrocytosis. Br J Haematol. 2005;130(2):174-195. (Pubitemid 41602518)
116. Barbui T, Barosi G, Grossi A, et al. Practice guidelines for the therapy of essential thrombocythemia. A statement from the Italian Society of Hematology, the Italian Society of Experimental Hematology and the Italian Group for Bone Marrow Transplantation. Haematologica. 2004;89(2): 215-232.
117. Barbui T, Barosi G, Birgegard G, et al. Philadelphia- negative classical myeloproliferative neoplasms: critical concepts and management recommendations from European LeukemiaNet. J Clin Oncol. 2011;29(6):761-770.
118. Finazzi G, Caruso V, Marchioli R, et al. Acute leukemia in polycythemia vera: an analysis of 1638 patients enrolled in a prospective observational study. Blood. 2005;105(7):2664-2670. (Pubitemid 40446255)
119. Kiladjian JJ, Rain JD, Bernard JF, Briere J, Chomienne C, Fenaux P. Long-term incidence of hematological evolution in three French prospective studies of hydroxyurea and pipobroman in polycythemia vera and essential thrombocythemia. Semin Thromb Hemost. 2006;32(4 Pt 2): 417-421.