The past and future of CD33 as therapeutic target in acute myeloid leukemia

Blood Reviews

Volumn 28, Issue 4, 2014, Pages 143-153

  Laszlo, George S ^a   Estey, Elihu H ^a,b   Walter, Roland B ^a,b  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Acute myeloid leukemia; Antibody; Antibody drug conjugate; Bispecific antibody; BiTE; CD33; Chimeric antigen receptor; Gemtuzumab ozogamicin; Immunotherapy; Radioimmunoconjugate

Indexed keywords

ANTIBODY CONJUGATE; AVE 9633; CD33 ANTIGEN; GEMTUZUMAB OZOGAMICIN; LINTUZUMAB; LYMPHOCYTE ANTIGEN RECEPTOR; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 33.1; RECOMBINANT GELONIN; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT;

ACUTE GRANULOCYTIC LEUKEMIA; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER MORTALITY; CANCER SURVIVAL; DRUG EFFICACY; DRUG TARGETING; HEMATOPOIETIC CELL; HUMAN; LEUKEMIA CELL; LIVER VENOOCCLUSIVE DISEASE; MORBIDITY; NEUTROPENIA; PRIORITY JOURNAL; REVIEW; STEM CELL; THROMBOCYTOPENIA; ANIMAL; ANTAGONISTS AND INHIBITORS; CLINICAL TRIAL (TOPIC); IMMUNOTHERAPY; LEUKEMIA, MYELOID, ACUTE; METABOLISM; MOLECULARLY TARGETED THERAPY;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; CLINICAL TRIALS AS TOPIC; HUMANS; IMMUNOCONJUGATES; IMMUNOTHERAPY; LEUKEMIA, MYELOID, ACUTE; MOLECULAR TARGETED THERAPY; SIALIC ACID BINDING IG-LIKE LECTIN 3;

EID: 84903122676     PISSN: 0268960X     EISSN: 15321681     Source Type: Journal    
DOI: 10.1016/j.blre.2014.04.001     Document Type: Article

References (165)

1. Weiner L.M., Surana R., Wang S. Monoclonal antibodies: versatile platforms for cancer immunotherapy. Nat Rev Immunol 2010, 10:317-327.
2. Sliwkowski M.X., Mellman I. Antibody therapeutics in cancer. Science 2013, 341:1192-1198.
3. Bross P.F., Beitz J., Chen G., Chen X.H., Duffy E., Kieffer L., et al. Approval summary: gemtuzumab ozogamicin in relapsed acute myeloid leukemia. Clin Cancer Res 2001, 7:1490-1496.
4. Varki A., Angata T. Siglecs-the major subfamily of I-type lectins. Glycobiology 2006, 16:1R-27R.
5. Crocker P.R., Paulson J.C., Varki A. Siglecs and their roles in the immune system. Nat Rev Immunol 2007, 7:255-266.
6. Simmons D., Seed B. Isolation of a cDNA encoding CD33, a differentiation antigen of myeloid progenitor cells. J Immunol 1988, 141:2797-2800.
7. Freeman S.D., Kelm S., Barber E.K., Crocker P.R. Characterization of CD33 as a new member of the sialoadhesin family of cellular interaction molecules. Blood 1995, 85:2005-2012.
8. Yousef G.M., Ordon M.H., Foussias G., Diamandis E.P. Genomic organization of the siglec gene locus on chromosome 19q13.4 and cloning of two new siglec pseudogenes. Gene 2002, 286:259-270.
9. Hernández-Caselles T., Martínez-Esparza M., Pérez-Oliva A.B., Quintanilla-Cecconi A.M., García-Alonso A., Alvarez-López D.M., et al. A study of CD33 (SIGLEC-3) antigen expression and function on activated human T and NK cells: two isoforms of CD33 are generated by alternative splicing. J Leukoc Biol 2006, 79:46-58.
10. Pérez-Oliva A.B., Martínez-Esparza M., Vicente-Fernández J.J., Corral-San Miguel R., García-Peñarrubia P., Hernández-Caselles T. Epitope mapping, expression and post-translational modifications of two isoforms of CD33 (CD33M and CD33m) on lymphoid and myeloid human cells. Glycobiology 2011, 21:757-770.
11. Taylor V.C., Buckley C.D., Douglas M., Cody A.J., Simmons D.L., Freeman S.D. The myeloid-specific sialic acid-binding receptor, CD33, associates with the protein-tyrosine phosphatases, SHP-1 and SHP-2. J Biol Chem 1999, 274:11505-11512.
12. Ulyanova T., Blasioli J., Woodford-Thomas T.A., Thomas M.L. The sialoadhesin CD33 is a myeloid-specific inhibitory receptor. Eur J Immunol 1999, 29:3440-3449.
13. Paul S.P., Taylor L.S., Stansbury E.K., McVicar D.W. Myeloid specific human CD33 is an inhibitory receptor with differential ITIM function in recruiting the phosphatases SHP-1 and SHP-2. Blood 2000, 96:483-490.
14. Orr S.J., Morgan N.M., Elliott J., Burrows J.F., Scott C.J., McVicar D.W., et al. CD33 responses are blocked by SOCS3 through accelerated proteasomal-mediated turnover. Blood 2007, 109:1061-1068.
15. Jilani I., Estey E., Huh Y., Joe Y., Manshouri T., Yared M., et al. Differences in CD33 intensity between various myeloid neoplasms. Am J Clin Pathol 2002, 118:560-566.
16. Andrews R.G., Torok-Storb B., Bernstein I.D. Myeloid-associated differentiation antigens on stem cells and their progeny identified by monoclonal antibodies. Blood 1983, 62:124-132.
17. Griffin J.D., Linch D., Sabbath K., Larcom P., Schlossman S.F. A monoclonal antibody reactive with normal and leukemic human myeloid progenitor cells. Leuk Res 1984, 8:521-534.
18. Andrews R.G., Takahashi M., Segal G.M., Powell J.S., Bernstein I.D., Singer J.W. The L4F3 antigen is expressed by unipotent and multipotent colony-forming cells but not by their precursors. Blood 1986, 68:1030-1035.
19. Andrews R.G., Singer J.W., Bernstein I.D. Precursors of colony-forming cells in humans can be distinguished from colony-forming cells by expression of the CD33 and CD34 antigens and light scatter properties. J Exp Med 1989, 169:1721-1731.
20. Tanimoto M., Scheinberg D.A., Cordon-Cardo C., Huie D., Clarkson B.D., Old L.J. Restricted expression of an early myeloid and monocytic cell surface antigen defined by monoclonal antibody M195. Leukemia 1989, 3:339-348.
21. Handgretinger R., Schafer H.J., Baur F., Frank D., Ottenlinger C., Buhring H.J., et al. Expression of an early myelopoietic antigen (CD33) on a subset of human umbilical cord blood-derived natural killer cells. Immunol Lett 1993, 37:223-228.
22. Nakamura Y., Noma M., Kidokoro M., Kobayashi N., Takei M., Kurashima S., et al. Expression of CD33 antigen on normal human activated T lymphocytes. Blood 1994, 83:1442-1443.
23. Schmidt-Wolf I.G., Grimm B., Lefterova P., Johnston V., Scheffold C., Huhn D., et al. Propagation of large numbers of cells of a human mixed-lineage T-lymphoid/myeloid. Br J Haematol 1995, 90:512-517.
24. Márquez C., Trigueros C., Franco J.M., Ramiro A.R., Carrasco Y.R., López-Botet M., et al. Identification of a common developmental pathway for thymic natural killer cells and dendritic cells. Blood 1998, 91:2760-2771.
25. Dworzak M.N., Fritsch G., Fröschl G., Printz D., Gadner H. Four-color flow cytometric investigation of terminal deoxynucleotidyl transferase-positive lymphoid precursors in pediatric bone marrow: CD79a expression precedes CD19 in early B-cell ontogeny. Blood 1998, 92:3203-3209.
26. Eksioglu-Demiralp E., Kibaroglu A., Direskeneli H., Yavuz S., Karsli F., Yurdakul S., et al. Phenotypic characteristics of B cells in Behcet's disease: increased activity in B cell subsets. J Rheumatol 1999, 26:826-832.
27. Eissens D.N., Spanholtz J., van der Meer A., van Cranenbroek B., Dolstra H., Kwekkeboom J., et al. Defining early human NK cell developmental stages in primary and secondary lymphoid tissues. PLoS One 2012, 7(2):e30930. (Epub 2012 Feb 3.). 10.1371/journal.pone.0030930.
28. La Russa V.F., Griffin J.D., Kessler S.W., Cutting M.A., Knight R.D., Blattler W.A., et al. Effects of anti-CD33 blocked ricin immunotoxin on the capacity of CD34+ human marrow cells to establish in vitro hematopoiesis in long-term marrow cultures. Exp Hematol 1992, 20:442-448.
29. Bernstein I.D., Andrews R.G., Berenson R., Bensinger W., Singer J.W., Buckner C.D. Isolation of human hematopoietic stem cells. New Strategies in Bone Marrow Transplantation 1991, 201-207. Wiley-Liss, New York. R.E. Champlin, R.P. Gale (Eds.).
30. Robertson M.J., Soiffer R.J., Freedman A.S., Rabinowe S.L., Anderson K.C., Ervin T.J., et al. Human bone marrow depleted of CD33-positive cells mediates delayed but durable reconstitution of hematopoiesis: clinical trial of MY9 monoclonal antibody-purged autografts for the treatment of acute myeloid leukemia. Blood 1992, 79:2229-2236.
31. Cao H., Crocker P.R. Evolution of CD33-related siglecs: regulating host immune functions and escaping pathogen exploitation?. Immunology 2011, 132:18-26.
32. Crocker P.R., McMillan S.J., Richards H.E. CD33-related siglecs as potential modulators of inflammatory responses. Ann N Y Acad Sci 2012, 1253:102-111.
33. Lajaunias F., Dayer J.M., Chizzolini C. Constitutive repressor activity of CD33 on human monocytes requires sialic acid recognition and phosphoinositide 3-kinase-mediated intracellular signaling. Eur J Immunol 2005, 35:243-251.
34. Sutherland M.S.K., Lewis T.S., Yu C., McEarchern J.A., Drachman J.G., Sievers E.L., et al. SGN-33 modulates cytokine and chemokine production by activated monocytes and macrophages [abstract]. Blood 2006, 108:564. [amul].
35. Scheinberg D.A., Lovett D., Divgi C.R., Graham M.C., Berman E., Pentlow K., et al. A phase I trial of monoclonal antibody M195 in acute myelogenous leukemia: specific bone marrow targeting and internalization of radionuclide. J Clin Oncol 1991, 9:478-490.
36. Caron P.C., Co M.S., Bull M.K., Avdalovic N.M., Queen C., Scheinberg D.A. Biological and immunological features of humanized M195 (anti-CD33) monoclonal antibodies. Cancer Res 1992, 52:6761-6767.
37. van der Jagt R.H.C., Badger C.C., Appelbaum F.R., Press O.W., Matthews D.C., Eary J.F., et al. Localization of radiolabeled antimyeloid antibodies in a human acute leukemia xenograft tumor model. Cancer Res 1992, 52:89-94.
38. Audran R., Drenou B., Wittke F., Gaudin A., Lesimple T., Toujas L. Internalization of human macrophage surface antigens induced by monoclonal antibodies. J Immunol Methods 1995, 188:147-154.
39. Press O.W., Shan D., Howell-Clark J., Eary J., Appelbaum F.R., Matthews D., et al. Comparative metabolism and retention of iodine-125, yttrium-90, and indium-111 radioimmunoconjugates by cancer cells. Cancer Res 1996, 56:2123-2129.
40. van der Velden V.H.J., te Marvelde J.G., Hoogeveen P.G., Bernstein I.D., Houtsmuller A.B., Berger A.S., et al. Targeting of the CD33-calicheamicin immunoconjugate Mylotarg (CMA-676) in acute myeloid leukemia: in vivo and in vitro saturation and internalization by leukemic and normal myeloid cells. Blood 2001, 97:3197-3204.
41. Walter R.B., Raden B.W., Kamikura D.M., Cooper J.A., Bernstein I.D. Influence of CD33 expression levels and ITIM-dependent internalization on gemtuzumab ozogamicin-induced cytotoxicity. Blood 2005, 105:1295-1302.
42. Walter R.B., Raden B.W., Zeng R., Häusermann P., Bernstein I.D., Cooper J.A. ITIM-dependent endocytosis of CD33-related Siglecs: role of intracellular domain, tyrosine phosphorylation, and the tyrosine phosphatases, Shp1 and Shp2. J Leukoc Biol 2008, 83:200-211.
43. Walter R.B., Häusermann P., Raden B.W., Teckchandani A.M., Kamikura D.M., Bernstein I.D., et al. Phosphorylated ITIMs enable ubiquitylation of an inhibitory cell surface receptor. Traffic 2008, 9:267-279.
44. Laszlo G.S., Gudgeon C.J., Harrington K.H., Dell'Aringa J., Newhall K.J., Means G.D., et al. Cellular determinants for preclinical activity of a novel CD33/CD3 bispecific T-cell engager (BiTE) antibody, AMG 330, against human AML. Blood 2014, 123:554-561.
45. Pollard J.A., Alonzo T.A., Loken M., Gerbing R.B., Ho P.A., Bernstein I.D., et al. Correlation of CD33 expression level with disease characteristics and response to gemtuzumab ozogamicin containing chemotherapy in childhood AML. Blood 2012, 119:3705-3711.
46. Krupka C., Kufer P., Kischel R., Zugmaier G., Bögeholz J., Köhnke T., et al. CD33 target validation and sustained depletion of AML blasts in long-term cultures by the bispecific T-cell-engaging antibody AMG 330. Blood 2014, 123:356-365.
47. Scheinberg D.A., Tanimoto M., McKenzie S., Strife A., Old L.J., Clarkson B.D. Monoclonal antibody M195: a diagnostic marker for acute myelogenous leukemia. Leukemia 1989, 3:440-445.
48. Hauswirth A.W., Florian S., Printz D., Sotlar K., Krauth M.T., Fritsch G., et al. Expression of the target receptor CD33 in CD34+/CD38-/CD123+ AML stem cells. Eur. J. Clin. Investig. 2007, 37:73-82.
49. Guglielmi C., Martelli M.P., Diverio D., Fenu S., Vegna M.L., Cantu-Rajnoldi A., et al. Immunophenotype of adult and childhood acute promyelocytic leukaemia: correlation with morphology, type of PML gene breakpoint and clinical outcome. A cooperative Italian study on 196 cases. Br J Haematol 1998, 102:1035-1041.
50. Paietta E. Expression of cell-surface antigens in acute promyelocytic leukaemia. Best Pract Res Clin Haematol 2003, 16:369-385.
51. De Propris M.S., Raponi S., Diverio D., Milani M.L., Meloni G., Falini B., et al. High CD33 expression levels in acute myeloid leukemia cells carrying the nucleophosmin (NPM1) mutation. Haematologica 2011, 96:1548-1551.
52. Dinndorf P.A., Buckley J.D., Nesbit M.E., Lampkin B.C., Piomelli S., Feig S.A., et al. Expression of myeloid differentiation antigens in acute nonlymphocytic leukemia: increased concentration of CD33 antigen predicts poor outcome-a report from the Children's Cancer Study Group. Med Pediatr Oncol 1992, 20:192-200.
53. Pollard J., Alonzo T.A., Gerbing R.B., Raimondi S.C., Hirsch B., Aplenc R., et al. Negative prognostic impact of high CD33 expression is negated with the use of gemtuzumab ozogamicin: a report from the Children's Oncology Group [abstract]. Blood 2013, 122:491.
54. Biedermann B., Gil D., Bowen D.T., Crocker P.R. Analysis of the CD33-related siglec family reveals that Siglec-9 is an endocytic receptor expressed on subsets of acute myeloid leukemia cells and absent from normal hematopoietic progenitors. Leuk Res 2007, 31:211-220.
55. Abdool A., Yeh C.H., Kantarjian H., O'Brien S., Bruey J., Giles F., et al. Circulating CD33 and its clinical value in acute leukemia. Exp Hematol 2010, 38:462-471.
56. Friedrich M., Henn A., Raum T., Bajtus M., Matthes K., Hendrich L., et al. Preclinical characterization of AMG 330, a CD3/CD33-bispecific T-cell-engaging antibody with potential for treatment of acute myelogenous leukemia. Mol Cancer Ther 2014, (Epub ahead of print). 10.1158/1535-7163.MCT-13-0956.
57. Bernstein I.D. Monoclonal antibodies to the myeloid stem cells: therapeutic implications of CMA-676, a humanized anti-CD33 antibody calicheamicin conjugate. Leukemia 2000, 14:474-475.
58. Walter R.B., Appelbaum F.R., Estey E.H., Bernstein I.D. Acute myeloid leukemia stem cells and CD33-targeted immunotherapy. Blood 2012, 119:6198-6208.
59. Fialkow P.J., Singer J.W., Adamson J.W., Vaidya K., Dow L.W., Ochs J., et al. Acute nonlymphocytic leukemia: heterogeneity of stem cell origin. Blood 1981, 57:1068-1073.
60. Fialkow P.J., Singer J.W., Raskind W.H., Adamson J.W., Jacobson R.J., Bernstein I.D., et al. Clonal development, stem-cell differentiation, and clinical remissions in acute nonlymphocytic leukemia. N Engl J Med 1987, 317:468-473.
61. Bernstein I.D., Singer J.W., Andrews R.G., Keating A., Powell J.S., Bjornson B.H., et al. Treatment of acute myeloid leukemia cells in vitro with a monoclonal antibody recognizing a myeloid differentiation antigen allows normal progenitor cells to be expressed. J Clin Invest 1987, 79:1153-1159.
62. Bernstein I.D., Singer J.W., Smith F.O., Andrews R.G., Flowers D.A., Petersens J., et al. Differences in the frequency of normal and clonal precursors of colony-forming cells in chronic myelogenous leukemia and acute myelogenous leukemia. Blood 1992, 79:1811-1816.
63. Taussig D.C., Pearce D.J., Simpson C., Rohatiner A.Z., Lister T.A., Kelly G., et al. Hematopoietic stem cells express multiple myeloid markers: implications for the origin and targeted therapy of acute myeloid leukemia. Blood 2005, 106:4086-4092.
64. Mejstríková E., Kalina T., Trka J., Starý J., Hrusák O. Correlation of CD33 with poorer prognosis in childhood ALL implicates a potential of anti-CD33 frontline therapy. Leukemia 2005, 19:1092-1094.
65. Schwartz M.A., Lovett D.R., Redner A., Finn R.D., Graham M.C., Divgi C.R., et al. Dose-escalation trial of M195 labeled with iodine 131 for cytoreduction and marrow ablation in relapsed or refractory myeloid leukemias. J Clin Oncol 1993, 11:294-303.
66. Jurcic J.G., Larson S.M., Sgouros G., McDevitt M.R., Finn R.D., Divgi C.R., et al. Targeted alpha particle immunotherapy for myeloid leukemia. Blood 2002, 100:1233-1239.
67. Roboz G.J., Knovich M.A., Bayer R.L., Schuster M.W., Seiter K., Powell B.L., et al. Efficacy and safety of gemtuzumab ozogamicin in patients with poor-prognosis acute myeloid leukemia. Leuk Lymphoma 2002, 43:1951-1955.
68. Burke J.M., Caron P.C., Papadopoulos E.B., Divgi C.R., Sgouros G., Panageas K.S., et al. Cytoreduction with iodine-131-anti-CD33 antibodies before bone marrow transplantation for advanced myeloid leukemias. Bone Marrow Transplant 2003, 32:549-556.
69. Jabbour E., Garcia-Manero G., Cortes J., Ravandi F., Plunkett W., Gandhi V., et al. Twice-daily fludarabine and cytarabine combination with or without gentuzumab ozogamicin is effective in patients with relapsed/refractory acute myeloid leukemia, high-risk myelodysplastic syndrome, and blast-phase chronic myeloid leukemia. Clin Lymphoma Myeloma Leuk 2012, 12:244-251.
70. Zwaan C.M., Reinhardt D., Jurgens H., Huismans D.R., Hahlen K., Smith O.P., et al. Gemtuzumab ozogamicin in pediatric CD33-positive acute lymphoblastic leukemia: first clinical experiences and relation with cellular sensitivity to single agent calicheamicin. Leukemia 2003, 17:468-470.
71. Hoelzer D., Gökbuget N. Chemoimmunotherapy in acute lymphoblastic leukemia. Blood Rev 2012, 26:25-32.
72. Vitale C., Romagnani C., Falco M., Ponte M., Vitale M., Moretta A., et al. Engagement of p75/AIRM1 or CD33 inhibits the proliferation of normal or leukemic myeloid cells. Proc Natl Acad Sci U S A 1999, 96:15091-15096.
73. Vitale C., Romagnani C., Puccetti A., Olive D., Costello R., Chiossone L., et al. Surface expression and function of p75/AIRM-1 or CD33 in acute myeloid leukemias: engagement of CD33 induces apoptosis of leukemic cells. Proc Natl Acad Sci U S A 2001, 98:5764-5769.
74. Caron P.C., Jurcic J.G., Scott A.M., Finn R.D., Divgi C.R., Graham M.C., et al. A phase 1B trial of humanized monoclonal antibody M195 (anti-CD33) in myeloid leukemia: specific targeting without immunogenicity. Blood 1994, 83:1760-1768.
75. Jurcic J.G., DeBlasio T., Dumont L., Yao T.J., Scheinberg D.A. Molecular remission induction with retinoic acid and anti-CD33 monoclonal antibody HuM195 in acute promyelocytic leukemia. Clin Cancer Res 2000, 6:372-380.
76. Caron P.C., Dumont L., Scheinberg D.A. Supersaturating infusional humanized anti-CD33 monoclonal antibody HuM195 in myelogenous leukemia. Clin Cancer Res 1998, 4:1421-1428.
77. Feldman E., Kalaycio M., Weiner G., Frankel S., Schulman P., Schwartzberg L., et al. Treatment of relapsed or refractory acute myeloid leukemia with humanized anti-CD33 monoclonal antibody HuM195. Leukemia 2003, 17:314-318.
78. Raza A., Jurcic J.G., Roboz G.J., Maris M., Stephenson J.J., Wood B.L., et al. Complete remissions observed in acute myeloid leukemia following prolonged exposure to lintuzumab: a phase 1 trial. Leuk Lymphoma 2009, 50:1336-1344.
79. Feldman E.J., Brandwein J., Stone R., Kalaycio M., Moore J., O'Connor J., et al. Phase III randomized multicenter study of a humanized anti-CD33 monoclonal antibody, lintuzumab, in combination with chemotherapy, versus chemotherapy alone in patients with refractory or first-relapsed acute myeloid leukemia. J Clin Oncol 2005, 23:4110-4116.
80. Lancet J.E., Sekeres M.A., Wood B.L., Grove L.E., Sandalic L., Sievers E.L., et al. Lintuzumab and low-dose cytarabine compared to placebo and low-dose cytarabine in patients with untreated acute myeloid leukemia (AML) 60years and older: results of a randomized, double-blinded phase 2b study [abstract]. Blood 2011, 118:1543-1544.
81. Linenberger M.L. CD33-directed therapy with gemtuzumab ozogamicin in acute myeloid leukemia: progress in understanding cytotoxicity and potential mechanisms of drug resistance. Leukemia 2005, 19:176-182.
82. Cowan A.J., Laszlo G.S., Estey E.H., Walter R.B. Antibody-based therapy of acute myeloid leukemia with gemtuzumab ozogamicin. Front Biosci (Landmark Ed) 2013, 18:1311-1334.
83. Sievers E.L., Larson R.A., Stadtmauer E.A., Estey E., Lowenberg B., Dombret H., et al. Efficacy and safety of gemtuzumab ozogamicin in patients with CD33-positive acute myeloid leukemia in first relapse. J Clin Oncol 2001, 19:3244-3254.
84. Sievers E.L., Appelbaum F.R., Spielberger R.T., Forman S.J., Flowers D., Smith F.O., et al. Selective ablation of acute myeloid leukemia using antibody-targeted chemotherapy: a phase I study of an anti-CD33 calicheamicin immunoconjugate. Blood 1999, 93:3678-3684.
85. Larson R.A., Sievers E.L., Stadtmauer E.A., Löwenberg B., Estey E.H., Dombret H., et al. Final report of the efficacy and safety of gemtuzumab ozogamicin (Mylotarg) in patients with CD33-positive acute myeloid leukemia in first recurrence. Cancer 2005, 104:1442-1452.
86. Giles F., Estey E., O'Brien S. Gemtuzumab ozogamicin in the treatment of acute myeloid leukemia. Cancer 2003, 98:2095-2104.
87. Fenton C., Perry C.M. Gemtuzumab ozogamicin: a review of its use in acute myeloid leukaemia. Drugs 2005, 65:2405-2427.
88. Tsimberidou A.M., Giles F.J., Estey E., O'Brien S., Keating M.J., Kantarjian H.M. The role of gemtuzumab ozogamicin in acute leukaemia therapy. Br J Haematol 2006, 132:398-409.
89. Abutalib S.A., Tallman M.S. Monoclonal antibodies for the treatment of acute myeloid leukemia. Curr Pharm Biotechnol 2006, 7:343-369.
90. Pagano L., Fianchi L., Caira M., Rutella S., Leone G. The role of gemtuzumab ozogamicin in the treatment of acute myeloid leukemia patients. Oncogene 2007, 26:3679-3690.
91. Stasi R., Evangelista M.L., Buccisano F., Venditti A., Amadori S. Gemtuzumab ozogamicin in the treatment of acute myeloid leukemia. Cancer Treat Rev 2008, 34:49-60.
92. Taksin A.L., Legrand O., Raffoux E., de Revel T., Thomas X., Contentin N., et al. High efficacy and safety profile of fractionated doses of Mylotarg as induction therapy in patients with relapsed acute myeloblastic leukemia: a prospective study of the alfa group. Leukemia 2007, 21:66-71.
93. Farhat H., Reman O., Raffoux E., Berthon C., Pautas C., Kammoun L., et al. Fractionated doses of gemtuzumab ozogamicin with escalated doses of daunorubicin and cytarabine as first acute myeloid leukemia salvage in patients aged 50-70-year old: a phase 1/2 study of the acute leukemia French association. Am J Hematol 2012, 87:62-65.
94. Estey E.H., Giles F.J., Beran M., O'Brien S., Pierce S.A., Faderl S.H., et al. Experience with gemtuzumab ozogamycin ("mylotarg") and all-trans retinoic acid in untreated acute promyelocytic leukemia. Blood 2002, 99:4222-4224.
95. Ravandi F., Estey E., Jones D., Faderl S., O'Brien S., Fiorentino J., et al. Effective treatment of acute promyelocytic leukemia with all-trans-retinoic acid, arsenic trioxide, and gemtuzumab ozogamicin. J Clin Oncol 2009, 27:504-510.
96. Lo-Coco F., Cimino G., Breccia M., Noguera N.I., Diverio D., Finolezzi E., et al. Gemtuzumab ozogamicin (Mylotarg) as a single agent for molecularly relapsed acute promyelocytic leukemia. Blood 2004, 104:1995-1999.
97. Petti M.C., Pinazzi M.B., Diverio D., Romano A., Petrucci M.T., De Santis S., et al. Prolonged molecular remission in advanced acute promyelocytic leukaemia after treatment with gemtuzumab ozogamicin (Mylotarg CMA-676). Br J Haematol 2001, 115:63-65.
98. Breccia M., Cimino G., Diverio D., Gentilini F., Mandelli F., Lo Coco F. Sustained molecular remission after low dose gemtuzumab-ozogamicin in elderly patients with advanced acute promyelocytic leukemia. Haematologica 2007, 92:1273-1274.
99. Takeshita A. Efficacy and resistance of gemtuzumab ozogamicin for acute myeloid leukemia. Int J Hematol 2013, 97:703-716.
100. Burnett A.K., Hills R.K., Milligan D., Kjeldsen L., Kell J., Russell N.H., et al. Identification of patients with acute myeloblastic leukemia who benefit from the addition of gemtuzumab ozogamicin: results of the MRC AML15 trial. J Clin Oncol 2011, 29:369-377.
101. Burnett A.K., Russell N.H., Hills R.K., Kell J., Freeman S., Kjeldsen L., et al. Addition of gemtuzumab ozogamicin to induction chemotherapy improves survival in older patients with acute myeloid leukemia. J Clin Oncol 2012, 30:3924-3931.
102. Castaigne S., Pautas C., Terré C., Raffoux E., Bordessoule D., Bastie J.N., et al. Effect of gemtuzumab ozogamicin on survival of adult patients with de-novo acute myeloid leukaemia (ALFA-0701): a randomised, open-label, phase 3 study. Lancet 2012, 379:1508-1516.
103. Delaunay J., Recher C., Pigneux A., Witz F., Vey N., Blanchet O., et al. Addition of gemtuzumab ozogamycin to chemotherapy improves event-free survival but not overall survival of AML patients with intermediate cytogenetics not eligible for allogeneic transplantation. Results of the GOELAMS AML 2006 IR study [abstract]. Blood 2011, 118:37-38.
104. Petersdorf S.H., Kopecky K.J., Slovak M., Willman C., Nevill T., Brandwein J., et al. A phase 3 study of gemtuzumab ozogamicin during induction and postconsolidation therapy in younger patients with acute myeloid leukemia. Blood 2013, 121:4854-4860.
105. Hills R.K., Petersdorf S., Estey E.H., Othus M., Appelbaum F.R., Castaigne S., et al. The addition of gemtuzumab ozogamicin (GO) to induction chemotherapy reduces relapse and improves survival in patients without adverse risk karyotype: results of an individual patient meta-analysis of the five randomised trials [abstract]. Blood 2013, 122:356.
106. Gamis A.S., Aplenc R., Alonzo T.A., Sung L., Meshinchi S., Gerbing R.B., et al. Gemtuzumab ozogamicin (GO) in children with de novo acute myeloid leukemia (AML) improves event-free survival (EFS) by reducing relapse risk - results from the randomized phase III Children's Oncology Group (COG) trial, AAML0531 [abstract]. Blood 2013, 122:355.
107. Amadori S., Suciu S., Stasi R., Salih H.R., Selleslag D., Muus P., et al. Sequential combination of gemtuzumab ozogamicin and standard chemotherapy in older patients with newly diagnosed acute myeloid leukemia: results of a randomized phase III trial by the EORTC and GIMEMA consortium (AML-17). J Clin Oncol 2013, 31:4424-4430.
108. Burnett A.K., Hills R.K., Hunter A.E., Milligan D., Kell W.J., Wheatley K., et al. The addition of gemtuzumab ozogamicin to low-dose Ara-C improves remission rate but does not significantly prolong survival in older patients with acute myeloid leukaemia: results from the LRF AML14 and NCRI AML16 pick-a-winner comparison. Leukemia 2013, 27:75-81.
109. Löwenberg B., Beck J., Graux C., van Putten W., Schouten H.C., Verdonck L.F., et al. Gemtuzumab ozogamicin as postremission treatment in AML at 60years of age or more: results of a multicenter phase 3 study. Blood 2010, 115:2586-2591.
110. Fernandez H.F., Sun Z., Litzow M.R., Luger S.M., Paietta E.M., Racevskis J., et al. Autologous transplantation gives encouraging results for young adults with favorable-risk acute myeloid leukemia, but is not improved with gemtuzumab ozogamicin. Blood 2011, 117:5306-5313.
111. Hasle H., Abrahamsson J., Forestier E., Ha S.Y., Heldrup J., Jahnukainen K., et al. Gemtuzumab ozogamicin as postconsolidation therapy does not prevent relapse in children with AML: results from NOPHO-AML 2004. Blood 2012, 120:978-984.
112. Estey E. Treatment of AML: resurrection for gemtuzumab ozogamicin?. Lancet 2012, 379:1468-1469.
113. Foran J.M. Gemtuzumab: time to bring back on the market?. Clin Adv Hematol Oncol 2012, 10:326-327.
114. Ravandi F., Estey E.H., Appelbaum F.R., Lo-Coco F., Schiffer C.A., Larson R.A., et al. Gemtuzumab ozogamicin: time to resurrect?. J Clin Oncol 2012, 30:3921-3923.
115. Rowe J.M., Löwenberg B. Gemtuzumab ozogamicin in acute myeloid leukemia: a remarkable saga about an active drug. Blood 2013, 121:4838-4841.
116. Ricart A.D. Antibody-drug conjugates of calicheamicin derivative: gemtuzumab ozogamicin and inotuzumab ozogamicin. Clin Cancer Res 2011, 17:6417-6427.
117. Lapusan S., Vidriales M.B., Thomas X., de Botton S., Vekhoff A., Tang R., et al. Phase I studies of AVE9633, an anti-CD33 antibody-maytansinoid conjugate, in adult patients with relapsed/refractory acute myeloid leukemia. Investig. New Drugs 2012, 30:1121-1131.
118. Borthakur G., Rosenblum M.G., Talpaz M., Daver N., Ravandi F., Faderl S., et al. Phase 1 study of an anti-CD33 immunotoxin, humanized monoclonal antibody M195 conjugated to recombinant gelonin (HUM-195/rGEL), in patients with advanced myeloid malignancies. Haematologica 2013, 98:217-221.
119. Thomas E.D., Storb R., Clift R.A., Fefer A., Johnson F.L., Neiman P.E., et al. Bone-marrow transplantation. N Engl J Med 1975, 292:832-843.
120. Clift R.A., Buckner C.D., Appelbaum F.R., Bearman S.I., Petersen F.B., Fisher L.D., et al. Allogeneic marrow transplantation in patients with acute myeloid leukemia in first remission: a randomized trial of two irradiation regimens. Blood 1990, 76:1867-1871.
121. Clift R.A., Buckner C.D., Appelbaum F.R., Sullivan K.M., Storb R., Thomas E.D. Long-term follow-up of a randomized trial of two irradiation regimens for patients receiving allogeneic marrow transplants during first remission of acute myeloid leukemia. Blood 1998, 92:1455-1456.
122. Appelbaum F.R., Matthews D.C., Eary J.F., Badger C.C., Kellogg M., Press O.W., et al. The use of radiolabeled anti-CD33 antibody to augment marrow irradiation prior to marrow transplantation for acute myelogenous leukemia. Transplantation 1992, 54:829-833.
123. Jurcic J.G., Caron P.C., Nikula T.K., Papadopoulos E.B., Finn R.D., Gansow O.A., et al. Radiolabeled anti-CD33 monoclonal antibody M195 for myeloid leukemias. Cancer Res 1995, 55:5908. [s-10s].
124. Matthews D.C., Appelbaum F.R. Radioimmunotherapy and hematopoietic cell transplantation. Thomas' Hematopoietic Cell Transplantion 2004, 198-208. Blackwell Publishing Ltd., Massachusetts, MA. 3rd ed. K.G. Blume, S.J. Forman, F.R. Appelbaum (Eds.).
125. Nikula T.K., McDevitt M.R., Finn R.D., Wu C., Kozak R.W., Garmestani K., et al. Alpha-emitting bismuth cyclohexylbenzyl DTPA constructs of recombinant humanized anti-CD33 antibodies: pharmacokinetics, bioactivity, toxicity and chemistry. J Nucl Med 1999, 40:166-176.
126. McDevitt M.R., Finn R.D., Ma D., Larson S.M., Scheinberg D.A. Preparation of alpha-emitting 213Bi-labeled antibody constructs for clinical use. J Nucl Med 1999, 40:1722-1727.
127. Mulford D.A., Pandit-Taskar N., McDevitt M.R., Finn R.D., Weiss M.A., Apostolidis C., et al. Sequential therapy with cytarabine and bismuth-213 (213Bi)-labeled-HuM195 (anti-CD33) for acute myeloid leukemia (AML) [abstract]. Blood 2004, 104:496a.
128. Rosenblat T.L., McDevitt M.R., Pandit-Taskar N., Carrasquillo J.A., Chanel S., Frattini M.G., et al. Phase I trial of the targeted alpha-particle nano-generator actinium-225 (225Ac)-HuM195 (anti-CD33) in acute myeloid leukemia (AML) [abstract]. Blood 2007, 110:277a.
129. Rosenblat T.L., McDevitt M.R., Mulford D.A., Pandit-Taskar N., Divgi C.R., Panageas K.S., et al. Sequential cytarabine and alpha-particle immunotherapy with bismuth-213-lintuzumab (HuM195) for acute myeloid leukemia. Clin Cancer Res 2010, 16:5303-5311.
130. Jurcic J.G., Ravandi F., Pagel J.M., Park J.H., Douer D., Estey E.H., et al. Phase I trial of the targeted alpha-particle nano-generator actinium-225 (225Ac)-lintuzumab (anti-CD33) in combination with low-dose cytarabine (LDAC) for older patients with untreated acute myeloid leukemia (AML) [abstract]. Blood 2013, 122:1460.
131. Giles F.J., Kantarjian H.M., Kornblau S.M., Thomas D.A., Garcia-Manero G., Waddelow T.A., et al. Mylotarg (gemtuzumab ozogamicin) therapy is associated with hepatic venoocclusive disease in patients who have not received stem cell transplantation. Cancer 2001, 92:406-413.
132. McDonald G.B. Management of hepatic sinusoidal obstruction syndrome following treatment with gemtuzumab ozogamicin (Mylotarg). Clin Lymphoma 2002, 2(Suppl. 1):S35-S39.
133. Wadleigh M., Richardson P.G., Zahrieh D., Lee S.J., Cutler C., Ho V., et al. Prior gemtuzumab ozogamicin exposure significantly increases the risk of veno-occlusive disease in patients who undergo myeloablative allogeneic stem cell transplantation. Blood 2003, 102:1578-1582.
134. McKoy J.M., Angelotta C., Bennett C.L., Tallman M.S., Wadleigh M., Evens A.M., et al. Gemtuzumab ozogamicin-associated sinusoidal obstructive syndrome (SOS): an overview from the research on adverse drug events and reports (RADAR) project. Leuk Res 2007, 31:599-604.
135. Rajvanshi P., Shulman H.M., Sievers E.L., McDonald G.B. Hepatic sinusoidal obstruction after gemtuzumab ozogamicin (Mylotarg) therapy. Blood 2002, 99:2310-2314.
136. Maniecki M.B., Hasle H., Bendix K., Moller H.J. Is hepatotoxicity in patients treated with gemtuzumabozogamicin due to specific targeting of hepatocytes?. Leuk Res 2011, 35:e84-e86.
137. Heider K.-H., Konopitzky R., Ostermann E., Lamche H., Kuepcue Z., Koessl C., et al. A novel Fc-engineered antibody to CD33 with enhanced ADCC activity for treatment of AML [abstract]. Blood 2012, 120:1363.
138. Senyukov V., Kelton W., Mehta N., Georgiou G., Lee D. Engineering anti-AML antibodies for improved NK cell ADCC [abstract]. Blood 2012, 120:3629.
139. Kung Sutherland M.S., Walter R.B., Jeffrey S.C., Burke P.J., Yu C., Kostner H., et al. SGN-CD33A: a novel CD33-targeting antibody-drug conjugate using a pyrrolobenzodiazepine dimer is active in models of drug-resistant AML. Blood 2013, 122:1455-1463.
140. ten Cate B., Bremer E., de Bruyn M., Bijma T., Samplonius D., Schwemmlein M., et al. A novel AML-selective TRAIL fusion protein that is superior to Gemtuzumab Ozogamicin in terms of in vitro selectivity, activity and stability. Leukemia 2009, 23:1389-1397.
141. Carter P. Improving the efficacy of antibody-based cancer therapies. Nat Rev Cancer 2001, 1:118-129.
142. Riethmüller G. Symmetry breaking: bispecific antibodies, the beginnings, and 50years on. Cancer Immun 2012, 12:12.
143. Baeuerle P.A., Reinhardt C. Bispecific T-cell engaging antibodies for cancer therapy. Cancer Res 2009, 69:4941-4944.
144. Choi B.D., Cai M., Bigner D.D., Mehta A.I., Kuan C.T., Sampson J.H. Bispecific antibodies engage T cells for antitumor immunotherapy. Expert Opin Biol Ther 2011, 11:843-853.
145. Topp M.S., Gökbuget N., Zugmaier G., Degenhard E., Goebeler M.E., Klinger M., et al. Long-term follow-up of hematologic relapse-free survival in a phase 2 study of blinatumomab in patients with MRD in B-lineage ALL. Blood 2012, 120:5185-5187.
146. Topp M.S., Goekbuget N., Zugmaier G., Viardot A., Stelljes M., Neumann S., et al. Anti-CD19 BiTE blinatumomab induces high complete remission rate and prolongs survival in adult patients with relapsed/refractory B-precursor acute lymphoblastic leukemia (ALL) [abstract]. Blood 2012, 120:670.
147. Aigner M., Feulner J., Schaffer S., Kischel R., Kufer P., Schneider K., et al. T lymphocytes can be effectively recruited for ex vivo and in vivo lysis of AML blasts by a novel CD33/CD3-bispecific BiTE antibody construct. Leukemia 2013, 27:1107-1115.
148. Stamova S., Cartellieri M., Feldmann A., Arndt C., Koristka S., Bartsch H., et al. Unexpected recombinations in single chain bispecific anti-CD3-anti-CD33 antibodies can be avoided by a novel linker module. Mol Immunol 2011, 49:474-482.
149. Arndt C., von Bonin M., Cartellieri M., Feldmann A., Koristka S., Michalk I., et al. Redirection of T cells with a first fully humanized bispecific CD33-CD3 antibody efficiently eliminates AML blasts without harming hematopoietic stem cells. Leukemia 2013, 27:964-967.
150. Arndt C., Feldmann A., von Bonin M., Cartellieri M., Ewen E.M., Koristka S., et al. Costimulation improves the killing capability of T cells redirected to tumor cells expressing low levels of CD33: description of a novel modular targeting system. Leukemia 2014, 28:59-69.
151. Kügler M., Stein C., Kellner C., Mentz K., Saul D., Schwenkert M., et al. A recombinant trispecific single-chain Fv derivative directed against CD123 and CD33 mediates effective elimination of acute myeloid leukaemia cells by dual targeting. Br J Haematol 2010, 150:574-586.
152. Schubert I., Kellner C., Stein C., Kugler M., Schwenkert M., Saul D., et al. A single-chain triplebody with specificity for CD19 and CD33 mediates effective lysis of mixed lineage leukemia cells by dual targeting. MAbs 2011, 3:21-30.
153. Stamova S., Cartellieri M., Feldmann A., Bippes C.C., Bartsch H., Wehner R., et al. Simultaneous engagement of the activatory receptors NKG2D and CD3 for retargeting of effector cells to CD33-positive malignant cells. Leukemia 2011, 25:1053-1056.
154. Singer H., Kellner C., Lanig H., Aigner M., Stockmeyer B., Oduncu F., et al. Effective elimination of acute myeloid leukemic cells by recombinant bispecific antibody derivatives directed against CD33 and CD16. J Immunother 2010, 33:599-608.
155. Wiernik A., Foley B., Zhang B., Verneris M.R., Warlick E., Gleason M.K., et al. Targeting natural killer cells to acute myeloid leukemia in vitro with a CD16×33 bispecific killer cell engager and ADAM17 inhibition. Clin Cancer Res 2013, 19:3844-3855.
156. Gleason M.K., Ross J.A., Warlick E.D., Lund T.C., Verneris M.R., Wiernik A., et al. CD16xCD33 bispecific killer cell engager (BiKE) activates NK cells from MDS patients against primary MDS and MDSC CD33+ targets. Blood 2014, (Epub ahead of print). 10.1182/blood-2013-10-533398.
157. Fry T.J., Mackall C.L. T-cell adoptive immunotherapy for acute lymphoblastic leukemia. Hematology Am Soc Hematol Educ Program 2013, 2013:348-353.
158. Marin V., Pizzitola I., Agostoni V., Attianese G.M., Finney H., Lawson A., et al. Cytokine-induced killer cells for cell therapy of acute myeloid leukemia: improvement of their immune activity by expression of CD33-specific chimeric receptors. Haematologica 2010, 95:2144-2152.
159. Pizzitola I., Agostoni V., Cribioli E., Pule M., Rousseau R., Finney H., et al. In vitro comparison of three different chimeric receptor-modified effector T-cell populations for leukemia cell therapy. J Immunother 2011, 34:469-479.
160. Dutour A., Marin V., Pizzitola I., Valsesia-Wittmann S., Lee D., Yvon E., et al. In vitro and in vivo antitumor effect of anti-CD33 chimeric receptor-expressing EBV-CTL against CD33+ acute myeloid leukemia. Adv Hematol 2012, 2012:683065.
161. Pizzitola I., Anjos-Afonso F., Rouault-Pierre K., Lassailly F., Tettamanti S., Spinelli O., et al. Chimeric antigen receptors against CD33/CD123 antigens efficiently target primary acute myeloid leukemia cells in vivo. Leukemia 2014, (Epub ahead of print). 10.1038/leu.2014.62.
162. Rubnitz J.E., Gibson B., Smith F.O. Acute myeloid leukemia. Hematol Oncol Clin N Am 2010, 24:35-63.
163. Burnett A., Wetzler M., Löwenberg B. Therapeutic advances in acute myeloid leukemia. J Clin Oncol 2011, 29:487-494.
164. Othus M., Kantarjian H., Petersdorf S., Ravandi F., Godwin J., Cortes J., et al. Declining rates of treatment-related mortality in patients with newly diagnosed AML given 'intense' induction regimens: a report from SWOG and MD Anderson. Leukemia 2014, 28:289-292.
165. Damle N.K., Frost P. Antibody-targeted chemotherapy with immunoconjugates of calicheamicin. Curr Opin Pharmacol 2003, 3:386-390.