Acute myeloid leukemia stem cells and CD33-targeted immunotherapy

Blood

Volumn 119, Issue 26, 2012, Pages 6198-6208

  Walter, Roland B ^a,b   Appelbaum, Frederick R ^a,b   Estey, Elihu H ^a,b   Bernstein, Irwin D ^a,b  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AZACITIDINE; CALICHEAMICIN GAMMA1; CD33 ANTIGEN; CD34 ANTIGEN; CLOFARABINE; CYTARABINE; DAUNORUBICIN; ETOPOSIDE; FLUDARABINE; GEMTUZUMAB OZOGAMICIN; GRANULOCYTE COLONY STIMULATING FACTOR; IDARUBICIN; MITOXANTRONE; MULTIDRUG RESISTANCE PROTEIN 1;

ACUTE GRANULOCYTIC LEUKEMIA; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER STEM CELL; CANCER SURVIVAL; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL HETEROGENEITY; CYTOTOXICITY; DISEASE FREE SURVIVAL; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG MECHANISM; DRUG TARGETING; EARLY TERMINATION OF CLINICAL TRIAL; EVENT FREE SURVIVAL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; LEUKEMIA REMISSION; LEUKEMIA STEM CELL; MALIGNANT TRANSFORMATION; MOLECULARLY TARGETED THERAPY; MULTIPLE CYCLE TREATMENT; MYELOID PROGENITOR CELL; NONHUMAN; OVERALL SURVIVAL; PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW;

EID: 84859899567     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-11-325050     Document Type: Review

References (130)

1. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414(6859):105-111. (Pubitemid 33041634)
2. Dick JE. Stem cell concepts renew cancer research. Blood. 2008;112(13):4793-4807.
3. Clarke MF, Dick JE, Dirks PB, et al. Cancer stem cells. Perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res. 2006;66(19):9339-9344.
4. Stubbs MC, Armstrong SA. Therapeutic implications of leukemia stem cell development. Clin Cancer Res. 2007;13(12):3439-3442. (Pubitemid 46955102)
5. Lane SW, Gilliland DG. Leukemia stem cells. Semin Cancer Biol. 2010;20(2):71-76.
6. Majeti R. Monoclonal antibody therapy directed against human acute myeloid leukemia stem cells. Oncogene. 2011;30(9):1009-1019.
7. Passegué E, Jamieson CH, Ailles LE, Weissman IL. Normal and leukemic hematopoiesis: are leukemias a stem cell disorder or a reacquisition of stem cell characteristics? Proc Natl Acad Sci U S A. 2003;100(Suppl 1):11842-11849. (Pubitemid 37205893)
8. Bernstein ID. Monoclonal antibodies to the myeloid stem cells: therapeutic implications of CMA- 676, a humanized anti-CD33 antibody calicheamicin conjugate. Leukemia. 2000;14(3):474-475. (Pubitemid 30142874)
9. Chen GL, Prchal JT. X-linked clonality testing: interpretation and limitations. Blood. 2007;110(5): 1411-1419. (Pubitemid 47443955)
10. Fialkow PJ, Singer JW, Adamson JW, et al. Acute nonlymphocytic leukemia: heterogeneity of stem cell origin. Blood. 1981;57(6):1068-1073. (Pubitemid 11050810)
11. Fialkow PJ, Singer JW, Raskind WH, et al. Clonal development, stem-cell differentiation, and clinical remissions in acute nonlymphocytic leukemia. N Engl J Med. 1987;317(8):468-473. (Pubitemid 17131352)
12. Bernstein ID, Singer JW, Andrews RG, 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(4): 1153-1159. (Pubitemid 17065497)
13. Bernstein ID, Singer JW, Smith FO, 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(7):1811-1816.
14. McCulloch EA. Stem cells in normal and leukemic hemopoiesis (Henry Stratton Lecture, 1982). Blood. 1983;62(1):1-13. (Pubitemid 13070585)
15. Lapidot T, Sirard C, Vormoor J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994; 367(6464):645-648. (Pubitemid 24067706)
16. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 1997;3(7):730-737. (Pubitemid 27298715)
17. Blair A, Hogge DE, Ailles LE, Lansdorp PM, Sutherland HJ. Lack of expression of Thy-1 (CD90) on acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo. Blood. 1997;89(9):3104-3112. (Pubitemid 27229792)
18. Miyamoto T, Weissman IL, Akashi K. AML1/ETO-expressing nonleukemic stem cells in acute myelogenous leukemia with 8;21 chromosomal translocation. Proc Natl Acad Sci U S A. 2000; 97(13):7521-7526. (Pubitemid 30431496)
19. Chao MP, Seita J, Weissman IL. Establishment of a normal hematopoietic and leukemia stem cell hierarchy. Cold Spring Harb Symp Quant Biol. 2008;73:439-449.
20. Taussig DC, Miraki-Moud F, Anjos-Afonso F, et al. Anti-CD38 antibody-mediated clearance of human repopulating cells masks the heterogeneity of leukemia-initiating cells. Blood. 2008;112(3): 568-575.
21. Taussig DC, Vargaftig J, Miraki-Moud F, et al. Leukemia-initiating cells from some acute myeloid leukemia patients with mutated nucleophosmin reside in the CD34- fraction. Blood. 2010; 115(10):1976-1984.
22. Goardon N, Marchi E, Atzberger A, et al. Coexistence of LMPP-like and GMP-like leukemia stem cells in acute myeloid leukemia. Cancer Cell. 2011;19(1):138-152.
23. Ailles LE, Gerhard B, Kawagoe H, Hogge DE. Growth characteristics of acute myelogenous leukemia progenitors that initiate malignant hematopoiesis in nonobese diabetic/severe combined immunodeficient mice. Blood. 1999;94(5):1761-1772. (Pubitemid 29411327)
24. Rombouts WJC, Martens ACM, Ploemacher RE. Identification of variables determining the engraftment potential of human acute myeloid leukemia in the immunodeficient NOD/SCID human chimera model. Leukemia. 2000;14(5):889-897. (Pubitemid 30235068)
25. Rombouts WJC, Blokland I, Löwenberg B, Ploemacher RE. Biological characteristics and prognosis of adult acute myeloid leukemia with internal tandem duplications in the Flt3 gene. Leukemia. 2000;14(4):675-683. (Pubitemid 30195459)
26. Lumkul R, Gorin NC, Malehorn MT, et al. Human AML cells in NOD/SCID mice: engraftment potential and gene expression. Leukemia. 2002;16(9): 1818-1826.
27. Monaco G, Konopleva M, Munsell M, et al. Engraftment of acute myeloid leukemia in NOD/ SCID mice is independent of CXCR4 and predicts poor patient survival. Stem Cells. 2004; 22(2):188-201. (Pubitemid 38282634)
28. Pearce DJ, Taussig D, Zibara K, et al. AML engraftment in the NOD/SCID assay reflects the outcome of AML: implications for our understanding of the heterogeneity of AML. Blood. 2006; 107(3):1166-1173. (Pubitemid 43156319)
29. Sanchez PV, Perry RL, Sarry JE, et al. A robust xenotransplantation model for acute myeloid leukemia. Leukemia. 2009;23(11):2109-2117.
30. Taussig DC, Pearce DJ, Simpson C, et al. Hematopoietic stem cells express multiple myeloid markers: implications for the origin and targeted therapy of acute myeloid leukemia. Blood. 2005; 106(13):4086-4092. (Pubitemid 41775913)
31. Andrews RG, Torok-Storb B, Bernstein ID. Myeloid-associated differentiation antigens on stem cells and their progeny identified by monoclonal antibodies. Blood. 1983;62(1):124-132. (Pubitemid 13070601)
32. Griffin JD, Linch D, Sabbath K, Larcom P, Schlossman SF. A monoclonal antibody reactive with normal and leukemic human myeloid progenitor cells. Leuk Res. 1984;8(4):521-534. (Pubitemid 14051256)
33. Andrews RG, Takahashi M, Segal GM, Powell JS, Bernstein ID, Singer JW. The L4F3 antigen is expressed by unipotent and multipotent colonyforming cells but not by their precursors. Blood. 1986;68(5):1030-1035. (Pubitemid 17186377)
34. Andrews RG, Singer JW, Bernstein ID. 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(5): 1721-1731. (Pubitemid 19126828)
35. Robertson MJ, Soiffer RJ, Freedman AS, 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(9):2229- 2236.
36. Bernstein ID, Andrews RG, Berenson R, Bensinger W, Singer JW, Buckner CD. Isolation of human hematopoietic stem cells. In: Champlin RE, Gale RP, eds. New Strategies in Bone Marrow Transplantation. New York, NY: Wiley-Liss; 1991:201-207.
37. Cozzio A, Passegué E, Ayton PM, Karsunky H, Cleary ML, Weissman IL. Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev. 2003;17(24):3029-3035. (Pubitemid 38040767)
38. Huntly BJ, Shigematsu H, Deguchi K, et al. MOZTIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell. 2004;6(6):587-596. (Pubitemid 40017702)
39. Krivtsov AV, Twomey D, Feng Z, et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature. 2006; 442(7104):818-822. (Pubitemid 44258912)
40. Somervaille TC, Cleary ML. Identification and characterization of leukemia stem cells in murine MLL-AF9 acute myeloid leukemia. Cancer Cell. 2006;10(4):257-268. (Pubitemid 44512188)
41. So CW, Karsunky H, Passegue E, Cozzio A, Weissman IL, Cleary ML. MLL-GAS7 transforms multipotent hematopoietic progenitors and induces mixed lineage leukemias in mice. Cancer Cell. 2003;3(2):161-171. (Pubitemid 37443388)
42. Chen W, Kumar AR, Hudson WA, et al. Malignant transformation initiated by Mll-AF9: gene dosage and critical target cells. Cancer Cell. 2008;13(5): 432-440. (Pubitemid 351609442)
43. Kirstetter P, Schuster MB, Bereshchenko O, et al. Modeling of C/EBPalpha mutant acute myeloid leukemia reveals a common expression signature of committed myeloid leukemia-initiating cells. Cancer Cell. 2008;13(4):299-310. (Pubitemid 351446194)
44. Guibal FC, Alberich-Jorda M, Hirai H, et al. Identification of a myeloid committed progenitor as the cancer-initiating cell in acute promyelocytic leukemia. Blood. 2009;114(27):5415-5425.
45. Kelly LM, Gilliland DG. Genetics of myeloid leukemias. Annu Rev Genomics Hum Genet. 2002;3: 179-198. (Pubitemid 35217435)
46. Fröhling S, Scholl C, Gilliland DG, Levine RL. Genetics of myeloid malignancies: pathogenetic and clinical implications. J Clin Oncol. 2005;23(26): 6285-6295. (Pubitemid 46218838)
47. Vassiliou GS, Cooper JL, Rad R, et al. Mutant nucleophosmin and cooperating pathways drive leukemia initiation and progression in mice. Nat Genet. 2011;43(5):470-475.
48. Corral J, Lavenir I, Impey H, et al. An Mll-AF9 fusion gene made by homologous recombination causes acute leukemia in chimeric mice: a method to create fusion oncogenes. Cell. 1996; 85(6):853-861. (Pubitemid 26192136)
49. Chen W, Li Q, Hudson WA, Kumar A, Kirchhof N, Kersey JH. A murine Mll-AF4 knock-in model results in lymphoid and myeloid deregulation and hematologic malignancy. Blood. 2006;108(2): 669-677. (Pubitemid 44061369)
50. Song WJ, Sullivan MG, Legare RD, et al. Haploinsufficiency of CBFA2 causes familial thrombocytopenia with propensity to develop acute myelogenous leukaemia. Nat Genet. 1999;23(2): 166-175. (Pubitemid 29455388)
51. Smith ML, Cavenagh JD, Lister TA, Fitzgibbon J. Mutation of CEBPA in familial acute myeloid leukemia. N Engl J Med. 2004;351(23):2403-2407.
52. Nanri T, Uike N, Kawakita T, Iwanaga E, Mitsuya H, Asou N. A family harboring a germ-line N-terminal C/EBPalpha mutation and development of acute myeloid leukemia with an additional somatic C-terminal C/EBPalpha mutation. Genes Chromosomes Cancer. 2010;49(3):237- 241.
53. Müller AMS, Duque J, Shizuru JA, Lübbert M. Complementing mutations in core binding factor leukemias: from mouse models to clinical applications. Oncogene. 2008;27(44):5759-5773.
54. Wiemels JL, Xiao Z, Buffler PA, et al. In utero origin of t(8;21) AML1-ETO translocations in childhood acute myeloid leukemia. Blood. 2002; 99(10):3801-3805. (Pubitemid 34534554)
55. Nucifora G, Larson RA, Rowley JD. Persistence of the 8;21 translocation in patients with acute myeloid leukemia type M2 in long-term remission. Blood. 1993;82(3):712-715. (Pubitemid 23221647)
56. Jurlander J, Caligiuri MA, Ruutu T, et al. Persistence of the AML1/ETO fusion transcript in patients treated with allogeneic bone marrow transplantation for t(8;21) leukemia. Blood. 1996; 88(6):2183-2191. (Pubitemid 26307921)
57. Miyamoto T, Nagafuji K, Akashi K, et al. Persistence of multipotent progenitors expressing AML1/ETO transcripts in long-term remission patients with t(8;21) acute myelogenous leukemia. Blood. 1996;87(11):4789-4796. (Pubitemid 26162380)
58. Saunders MJ, Brereton ML, Adams JA, Tobal K, Liu Yin JA. Expression of AML1/MTG8 transcripts in clonogenic cells grown from bone marrow of patients in remission of acute myeloid leukaemia with t(8;21). Br J Haematol. 1997;99(4):921-924. (Pubitemid 28047160)
59. Shih LY, Liang DC, Huang CF, et al. AML patients with CEBPalpha mutations mostly retain identical mutant patterns but frequently change in allelic distribution at relapse: a comparative analysis on paired diagnosis and relapse samples. Leukemia. 2006;20(4):604-609.
60. Falini B, Martelli MP, Bolli N, et al. Acute myeloid leukemia with mutated nucleophosmin (NPM1): is it a distinct entity? Blood. 2011;117(4):1109-1120.
61. Hou HA, Kuo YY, Liu CY, et al. DNMT3A mutations in acute myeloid leukemia: stability during disease evolution and clinical implications. Blood. 2012;119(2):559-568.
62. Kihara R, Hoshino H, Kiyoi H, Naoe T. DNMT3A and IDH1/2 mutations are stable during the progression of acute myeloid leukemia [abstract]. Blood (ASH Annual Meeting Abstracts). 2011; 118(21):637.
63. Kottaridis PD, Gale RE, Langabeer SE, Frew ME, Bowen DT, Linch DC. Studies of FLT3 mutations in paired presentation and relapse samples from patients with acute myeloid leukemia: implications for the role of FLT3 mutations in leukemo-genesis, minimal residual disease detection, and possible therapy with FLT3 inhibitors. Blood. 2002;100(7):2393-2398.
64. Shih LY, Huang CF, Wu JH, et al. Heterogeneous patterns of FLT3 Asp(835) mutations in relapsed de novo acute myeloid leukemia: a comparative analysis of 120 paired diagnostic and relapse bone marrow samples. Clin Cancer Res. 2004; 10(4):1326-1332.
65. Bachas C, Schuurhuis GJ, Hollink IH, et al. High-frequency type I/II mutational shifts between diagnosis and relapse are associated with outcome in pediatric AML: implications for personalized medicine. Blood. 2010;116(15):2752-2758.
66. Pollard JA, Meshinchi S, Harrington KH, Zeng R, Bernstein ID, Walter RB. Sequential acquisition of somatic mutations in progenitors with differential proliferative potential in human acute myeloid leukemia [abstract]. Blood (ASH Annual Meeting Abstracts). 2010;116(21):332.
67. Wang YY, Zhou GB, Yin T, et al. AML1-ETO and C-KIT mutation/ overexpression in t(8;21) leukemia: implication in stepwise leukemogenesis and response to Gleevec. Proc Natl Acad Sci U S A. 2005;102(4):1104-1109. (Pubitemid 40170733)
68. Fearon ER, Burke PJ, Schiffer CA, Zehnbauer BA, Vogelstein B. Differentiation of leukemia cells to polymorphonuclear leukocytes in patients with acute nonlymphocytic leukemia. N Engl J Med. 1986;315(1):15-24. (Pubitemid 16093246)
69. Gale RE, Wheadon H, Goldstone AH, Burnett AK, Linch DC. Frequency of clonal remission in acute myeloid leukaemia. Lancet. 1993;341(8838):138-142. (Pubitemid 23029306)
70. Jowitt SN, Liu Yin JA, Saunders MJ, Lucas GS. Clonal remissions in acute myeloid leukaemia are commonly associated with features of trilineage myelodysplasia during remission. Br J Haematol. 1993;85(4):698-705. (Pubitemid 24003583)
71. Jinnai I, Nagai K, Yoshida S, et al. Incidence and characteristics of clonal hematopoiesis in remission of acute myeloid leukemia in relation to morphological dysplasia. Leukemia. 1995;9(10): 1756-1761.
72. Grimwade D, Enver T. Acute promyelocytic leukemia: where does it stem from? Leukemia. 2004; 18(3):375-384. (Pubitemid 38425848)
73. Eppert K, Takenaka K, Lechman ER, et al. Stem cell gene expression programs influence clinical outcome in human leukemia. Nat Med. 2011; 17(9):1086-1093.
74. Pollard JA, Alonzo TA, Gerbing RB, et al. FLT3 internal tandem duplication in CD34+/CD33-precursors predicts poor outcome in acute myeloid leukemia. Blood. 2006;108(8):2764-2769.
75. Dinndorf PA, Andrews RG, Benjamin D, Ridgway D, Wolff L, Bernstein ID. Expression of normal myeloid-associated antigens by acute leukemia cells. Blood. 1986;67(4):1048-1053. (Pubitemid 16116418)
76. Scheinberg DA, Lovett D, Divgi CR, 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(3):478-490.
77. Caron PC, Dumont L, Scheinberg DA. Supersaturating infusional humanized anti-CD33 monoclonal antibody HuM195 in myelogenous leukemia. Clin Cancer Res. 1998;4(6):1421-1428. (Pubitemid 28265224)
78. Appelbaum FR, Matthews DC, Eary JF, et al. The use of radiolabeled anti-CD33 antibody to augment marrow irradiation prior to marrow transplantation for acute myelogenous leukemia. Transplantation. 1992;54(5):829-833.
79. van der Jagt RHC, Badger CC, Appelbaum FR, et al. Localization of radiolabeled antimyeloid antibodies in a human acute leukemia xenograft tumor model. Cancer Res. 1992;52(1):89-94.
80. Hamann PR, Hinman LM, Beyer CF, et al. An anti-CD33 antibody- calicheamicin conjugate for treatment of acute myeloid leukemia: choice of linker. Bioconjug Chem. 2002;13(1):40-46. (Pubitemid 34119633)
81. Damle NK, Frost P. Antibody-targeted chemotherapy with immunoconjugates of calicheamicin. Curr Opin Pharmacol. 2003;3(4):386-390. (Pubitemid 36908942)
82. Hamann PR, Hinman LM, Hollander I, et al. Gemtuzumab ozogamicin, a potent and selective anti-CD33 antibody-calicheamicin conjugate for treatment of acute myeloid leukemia. Bioconjug Chem. 2002;13(1):47-58. (Pubitemid 34119634)
83. Walter RB, Fairchild SE, Flowers DA, Hong TC, Bernstein ID. Priming with myeloid growth factors enhances CD33 expression, decreases P-glycoprotein activity, and improves efficacy of gemtuzumab ozogamicin against acute myeloid leukemia (AML) colony forming cells (CFC) [abstract]. Blood (ASH Annual Meeting Abstracts). 2008;112(11):912-913.
84. Linenberger ML. CD33-directed therapy with gemtuzumab ozogamicin in acute myeloid leukemia: progress in understanding cytotoxicity and potential mechanisms of drug resistance. Leukemia. 2005;19(2):176-182. (Pubitemid 40220577)
85. Sullivan N, Lyne L. Sensitivity of fibroblasts derived from ataxia-telangiectasia patients to calicheamicin gamma 1I. Mutat Res. 1990;245(3): 171-175. (Pubitemid 20368890)
86. van Duijn-Goedhart A, Zdzienicka MZ, Sankaranarayanan K, van Buul PP. Differential responses of Chinese hamster mutagen sensitive cell lines to low and high concentrations of calicheamicin and neocarzinostatin. Mutat Res. 2000;471(1):95-105.
87. Goemans BF, Zwaan CM, Vijverberg SJ, et al. Large interindividual differences in cellular sensitivity to calicheamicin may influence gemtuzumab ozogamicin response in acute myeloid leukemia. Leukemia. 2008;22(12):2284-2285.
88. Walter RB, Raden BW, Hong TC, Flowers DA, Bernstein ID, Linenberger ML. Multidrug resistance protein attenuates gemtuzumab ozogamicin-induced cytotoxicity in acute myeloid leukemia cells. Blood. 2003;102(4):1466-1473. (Pubitemid 36988058)
89. Taksin AL, Legrand O, Raffoux E, 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(1):66-71. (Pubitemid 44921836)
90. Walter RB, Gooley TA, van der Velden VH, et al. CD33 expression and P-glycoprotein-mediated drug efflux inversely correlate and predict clinical outcome in patients with acute myeloid leukemia treated with gemtuzumab ozogamicin monotherapy. Blood. 2007;109(10):4168-4170. (Pubitemid 46743379)
91. Walter RB, Raden BW, Kamikura DM, Cooper JA, Bernstein ID. Influence of CD33 expression levels and ITIM-dependent internalization on gemtuzumab ozogamicin-induced cytotoxicity. Blood. 2005;105(3):1295-1302. (Pubitemid 40170906)
92. Jager E, van der Velden VHJ, te Marvelde JG, Walter RB, Agur Z, Vainstein V. Targeted drug delivery by gemtuzumab ozogamicin: mechanism-based mathematical model for treatment strategy improvement and therapy individualization. PLoS One. 2011;6(9):e24265.
93. Jedema I, Barge RM, van der Velden VH, et al. Internalization and cell cycle-dependent killing of leukemic cells by gemtuzumab ozogamicin: rationale for efficacy in CD33-negative malignancies with endocytic capacity. Leukemia. 2004;18(2): 316-325. (Pubitemid 38240048)
94. Sievers EL, Appelbaum FR, Spielberger RT, 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(11):3678-3684. (Pubitemid 29249814)
95. Sievers EL, Larson RA, Stadtmauer EA, et al. Efficacy and safety of gemtuzumab ozogamicin in patients with CD33-positive acute myeloid leukemia in first relapse. J Clin Oncol. 2001;19(13): 3244-3254. (Pubitemid 32591442)
96. Bross PF, Beitz J, Chen G, et al. Approval summary: gemtuzumab ozogamicin in relapsed acute myeloid leukemia. Clin Cancer Res. 2001;7(6): 1490-1496. (Pubitemid 32708610)
97. Larson RA, Sievers EL, Stadtmauer EA, 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(7):1442-1452. (Pubitemid 41356159)
98. Giles F, Estey E, O'Brien S. Gemtuzumab ozogamicin in the treatment of acute myeloid leukemia. Cancer. 2003;98(10):2095-2104. (Pubitemid 37392412)
99. Fenton C, Perry CM. Gemtuzumab ozogamicin: a review of its use in acute myeloid leukaemia. Drugs. 2005;65(16):2405-2427. (Pubitemid 41573610)
100. Tsimberidou AM, Giles FJ, Estey E, O'Brien S, Keating MJ, Kantarjian HM. The role of gemtuzumab ozogamicin in acute leukaemia therapy. Br J Haematol. 2006;132(4):398-409. (Pubitemid 43381615)
101. Abutalib SA, Tallman MS. Monoclonal antibodies for the treatment of acute myeloid leukemia. Curr Pharm Biotechnol. 2006;7(5):343-369. (Pubitemid 44524417)
102. 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(25):3679-3690. (Pubitemid 46842699)
103. Stasi R, Evangelista ML, Buccisano F, Venditti A, Amadori S. Gemtuzumab ozogamicin in the treatment of acute myeloid leukemia. Cancer Treat Rev. 2008;34(1):49-60. (Pubitemid 351168609)
104. Caron PC, Jurcic JG, Scott AM, et al. A phase 1B trial of humanized monoclonal antibody M195 (anti-CD33) in myeloid leukemia: specific targeting without immunogenicity. Blood. 1994;83(7): 1760-1768. (Pubitemid 24107898)
105. van der Velden VHJ, te Marvelde JG, Hoogeveen PG, 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(10): 3197-3204.
106. Farhat H, Reman O, Raffoux E, 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(1):62-65.
107. Lo-Coco F, Cimino G, Breccia M, et al. Gemtuzumab ozogamicin (Mylotarg) as a single agent for molecularly relapsed acute promyelocytic leukemia. Blood. 2004;104(7):1995-1999. (Pubitemid 39297848)
108. 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(9):1273- 1274.
109. Takeshita A, Ono T, Kojima Y, et al. Efficacy of gemtuzumab ozogamicin (GO) monotherapy on relapsed/refractory acute promyelocytic leukemia (APL) [abstract]. Blood (ASH Annual Meeting Abstracts). 2011;118(21):665-666.
110. Estey EH, Giles FJ, Beran M, et al. Experience with gemtuzumab ozogamycin ("mylotarg") and all-trans retinoic acid in untreated acute promyelocytic leukemia. Blood. 2002;99(11):4222-4224. (Pubitemid 35332070)
111. Ravandi F, Estey E, Jones D, et al. Effective treatment of acute promyelocytic leukemia with all-trans-retinoic acid, arsenic trioxide, and gemtuzumab ozogamicin. J Clin Oncol. 2009;27(4): 504-510.
112. Burnett AK, Hills RK, Milligan D, et al. Identification of patients with acute myeloblastic leukaemia who benefit from the addition of gemtuzumab ozogamicin: results of the MRC AML15 trial. J Clin Oncol. 2011;29(4):369-377.
113. Castaigne S, Pautas C, Terre C, et al. Effect of gemtuzumab ozogamicin on survival of adult patients with de-novo acute myeloid leukemia (ALFA-0701): a randomised, open-label, phase 3 study. Lancet. 2012;379(9825):1508-1516.
114. Delaunay J, Recher C, Pigneux A, 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. (ASH Annual Meeting Abstracts) 2011;118(21):37-38.
115. Burnett AK, Hill RK, Hunter AE, et al. The addition of gemtuzumab ozogamicin to induction chemotherapy improves survival in older patients with acute myeloid leukemia. J Clin Oncol. 2012; in press.
116. Petersdorf S, Kopecky K, Stuart RK, et al. Preliminary results of Southwest Oncology Group Study S0106: an international intergroup phase 3 randomized trial comparing the addition of gemtuzumab ozogamicin to standard induction therapy versus standard induction therapy followed by a second randomization to post-consolidation gemtuzumab ozogamicin versus no additional therapy for previously untreated acute myeloid leukemia [abstract]. Blood (ASH Annual Meeting Abstracts). 2009;114(22):326-327.
117. http://www.swogstat.org/ROS/ROSBooks/ Spring%202010/Leukemia.pdf. Accessed January 23, 2012.
118. http://media.pfizer.com/files/products/mylotarg- hcp-letter.pdf. Accessed January 23, 2012.
119. Lo Coco F, Ammatuna E, Noguera N. Treatment of acute promyelocytic leukemia with gemtuzumab ozogamicin. Clin Adv Hematol Oncol. 2006;4(1):57-62.
120. Breccia M, Lo-Coco F. Gemtuzumab ozogamicin for the treatment of acute promyelocytic leukemia: mechanisms of action and resistance, safety and efficacy. Expert Opin Biol Ther. 2011;11(2): 225-234.
121. Jurcic JG, DeBlasio T, Dumont L, Yao TJ, Scheinberg DA. Molecular remission induction with retinoic acid and anti-CD33 monoclonal antibody HuM195 in acute promyelocytic leukemia. Clin Cancer Res. 2000;6(2):372-380. (Pubitemid 30111453)
122. Jilani I, Estey E, Huh Y, et al. Differences in CD33 intensity between various myeloid neoplasms. Am J Clin Pathol. 2002;118(4):560-566. (Pubitemid 44698513)
123. Hauswirth AW, Florian S, Printz D, et al. Expression of the target receptor CD33 in CD34+/ CD38-/CD123+AML stem cells. Eur J Clin Invest. 2007;37(1):73-82. (Pubitemid 44934775)
124. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer. 2005;5(4):275- 284.
125. Jawad M, Seedhouse C, Mony U, Grundy M, Russell NH, Pallis M. Analysis of factors that affect in vitro chemosensitivity of leukaemic stem and progenitor cells to gemtuzumab ozogamicin (Mylotarg) in acute myeloid leukaemia. Leukemia. 2010;24(1):74-80.
126. Pollard JA, Alonzo TA, Loken M, et al. Correlation of CD33 expression level with disease characteristics and response to gemtuzumab ozogamicin containing chemotherapy in childhood AML. Blood. 2012;119(16):3705-3711.
127. Lamba J, Mortland LJ, Mitra A, et al. Clinical significance of CD33 non-synonymous single nucleotide polymorphisms (SNPs) in pediatric patients with acute myeloid leukemia treated with gemtuzumab ozogamicin-containing chemotherapy [abstract]. Blood (ASH Annual Meeting Abstracts). 2011;118(21):1489.
128. van der Velden VHJ, Boeckx N, Jedema I, et al. High CD33-antigen loads in peripheral blood limit the efficacy of gemtuzumab ozogamicin (Mylotarg) treatment in acute myeloid leukemia patients. Leukemia. 2004;18(5):983-988. (Pubitemid 38714624)
129. Jordan CT, Guzman ML. Mechanisms controlling pathogenesis and survival of leukemic stem cells. Oncogene. 2004;23(43):7178-7187. (Pubitemid 39382152)
130. Wu AM, Senter PD. Arming antibodies: prospects and challenges for immunoconjugates. Nat Biotechnol. 2005;23(9):1137-1146. (Pubitemid 41486395)