Distribution and levels of cell surface expression of CD33 and CD123 in acute myeloid leukemia

Blood Cancer Journal

Volumn 4, Issue 6, 2014, Pages

  Ehninger, A ^a   Kramer, M ^a   Rollig C ^a   Thiede, C ^a   Bornhauser M ^a   Von Bonin, M ^a   Wermke, M ^a   Feldmann, A ^b   Bachmann, M ^b   Ehninger, G ^a   Oelschlagel U ^a  

^a UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD123 ANTIGEN; CD135 ANTIGEN; CD33 ANTIGEN; CD34 ANTIGEN; NUCLEOPHOSMIN; CD33 PROTEIN, HUMAN; FLT3 PROTEIN, HUMAN; IL3RA PROTEIN, HUMAN;

ACUTE GRANULOCYTIC LEUKEMIA; ADULT; AGED; ANTIGEN EXPRESSION; ARTICLE; BLAST CELL; CELL SURFACE; CELLULAR DISTRIBUTION; COHORT ANALYSIS; CYTOGENETICS; FLOW CYTOMETRY; GENE MUTATION; HIGH RISK POPULATION; HUMAN; LYMPHOCYTE; MAJOR CLINICAL STUDY; MINIMAL RESIDUAL DISEASE; MONOSOMY; MYELODYSPLASTIC SYNDROME; MYELOID PROGENITOR CELL; ADOLESCENT; BIOSYNTHESIS; BLOOD; ENZYMOLOGY; FEMALE; GENETICS; IMMUNOLOGY; MALE; MIDDLE AGED; RISK FACTOR; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; FEMALE; FLOW CYTOMETRY; FMS-LIKE TYROSINE KINASE 3; HUMANS; INTERLEUKIN-3 RECEPTOR ALPHA SUBUNIT; LEUKEMIA, MYELOID, ACUTE; MALE; MIDDLE AGED; RISK FACTORS; SIALIC ACID BINDING IG-LIKE LECTIN 3; YOUNG ADULT;

EID: 84903691167     PISSN: None     EISSN: 20445385     Source Type: Journal    
DOI: 10.1038/bcj.2014.39     Document Type: Article

References (63)

1. Fernandez HF, Sun Z, Yao X, Litzow MR, Luger SM, Paietta EM et al. Anthracycline dose intensification in acute myeloid leukemia. N Engl J Med 2009; 361: 1249-1259.
2. Rollig C, Bornhauser M, Thiede C, Taube F, Kramer M, Mohr B et al. Long-term prognosis of acute myeloid leukemia according to the new genetic risk classification of the European LeukemiaNet recommendations: Evaluation of the proposed reporting system. J Clin Oncol 2011; 29: 2758-2765.
3. Schaich M, Rollig C, Soucek S, Kramer M, Thiede C, Mohr B et al. Cytarabine dose of 36 g/m(2) compared with 12 g/m(2) within first consolidation in acute myeloid leukemia: results of patients enrolled onto the prospective randomized AML96 study. J Clin Oncol 2011; 29: 2696-2702.
4. Robak T, Wierzbowska A. Current and emerging therapies for acute myeloid leukemia. Clin Ther 2009; 31(Part 2): 2349-2370.
5. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105-111.
6. ten Cate B, de Bruyn M, Wei Y, Bremer E, Helfrich W. Targeted elimination of leukemia stem cells; a new therapeutic approach in hemato-oncology. Curr Drug Targets 2010; 11: 95-110.
7. 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: 521-534.
8. 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: 1048-1053.
9. Scheinberg DA, Tanimoto M, McKenzie S, Strife A, Old LJ, Clarkson BD. Monoclonal antibody M195: A diagnostic marker for acute myelogenous leukemia. Leukemia 1989; 3: 440-445.
10. Schwonzen M, Diehl V, Dellanna M, Staib P. Immunophenotyping of surface antigens in acute myeloid leukemia by flow cytometry after red blood cell lysis. Leuk Res 2007; 31: 113-116.
11. Gorczyca W, Sun ZY, Cronin W, Li X, Mau S, Tugulea S. Immunophenotypic pattern of myeloid populations by flow cytometry analysis. Methods Cell Biol 2011; 103: 221-266.
12. Favaloro EJ, Bradstock KF, Kabral A, Grimsley P, Zowtyj H, Zola H. Further characterization of human myeloid antigens (gp160, 95; gp150; gp67): investigation of epitopic heterogeneity and non-haemopoietic distribution using panels of monoclonal antibodies belonging to CD-11b, CD-13 and CD-33. Br J Haematol 1988; 69: 163-171.
13. Hoyer JD, Grogg KL, Hanson CA, Gamez JD, Dogan A. CD33 detection by immunohistochemistry in paraffin-embedded tissues: A new antibody shows excellent specificity and sensitivity for cells of myelomonocytic lineage. Am J Clin Pathol 2008; 129: 316-323.
14. Andrews RG, Takahashi M, Segal GM, Powell JS, Bernstein ID, Singer JW. The L4F3 antigen is expressed by unipotent and multipotent colony-forming cells but not by their precursors. Blood 1986; 68: 1030-1035.
15. 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.
16. Robertson MJ, Soiffer RJ, Freedman AS, Rabinowe SL, Anderson KC, Ervin TJ 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.
17. Hauswirth AW, Florian S, Printz D, Sotlar K, Krauth MT, Fritsch G et al. Expression of the target receptor CD33 in CD34/CD38-/CD123 AML stem cells. Eur J Clin Invest 2007; 37: 73-82.
18. Bross PF, Beitz J, Chen G, Chen XH, Duffy E, Kieffer L et al. Approval summary: gemtuzumab ozogamicin in relapsed acute myeloid leukemia. Clin Cancer Res 2001; 7: 1490-1496.
19. Sievers EL, Larson RA, Stadtmauer EA, 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.
20. Rowe JM, Lowenberg B. Gemtuzumab ozogamicin in acute myeloid leukemia: A remarkable saga about an active drug. Blood 2013; 121: 4838-4841.
21. Rajvanshi P, Shulman HM, Sievers EL, McDonald GB. Hepatic sinusoidal obstruction after gemtuzumab ozogamicin (Mylotarg) therapy. Blood 2002; 99: 2310-2314.
22. Castaigne S, Pautas C, Terre C, Raffoux E, Bordessoule D, Bastie JN 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.
23. Lo-Coco F, Cimino G, Breccia M, Noguera NI, Diverio D, Finolezzi E et al. Gemtuzumab ozogamicin (Mylotarg) as a single agent for molecularly relapsed acute promyelocytic leukemia. Blood 2004; 104: 1995-1999.
24. Taksin AL, 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.
25. Walter RB, Appelbaum FR, Estey EH, Bernstein ID. Acute myeloid leukemia stem cells and CD33-targeted immunotherapy. Blood 2012; 119: 6198-6208.
26. Burnett AK, Hills RK, Hunter AE, Milligan D, Kell WJ, 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.
27. Walter RB, Gooley TA, van der Velden VH, Loken MR, van Dongen JJ, Flowers DA 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: 4168-4170.
28. Kung Sutherland MS, Walter RB, Jeffrey SC, Burke PJ, 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.
29. Arndt C, Feldmann A, von Bonin M, Cartellieri M, Ewen EM, 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 2013; 28: 59-69.
30. 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.
31. Hwang K, Park CJ, Jang S, Chi HS, Kim DY, Lee JH et al. Flow cytometric quantification and immunophenotyping of leukemic stem cells in acute myeloid leukemia. Ann Hematol 2012; 91: 1541-1546.
32. Jordan CT, Upchurch D, Szilvassy SJ, Guzman ML, Howard DS, Pettigrew AL et al. The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells. Leukemia 2000; 14: 1777-1784.
33. Munoz L, Nomdedeu JF, Lopez O, Carnicer MJ, Bellido M, Aventin A et al. Interleukin-3 receptor alpha chain (CD123) is widely expressed in hematologic malignancies. Haematologica 2001; 86: 1261-1269.
34. Jin L, Lee EM, Ramshaw HS, Busfield SJ, Peoppl AG, Wilkinson L et al. Monoclonal antibody-mediated targeting of CD123, IL-3 receptor alpha chain, eliminates human acute myeloid leukemic stem cells. Cell Stem Cell 2009; 5: 31-42.
35. Stein C, Kellner C, Kugler M, Reiff N, Mentz K, Schwenkert M et al. Novel conjugates of single-chain Fv antibody fragments specific for stem cell antigen CD123 mediate potent death of acute myeloid leukaemia cells. Br J Haematol 2010; 148: 879-889.
36. Gilliet M, Conrad C, Geiges M, Cozzio A, Thurlimann W, Burg G et al. Psoriasis triggered by toll-like receptor 7 agonist imiquimod in the presence of dermal plasmacytoid dendritic cell precursors. Arch Dermatol 2004; 140: 1490-1495.
37. Florian S, Sonneck K, Hauswirth AW, Krauth MT, Schernthaner GH, Sperr WR et al. Detection of molecular targets on the surface of CD34/CD38- stem cells in various myeloid malignancies. Leuk Lymphoma 2006; 47: 207-222.
38. Kugler 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.
39. Oelschlaegel U, Mohr B, Schaich M, Schakel U, Kroschinsky F, Illmer T et al. HLA-DRneg patients without acute promyelocytic leukemia show distinct immunophenotypic, genetic, molecular, and cytomorphologic characteristics compared to acute promyelocytic leukemia. Cytometry B 2009; 76: 321-327.
40. Shayegi N, Kramer M, Bornhauser M, Schaich M, Schetelig J, Platzbecker U et al. The level of residual disease based on mutant NPM1 is an independent prognostic factor for relapse and survival in AML. Blood 2013; 122: 83-92.
41. Thiede C, Koch S, Creutzig E, Steudel C, Illmer T, Schaich M et al. Prevalence and prognostic impact of NPM1 mutations in 1485 adult patients with acute myeloid leukemia (AML). Blood 2006; 107: 4011-4020.
42. Thiede C, Steudel C, Mohr B, Schaich M, Schakel U, Platzbecker U et al. Analysis of FLT3-activating mutations in 979 patients with acute myelogenous leukemia: Association with FAB subtypes and identification of subgroups with poor prognosis. Blood 2002; 99: 4326-4335.
43. Vardiman JW, Thiele J, Arber DA, Brunning RD, Borowitz MJ, Porwit A 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: 937-951.
44. Mohr B, Schetelig J, Schafer-Eckart K, Schmitz N, Hanel M, Rosler W et al. Impact of allogeneic haematopoietic stem cell transplantation in patients with abnl(17p) acute myeloid leukaemia. Br J Haematol 2013; 161: 237-244.
45. Kottaridis PD, Gale RE, Frew ME, Harrison G, Langabeer SE, Belton AA et al. The presence of a FLT3 internal tandem duplication in patients with acute myeloid leukemia (AML) adds important prognostic information to cytogenetic risk group and response to the first cycle of chemotherapy: Analysis of 854 patients from the United Kingdom Medical Research Council AML 10 and 12 trials. Blood 2001; 98: 1752-1759.
46. Dohner H, Estey EH, Amadori S, Appelbaum FR, Buchner T, Burnett AK et al. Diagnosis and management of acute myeloid leukemia in adults: recommendations from an international expert panel, on behalf of the European Leukemia Net. Blood 2010; 115: 453-474.
47. Eppert K, Takenaka K, Lechman ER, Waldron L, Nilsson B, van Galen P et al. Stem cell gene expression programs influence clinical outcome in human leukemia. Nat Med 2011; 17: 1086-1093.
48. Goardon N, Marchi E, Atzberger A, Quek L, Schuh A, Soneji S et al. Coexistence of LMPP-like and GMP-like leukemia stem cells in acute myeloid leukemia. Cancer Cell 2011; 19: 138-152.
49. Taussig DC, Miraki-Moud F, Anjos-Afonso F, Pearce DJ, Allen K, Ridler C et al. Anti-CD38 antibody-mediated clearance of human repopulating cells masks the heterogeneity of leukemia-initiating cells. Blood 2008; 112: 568-575.
50. Taussig DC, Vargaftig J, Miraki-Moud F, Griessinger E, Sharrock K, Luke T et al. Leukemia-initiating cells from some acute myeloid leukemia patients with mutated nucleophosmin reside in the CD34(-) fraction. Blood 2010; 115: 1976-1984.
51. Lewis RE, Cruse JM, Webb RN, Sanders CM, Beason K. Contrasting antigenic maturation patterns in M0-M2 versus M3 acute myeloid leukemias. Exp Mol Pathol 2007; 83: 269-273.
52. Schubert I, Stein C, Fey GH. Dual-targeting for the elimination of cancer cells with increased selectivity. Antibodies 2012; 1: 2-18.
53. Ding L, Ley TJ, Larson DE, Miller CA, Koboldt DC, Welch JS et al. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 2012; 481: 506-510.
54. Welch JS, Ley TJ, Link DC, Miller CA, Larson DE, Koboldt DC et al. The origin and evolution of mutations in acute myeloid leukemia. Cell 2012; 150: 264-278.
55. Khoury H, Dalal BI, Nantel SH, Horsman DE, Lavoie JC, Shepherd JD et al. Correlation between karyotype and quantitative immunophenotype in acute myelogenous leukemia with t(8;21). Mod Pathol 2004; 17: 1211-1216.
56. De Propris MS, Raponi S, Diverio D, Milani ML, 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.
57. Pollard JA, Alonzo TA, Loken M, Gerbing RB, Ho PA, Bernstein ID 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.
58. Riccioni R, Diverio D, Riti V, Buffolino S, Mariani G, Boe A et al. Interleukin (IL)-3/granulocyte macrophage-colony stimulating factor/IL-5 receptor alpha and beta chains are preferentially expressed in acute myeloid leukaemias with mutated FMS-related tyrosine kinase 3 receptor. Br J Haematol 2009; 144: 376-387.
59. Riccioni R, Pelosi E, Riti V, Castelli G, Lo-Coco F, Testa U. Immunophenotypic features of acute myeloid leukaemia patients exhibiting high FLT3 expression not associated with mutations. Br J Haematol 2011; 153: 33-42.
60. Rollins-Raval M, Pillai R, Warita K, Mitsuhashi-Warita T, Mehta R, Boyiadzis M et al. CD123 immunohistochemical expression in acute myeloid leukemia is associated with underlying FLT3-ITD and NPM1 mutations. Appl Immunohistochem Mol Morphol 2013; 21: 212-217.
61. Topp MS, Kufer P, Gokbuget N, Goebeler M, Klinger M, Neumann S et al. Targeted therapy with the T-cell-engaging antibody blinatumomab of chemotherapy-refractory minimal residual disease in B-lineage acute lymphoblastic leukemia patients results in high response rate and prolonged leukemiafree survival. J Clin Oncol 2011; 29: 2493-2498.
62. Chevallier P, Robillard N, Ayari S, Guillaume T, Delaunay J, Mechinaud F et al. Persistence of CD33 expression at relapse in CD33() acute myeloid leukaemia patients after receiving Gemtuzumab in the course of the disease. Br J Haematol 2008; 143: 744-746.
63. Baer MR, Stewart CC, Dodge RK, Leget G, Sule N, Mrozek K et al. High frequency of immunophenotype changes in acute myeloid leukemia at relapse: implications for residual disease detection (Cancer and Leukemia Group B Study 8361). Blood 2001; 97: 3574-3580.