Expression of interleukin-3 receptor subunits on defined subpopulations of acute myeloid leukemia blasts predicts the cytotoxicity of diphtheria toxin interleukin-3 fusion protein against malignant progenitors that engraft in immunodeficient mice

Blood

Volumn 108, Issue 10, 2006, Pages 3530-3537

  Yalcintepe, Leman ^b   Frankel, Arthur E ^b   Hogge, Donna E ^a  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; CD38 ANTIGEN; CD71 ANTIGEN; DENILEUKIN DIFTITOX; DIPHTHERIA TOXIN INTERLEUKIN 3; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HYBRID PROTEIN; INTERLEUKIN 3 RECEPTOR; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL CELL; ARTICLE; CD34 SELECTION; CONTROLLED STUDY; CYTOTOXICITY; FLUORESCENCE ACTIVATED CELL SORTER; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL;

EID: 33751174737     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-04-013813     Document Type: Article

References (45)

1. 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;317:468-473.
2. McCulloch EA. Stem cells in normal and leukemic hemopoiesis. Blood. 1983;62:1-13.
3. Griffin JD, Lowenberg B. Clonogenic cells in acute myeloblastic leukemia. Blood. 1986;68:1185-1195.
4. Sutherland HJ, Blair A, Zapf RW. Characterization of a hierarchy in human acute myeloid leukemia progenitor cells. Blood. 1996;87:4754-4761.
5. Ailles LE, Gerhard B, Hogge DE. Detection and characterization of primitive malignant and normal progenitors in patients with acute myelogenous leukemia using long-term coculture with supportive feeder layers and cytokines. Blood. 1997;90:2555-2564.
6. Hogge DE, Lansdorp PM, Reid D, Gerhard B, Eaves CJ. Enhanced detection, maintenance and differentiation of primitive human hematopoietic cells in cultures containing murine fibroblasts engineered to produce human Steel factor, interleukin-3 and granulocyte colony-stimulating factor. Blood. 1996;88:3765-3773.
7. 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;94:1761-1772.
8. Kawagoe H, Humphries RK, Blair A, Sutherland HJ, Hogge DE. Expression of Hox genes, HOX cofactors, and MLL in phenotypically and functionally defined subpopulations of leukemic and normal human hematopoietic cells. Leukemia. 1999;13:687-698.
9. + subpopulations of human bone marrow cells. Proc Natl Acad Sci U S A. 1994;91:12223-12227.
10. Bhatia M, Wang JCY, Kapp U, Bonnet D, Dick JE. Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proc Natl Acad Sci U S A. 1997;94:5320-5325.
11. Conneally E, Cashman J, Petzer A, Eaves C. Expansion in vitro of transplantable human cord blood stem cells demonstrated using a quantitative assay of their lympho-myeloid repopulating activity in nonobese diabetic-scid/scid mice. Proc Natl Acad Sci U S A. 1997;94:9836-9841.
12. Blair A, Hogge DE, Ailles LE, Lansdorp PM, Sutherland HJ. Lack of expression of Thy-1 (CD90) on acute myeloid leukaemia cells with long-term proliferative ability in vitro and in vivo. Blood. 1997;89:3104-3112.
13. Blair A, Sutherland HJ. Primitive acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo lack surface expression of c-kit. Exp Hematol. 2000;28:660-671.
14. Jordan CT, Upchurch D, Szilvassy SJ, et al. The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells. Leukemia. 2000;14:1777-1784.
15. -. Blood. 1998;92:4325-4335.
16. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 1997;3:730-736.
17. Chang F, Steelman LS, Lee JT, et al. Signal transduction mediated by the Ras/Raf/MEK/ERK pathway from cytokine receptors to transcription factors: potential targeting for therapeutic intervention. Leukemia. 2003;17:1263-1293.
18. Feuring-Buske M, Frankel AE, Alexander RL, Gerhard B, Hogge DE. A diphtheria toxin-interleukin 3 fusion protein is cytotoxic to primitive acute myeloid leukemia progenitors but spares normal progenitors. Cancer Res. 2002;62:1730-1736.
19. Alexander RL, Ramage J, Kucera GL, Caligiuri MA, Frankel AE. High affinity interleukin-3 receptor expression on blasts from patients with acute myelogenous leukemia correlates with cytotoxicity of a diphtheria toxin/IL-3 fusion protein. Leuk Res. 2001;25:875-881.
20. Testa U, Riccioni R, Militi S, et al. Elevated expression of IL-3Rα in acute myelogenous leukemia is associated with enhanced blast proliferation, increased cellularity, and poor prognosis. Blood. 2002;100:2980-2988.
21. Fitzgerald D, Pastan I. Targeted toxin therapy for the treatment of cancer. J Natl Cancer Inst. 1989;81:1455-1463.
22. Frankel AE, Ramage J, Kiser M, Alexander R, Kucera G, Miller MS. Characterization of diphtheria fusion proteins targeted to the human interleukin-3 receptor. Protein Eng. 2000;13:575-581.
23. Murphy JR, Bishai W, Borowski M, Miyanohara A, Boyd J, Nagle S. Genetic construction, expression, and melanoma-selective cytotoxicity of a diphtheria-toxin-related alpha-melanocyte-stimulating hormone fusion protein. Proc Natl Acad Sci U S A. 1986;83:8258-8262.
24. Williams DP, Parker K, Bacha P, et al. Diphtheria toxin receptor binding domain substitution with interleukin-2: genetic construction and properties of a diphtheria toxin-related interleukin-2 fusion protein. Protein Eng. 1991;1:493-498.
25. Chadwick DE, Williams DP, Niho Y, Murphy JR, Minden MD. Cytotoxicity of a recombinant diphtheria toxin-granulocyte colony-stimulating factor fusion protein on human leukemic blast cells. Leuk Lymphoma. 1993;11:249-262.
26. Feuring-Buske M, Frankel A, Gerhard B, Hogge D. Variable cytotoxicity of diphtheria toxin 388-granulocyte-macrophage colony-stimulating factor fusion protein for acute myelogenous leukemia stem cells. Exp Hematol. 2000;28:1390-1400.
27. Sandvig K, Olsnes S. Rapid entry of nicked diphtheria toxin into cell at low pH: characterization of the entry process and effects of low pH on the toxin molecule. J Biol Chem. 1981;256:9068-9076.
28. Draper RK, Simon MI. The entry of diphtheria toxin into the mammalian cell cytoplasm: evidence for lysosomal involvement. J Biol Chem. 1980;87:849-854.
29. Honjo T, Nishizuka Y, Kato I, Hayaishi O. Adenosine diphosphate ribosylation of aminoacyl transferase II and inhibition of protein synthesis by diphtheria toxin. J Biol Chem. 1971;246:4251-4260.
30. Yamaizumi M, Mekada E, Uchida T, Okada Y. One molecule of diphtheria toxin fragment A introduced into a cell can kill the cell. Cell. 1978;15:245-250.
31. Frankel AE, McCubrey JA, Miller MS, et al. Diphtheria toxin fused to human interleukin-3 is toxic to blasts from patients with myeloid leukemias. Leukemia. 2000;14:576-585.
32. Hogge DE, Yalcintepe L, Wong S-H, Gerhard B, Frankel AE. Variant diphtheria toxin-interleukin-3 fusion proteins with increased receptor affinity have enhanced cytotoxicity against acute myeloid leukemia progenitors. Clin Cancer Res. 2006;12:1284-1291.
33. Bennett JM, Catovsky D, Daniel MT, et al. Proposed revised criteria for the classification of acute myeloid leukemia: a report of the French-American-British Cooperative Group. Ann Intern Med. 1985;103:620-625.
34. Alexander RL, Kucera GL, Klein B, Frankel AE. In vitro interleukin-3 binding to leukemia cells predicts cytotoxicity of a diphtheria toxin/IL-3 fusion protein. Bioconjug Chem. 2000;11:564-568.
35. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29:e45.
36. Bustin SA. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J Mol Endocrinol. 2000;25:169-193.
37. 2-microglobulin-deficient NOD-scid mice. J Immunol. 1997;158:3578-3586.
38. Feuring-Buske M, Gerhard B, Cashman J, Humphries RK, Eaves CJ, Hogge DE. Improved engraftment of human acute myeloid leukemia progenitor cells in beta 2-microglobulin-deficient NOD/SCID mice and in NOD/SCID mice transgenic for human growth factors. Leukemia. 2003;17:760-763.
39. Verlinden SF, van Es HH, van Bekkum DW. Serial bone marrow sampling for long-term follow up of human hematopoiesis in NOD/SCID mice. Exp Hematol. 1998;26:627-630.
40. Grimwade D, Walker H, Oliver F, et al. The importance of diagnostic cytogenetics on outcome in AML: analysis of 1,612 patients entered into the MRC AML 10 trial. Blood. 1998;92:2322-2333.
41. Slovak ML, Kopecky KJ, Cassileth PA, et al. Karyotypic analysis predicts outcome of pre- and post-remission therapy in adult acute myeloid leukemia (AML): A SWOG/ECOG intergroup study [abstract]. Blood. 1998;92:678a.
42. Testa U, Riccioni R, Biffoni M, et al. Diphtheria toxin fused to variant human interleukin-3 induces cytotoxicity of blasts from patients with acute myeloid leukemia according to the level of interleukin-3 receptor expression. Blood. 2005;106:2527-2529.
43. -) hematopoietic cells show altered expression of a subset of genes associated with early cytokine and differentiation responses of their adult counterparts. Blood. 2000;96:4160-4168.
44. Sato N, Caux C, Kitamura T, et al. Expression and factor-dependent modulation of the interleukin-3 receptor subunits on human hematopoietic cells. Blood. 1993;82:752-761.
45. Frankel AE, Weir MA, Hall PD, Hogge DE, Rizzieri DA. Diphtheria toxin-interleukin 3 fusion protein therapy of patients with elderly or relapsed/refractory acute myeloid leukemia (AML) [abstract]. J Clin Oncol [suppl Jun 20]. 2006;24:6569.