Targeting the silent minority: Emerging immunotherapeutic strategies for eradication of malignant stem cells in chronic myeloid leukaemia

Cancer Immunology, Immunotherapy

Volumn 54, Issue 4, 2005, Pages 297-306

  Copland, M ^a   Fraser, A R ^a   Harrison, S J ^a   Holyoake, T L ^a  

^a GLASGOW ROYAL INFIRMARY   (United Kingdom)

Author keywords

Allogeneic stem cell transplantation; Chronic myeloid leukaemia; Cytotoxic T lymphocytes; Dendritic cells; Imatinib; Immunotherapy

Indexed keywords

HEAT SHOCK PROTEIN; IMATINIB; IMMUNOMODULATING AGENT; VACCINE;

ALLOGENEIC STEM CELL TRANSPLANTATION; ANTIGEN SPECIFICITY; CANCER CELL; CHRONIC MYELOID LEUKEMIA; ERADICATION THERAPY; HUMAN; IMMUNOSTIMULATION; IMMUNOTHERAPY; MEDICAL RESEARCH; ONCOGENE; PRIORITY JOURNAL; QUALITY OF LIFE; REDUCTION; REMISSION; REVIEW; SIGNAL TRANSDUCTION; TOXICITY;

ANIMALS; ANTINEOPLASTIC AGENTS; DENDRITIC CELLS; FUSION PROTEINS, BCR-ABL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; IMMUNOTHERAPY; LEUKEMIA, MYELOID, CHRONIC; PIPERAZINES; PYRIMIDINES; STEM CELLS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 13744251502     PISSN: 03407004     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00262-004-0573-1     Document Type: Review

References (97)

1. + peripheral blood progenitor cells. Blood 103:538-544
2. Avery S, Nadal E, Davis J, Apperley J, Goldman J, Marin D (2003) Infusion of peripheral blood stem cells collected at diagnosis can improve the level of cytogenetic response in CML patients on imatinib whose treatment is limited by cytopaenia. Blood 102:318b
3. Bakalova R, Ohba H, Zhelev Z, Ishikawa M, Shinohara Y, Baba Y (2003) Cross-talk between Bcr-Abl tyrosine kinase, protein kinase C and telomerase-a potential reason for resistance to Glivec in chronic myelogenous leukaemia. Biochem Pharmacol 66:1879-1884
4. Banchereau J, Steinman RM (1998) Dendritic cells and the control of immunity. Nature 392:245-252
5. Barrett AJ, van Rhee F (1997) Graft-versus-leukaemia. Baillieres Clin Haematol 10:337-355
6. Bedi A, Zehnbauer BA, Barber JP, Sharkis SJ, Jones RJ (1994) Inhibition of apoptosis by BCR-ABL in chronic myeloid leukaemia. Blood 83:2038-2044
7. Bellantuono I, Gao L, Parry S, Marley S, Dazzi F, Apperley J, Goldman JM, Stauss HJ (2002) Two distinct HLA-A0201-presented epitopes of the Wilms tumor antigen 1 can function as targets for leukemia-reactive CTL. Blood 100:3835-3837
8. Berke Z, Andersen MH, Pedersen M, Fugger L, Zeuthen J, Haurum JS (2000) Peptides spanning the junctional region of both the abl/bcr and the bcr/abl fusion proteins bind common HLA class I molecules. Leukemia 14:419-426
9. Bhatia R, Wayner EA, McGlave P, Verfaillie CM (1994) Interferon-alpha restores normal adhesion of chronic myelogenous leukaemia hematopoietic progenitors to bone marrow strom by correcting impaired beta 1 integrin receptor function. J Clin Invest 94:384-391
10. Bhatia R, Holtz M, Niu N, Gray R, Snyder DS, Sawyers CL, Arber DA, Slovak ML, Forman SJ (2003) Persistence of malignant hematopoietic progenitors in chronic myelogenous leukemia patients in complete cytogenetic remission following imatinib mesylate treatment. Blood 101:4701-4707
11. Bocchia M, Gentili S, Abruzzese E, Fanelli A, Iuliano F, Tabilio A, Amabile M, Forconi F, Pirrotta MT, Gozzetti A, Ippoliti M, Raspadori I, Lauria F (2003) Imatinib plus CMLVAX100 (p210 derived multipeptide vaccine): induction of complete molecular responses in patients with chronic myeloid leukaemia (CML) showing persistent residual disease during treatment with imatinib mesylate. Blood 102:30a
12. Brummendorf TH, Holyoake TL, Rufer N, Barnett MJ, Schulzer M, Eaves CJ, Eaves AC, Lansdorp PM (2000) Prognostic implications of differences in telomere length between normal and malignant cells from patients with chronic myeloid leukemia measured by flow cytometry. Blood 95:1883-1890
13. Buchdunger E, Zimmermann J, Mett H, Meyer T, Muller M, Druker BJ, Lydon NB (1996) Inhibition of the Abl protein-tyrosine kinase in vitro and in vivo by a 2-phenylaminopyrimidine derivative. Cancer Res 56:100-104
14. Burchert A, Wolfl S, Schmidt M, Brendel C, Denecke B, Cai D, Odyvanova L, Lahaye T, Muller MC, Berg T, Gschaidmeier H, Wittig B, Hehlmann R, Hochhaus A, Neubauer A (2003) Interferon-alpha, but not the ABL-kinase inhibitor imatinib (STI571), induces expression of myeloblastin and a specific T-cell response in chronic myeloid leukemia. Blood 101:259-264
15. Burton CH, Avery S, Ranger A, Nadal E, Nathan I, Olavarria E, Apperley J, Goldman J (2003) Use of RT-PCR to monitor the possible benefit of adding interferon-alpha to imatinib for patients with CML in chronic phase. Blood 102:908a
16. Campbell JD, Cook G, Holyoake TL (2001) Evolution of bone marrow transplantation - the original immunotherapy. Trends Immunol 22:88-92
17. Carter BZ, Schober WD, McQueen T, Andreeff M (2003) Reguation of survivin expression through bcr-abl/MAPK cascade: survivin as a therapeutic target in STI571 resistant CML cells. Blood 102:651a
18. Cathcart K, Pinilla-Ibarz J, Korontsvit T, Schwartz J, Zakhaleva V, Papadopoulos EB, Scheinberg DA (2004) A multivalent bcr-abl fusion peptide vaccination trial in patients with chronic myeloid leukemia. Blood 103:1037-1042
19. + hematopoietic progenitors from human cord blood differentiate along two independent dendritic cell pathways in response to granulocyte-macrophage colony-stimulating factor plus tumor necrosis factor alpha, II: functional analysis. Blood 90:1458-1470
20. Cervantes F (2003) Durability of responses to imatinib in newly diagnosed chronic phase chronic myeloid leukaemia: 24 month update from the IRIS study. Blood 102:181a
21. Champlin R, Khouri I, Shimoni A, Gajewski J, Kornblau S, Molldrem J, Ueno N, Giralt S, Anderlini P (2000) Harnessing graft-versus-malignancy: non-myeloablative preparative regimens for allogeneic haematopoietic transplantation, an evolving strategy for adoptive immunotherapy. Br J Haematol 111:18-29
22. Choudhury A, Gajewski JL, Liang JC, Popat U, Claxton DF, Kliche KO, Andreeff M, Champlin RE (1997) Use of leukemic dendritic cells for the generation of antileukemic cellular cytotoxicity against Philadelphia chromosome-positive chronic myelogenous leukemia. Blood 89:1133-1142
23. Clark RE, Dodi IA, Hill SC, Lill JR, Aubert G, Macintyre AR, Rojas J, Bourdon A, Bonner PL, Wang L, Christmas SE, Travers PJ, Creaser CS, Rees RC, Madrigal JA (2001) Direct evidence that leukemic cells present HLA-associated immunogenic peptides derived from the BCR-ABL b3a2 fusion protein. Blood 98:2887-2893
24. Clift RA, Anasetti C (1997) Allografting for chronic myeloid leukaemia. Baillieres Clin Haematol 10:319-336
25. Daley GQ, Van Etten RA, Baltimore D (1990) Induction of chronic myelogenous leukemia in mice by the P210bcr/abl gene of the Philadelphia chromosome. Science 247:824-830
26. de Castro FA, Palma PV, Morais FR, Simoes BP, Carvalho PV, Ismael SJ, Lima CP, Voltarelli JC (2003) Immunological effects of interferon-alpha on chronic myelogenous leukemia. Leuk Lymphoma 44:2061-2067
27. Deininger MW, Goldman JM, Lydon N, Melo JV (1997) The tyrosine kinase inhibitor CGP57148B selectively inhibits the growth of BCR-ABL-positive cells. Blood 90:3691-3698
28. Dhodapkar MV, Steinman RM, Krasovsky J, Munz C, Bhardwaj N (2001) Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells. J Exp Med 193:233-238
29. Dietz AB, Souan L, Knutson GJ, Bulur PA, Litzow MR, Vuk-Pavlovic S (2004) Imatinib mesylate inhibits T cell proliferation in vitro and delayed-type hypersensitivity in vivo. Blood 104:1094-1099
30. Druker BJ, Tamura S, Buchdunger E, Ohno S, Segal GM, Fanning S, Zimmermann J, Lydon NB (1996) Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med 2:561-566
31. Druker BJ, Sawyers CL, Kantarjian H, Resta DJ, Reese SF, Ford JM, Capdeville R, Talpaz M (2001) Activity of a specific inhibitor of the BCR-ABL tyrosine kinase in the blast crisis of chronic myeloid leukemia and acute lymphoblastic leukemia with the Philadelphia chromosome. N Engl J Med 344:1038-1042
32. Drummond MW, Holyoake TL (2001) Tyrosine kinase inhibitors in the treatment of chronic myeloid leukaemia: so far so good? Blood Rev 15:85-95
33. Eaves AC, Cashman JD, Gaboury LA, Eaves CJ (1987) Clinical significance of long-term cultures of myeloid blood cells. Crit Rev Oncol Hematol 7:125-138
34. Eisendle K, Lang A, Eibl B, Nachbaur D, Glassl H, Fiegl M, Thaler J, Gastl G (2003) Phenotypic and functional deficiencies of leukaemic dendritic cells from patients with chronic myeloid leukaemia. Br J Haematol 120:63-73
35. Feng L, Drummond MW, Byrne J, Shepherd PC, Apperley JF, O'Brien SG, Craddock C, Clark RE, Cervantes F, Lennard AL, Holyoake TL, Szydlo RM, Goldman JM, Kaeda JS (2002) Molecular monitoring of complete cytogenic responders following treatment with imatinib (STI571, Glivec) for CML: a report from the UKSTI571 study group. Blood 100:1425
36. Gabriele L, Borghi P, Rozera C, Sestili P, Andreotti M, Guarini A, Montefusco E, Foa R, Belardelli F (2004) IFN-alpha promotes the rapid differentiation of monocytes from patients with chronic myeloid leukemia into activated dendritic cells tuned to undergo full maturation after LPS treatment. Blood 103:980-987
37. Gale RP, Horowitz MM, Bortin MM (1989) IBMTR analysis of bone marrow transplants in acute leukaemia. Advisory Committee of the International Bone Marrow Transplant Registry (IBMTR). Bone Marrow Transplant 4[Suppl 3]:83-84
38. Gale RP, Horowitz MM, Ash RC, Champlin RE, Goldman JM, Rimm AA, Ringden O, Stone JA, Bortin MM (1994) Identical-twin bone marrow transplants for leukemia. Ann Intern Med 120:646-652
39. Gao L, Bellantuono I, Elsasser A, Marley SB, Gordon MY, Goldman JM, Stauss HJ (2000) Selective elimination of leukemic CD34(+) progenitor cells by cytotoxic T lymphocytes specific for WT1. Blood 95:2198-2203
40. Gao L, Xue SA, Hasserjian R, Cotter F, Kaeda J, Goldman JM, Dazzi F, Stauss HJ (2003) Human cytotoxic T lymphocytes specific for Wilms' tumor antigen-1 inhibit engraftment of leukemia-initiating stem cells in non-obese diabetic-severe combined immunodeficient recipients. Transplantation 75:1429-1436
41. Goldman JM, Gale RP, Horowitz MM, Biggs JC, Champlin RE, Gluckman E, Hoffmann RG, Jacobsen SJ, Marmont AM, McGlave PB et al (1988) Bone marrow transplantation for chronic myelogenous leukemia in chronic phase: increased risk for relapse associated with T-cell depletion. Ann Intern Med 108:806-814
42. Goodman M, Spector N, Rodrigues G, Cassileth PA (1998) Interleukin-2 therapy for advanced chronic myeloid leukemia. Leukemia 12:1682-1684
43. Gorre ME, Mohammed M, Ellwood K, Hsu N, Paquette R, Rao PN, Sawyers CL (2001) Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 293:876-880
44. Graham SM, Jorgensen HG, Allan E, Pearson C, Alcorn MJ, Richmond L, Holyoake TL (2002) Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. Blood 99:319-325
45. Graner MW, Zeng Y, Feng H, Katsanis E (2003) Tumor-derived chaperone-rich cell lysates are effective therapeutic vaccines against a variety of cancers. Cancer Immunol Immunother 52:226-234
46. Granucci F, Vizzardelli C, Pavelka N, Feau S, Persico M, Virzi E, Rescigno M, Moro G, Ricciardi-Castagnoli P (2001) Inducible IL-2 production by dendritic cells revealed by global gene expression analysis. Nat Immunol 2:882-888
47. Greiner J, Ringhoffer M, Taniguchi M, Schmitt A, Kirchner D, Krahn G, Heilmann V, Gschwend J, Bergmann L, Dohner H, Schmitt M (2002) Receptor for hyaluronan acid-mediated motility (RHAMM) is a new immunogenic leukemia-associated antigen in acute and chronic myeloid leukemia. Exp Hematol 30:1029-1035
48. Greiner J, Ringhoffer M, Taniguchi M, Hauser T, Schmitt A, Dohner H, Schmitt M (2003) Characterization of several leukemia-associated antigens inducing humoral immune responses in acute and chronic myeloid leukemia. Int J Cancer 106:224-231
49. Hahn EA, Glendenning GA, Sorensen MV, Hudgens SA, Druker BJ, Guilhot F, Larson RA, O'Brien SG, Dobrez DG, Hensley ML, Cella D (2003) Quality of life in patients with newly diagnosed chronic phase chronic myeloid leukemia on imatinib versus interferon alfa plus low-dose cytarabine: results from the IRIS Study. J Clin Oncol 21:2138-2146
50. Hochhaus A, Fischer T, Brummendorf TH, Schoch C, Muller MC, Merx K, Berger U, Gschaidmeier H, Hehlmann R (2002) Imatinib (Glivec) and pegylated interferon a2a (Pegasys) phase I/II combination study in chronic phase myelogenous leukaemia (CML). Blood 100:164a
51. Holyoake T, Jiang X, Eaves C, Eaves A (1999) Isolation of a highly quiescent subpopulation of primitive leukemic cells in chronic myeloid leukemia. Blood 94:2056-2064
52. Holyoake TL, Jiang X, Jorgensen HG, Graham S, Alcorn MJ, Laird C, Eaves AC, Eaves CJ (2001) Primitive quiescent leukemic cells from patients with chronic myeloid leukemia spontaneously initiate factor-independent growth in vitro in association with up-regulation of expression of interleukin-3. Blood 97:720-728
53. Holyoake TL, Allan EK, Graham SJ, Godden JL, Mountford JC, Gilmour D, Richmond L, Jorgensen HG (2003) Combination therapies including imatinib do not eradicate quiescent chronic myeloid leukaemia stem cells in vitro. Blood 102:71a
54. Horowitz MM, Gale RP, Sondel PM, Goldman JM, Kersey J, Kolb HJ, Rimm AA, Ringden O, Rozman C, Speck B et al (1990) Graft-versus-leukemia reactions after bone marrow transplantation. Blood 75:555-562
55. Hughes T, Branford S (2003) Molecular monitoring of chronic myeloid leukemia. Semin Hematol 40:62-68
56. Hughes TP, Economou K, Mackinnon S, Vlitos M, Arthur CK, Guo AP, Rassool F, Apperley JF, Hows J, Goldman JM (1989) Slow evolution of chronic myeloid leukaemia relapsing after BMT with T-cell depleted donor marrow. Br J Haematol 73:462-467
57. Hughes TP, Kaeda J, Branford S, Rudzki Z, Hochhaus A, Hensley ML, Gathmann I, Bolton AE, van Hoomissen IC, Goldman JM, Radich JP (2003) Frequency of major molecular responses to imatinib or interferon alfa plus cytarabine in newly diagnosed chronic myeloid leukemia. N Engl J Med 349:1423-1432
58. Kloosterboer FM, van Luxemburg-Heijs SA, van Soest RA, Barbui AM, van Egmond HM, Strijbosch MP, Kester MG, Marijt WA, Goulmy E, Willemze R, Falkenburg JH (2004) Direct cloning of leukemia-reactive T cells from patients treated with donor lymphocyte infusion shows a relative dominance of hematopoiesis-restricted minor histocompatibility antigen HA-1 and HA-2 specific T cells. Leukemia 18:798-808
59. KoIb HJ, Mittermuller J, Clemm C, Holler E, Ledderose G, Brehm G, Heim M, Wilmanns W (1990) Donor leukocyte transfusions for treatment of recurrent chronic myelogenous leukemia in marrow transplant patients. Blood 76:2462-2465
60. Kolb HJ, Schattenberg A, Goldman JM, Hertenstein B, Jacobsen N, Arcese W, Ljungman P, Ferrant A, Verdonck L, Niederwieser D et al (1995) Graft-versus-leukemia effect of donor lymphocyte transfusions in marrow grafted patients. European Group for Blood and Marrow Transplantation Working Party Chronic Leukemia. Blood 86:2041-2050
61. le Coutre P, Mologni L, Cleris L, Marchesi E, Buchdunger E, Giardini R, Formelli F, Gambacorti-Passerini C (1999) In vivo eradication of human BCR/ABL-positive leukemia cells with an ABL kinase inhibitor. J Natl Cancer Inst 91:163-168
62. Li Z, Qiao Y, Laska E, Liu B, Glynn L, Kulko J, Bona RD, Gaffney J, Hegde UP, Moyo V, Srivastava PK (2003) Autologous heat shock protein 70-peptide complex as a vaccine for chronic myeloid leukaemia in chronic phase: an updated phase I study. Blood 102:911a
63. Mathe G, Amiel JL, Schwarzenberg L, Cattan A, Schneider M (1965) Adoptive immunotherapy of acute leukemia: experimental and clinical results. Cancer Res 25:1525-1531
64. Mauro MJ, O'Dwyer M, Stone RM, Walker T, Druker B (2002) Preliminary evaluation of the combination of imatinib mesylate (Gleevec) with low-dose Ara-C as initial therapy for newly diagnosed chronic phase CML. Blood 101:165a
65. Mohty M, Jarrossay D, Lafage-Pochitaloff M, Zandotti C, Briere F, de Lamballeri XN, Isnardon D, Sainty D, Olive D, Gaugler B (2001) Circulating blood dendritic cells from myeloid leukemia patients display quantitative and cytogenetic abnormalities as well as functional impairment. Blood 98:3750-3756
66. Mohty M, Jourdan E, Ben Mami N, Vey N, Damaj G, Blaise D, Isnardon D, Olive D, Gaugler B (2004) Imatinib and plasmacytoid dendritic cell function in chronic myeloid leukemia patients. Blood 103:4666-4668
67. Molldrem JJ, Lee PP, Wang C, Felio K, Kantarjian HM, Champlin RE, Davis MM (2000) Evidence that specific T lymphocytes may participate in the elimination of chronic myelogenous leukemia. Nat Med 6:1018-1023
68. Morse MA, Lyerly HK, Li Y (1999) The role of IL-13 in the generation of dendritic cells in vitro. J Immunother 22:506-513
69. O'Brien SG, Guilhot F, Larson RA, Gathmann I, Baccarani M, Cervantes F, Cornelissen JJ, Fischer T, Hochhaus A, Hughes T, Lechner K, Nielsen JL, Rousselot P, Reiffers J, Saglio G, Shepherd J, Simonsson B, Gratwohl A, Goldman JM, Kantarjian H, Taylor K, Verhoef G, Bolton AE, Capdeville R, Druker BJ (2003) Imatinib compared with interferon and low-dose cytarabine for newly diagnosed chronic-phase chronic myeloid leukemia. N Engl J Med 348:994-1004
70. O'Dwyer ME, Mauro MJ, Kuyl JM, Paquette R, Sawyers CL, Druker BJ (2001) Preliminary evaluation of the combination of imatinib mesylate (Gleevec) in combination with low dose interferon-alpha for the treatment of chronic phase CML. Blood 100:846a
71. Or R, Shapira MY, Resnick I, Amar A, Ackerstein A, Samuel S, Aker M, Naparstek E, Nagler A, Slavin S (2003) Non-myeloablative allogeneic stem cell transplantation for the treatment of chronic myeloid leukemia in first chronic phase. Blood 101:441-445
72. Osman Y, Takahashi M, Zheng Z, Koike T, Toba K, Liu A, Furukawa T, Aoki S, Aizawa Y (1999) Generation of bcr-abl specific cytotoxic T-lymphocytes by using dendritic cells pulsed with bcr-abl (b3a2) peptide: its applicability for donor leukocyte transfusions in marrow grafted CML patients. Leukemia 13:166-174
73. Osman Y, Takahashi M, Zheng Z, Toba K, Liu A, Furukawa T, Aizawa Y, Shibata A, Koike T (1999) Activation of autologous or HLA-identical sibling cytotoxic T lymphocytes by blood derived dendritic cells pulsed with tumor cell extracts. Oncol Rep 6:1057-1063
74. Ossenkoppele GJ, Stam AG, Westers TM, de Gruijl TD, Janssen JJ, van de Loosdrecht AA, Scheper RJ (2003) Vaccination of chronic myeloid leukemia patients with autologous in vitro cultured leukemic dendritic cells. Leukemia 17:1424-1426
75. Pawelec G (2004) Tumour escape: antitumour effectors too much of a good thing? Cancer Immunol Immunother 53:262-274
76. Pinilla-Ibarz J, Cathcart K, Korontsvit T, Soignet S, Bocchia M, Caggiano J, Lai L, Jimenez J, Kolitz J, Scheinberg DA (2000) Vaccination of patients with chronic myelogenous leukemia with bcr-abl oncogene breakpoint fusion peptides generates specific immune responses. Blood 95:1781-1787
77. Ridgway D (2003) The first 1000 dendritic cell vaccinees. Cancer Invest 21:873-886
78. Rowley JD (1973) Letter: a new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature 243:290-293
79. Sallusto F, Lanzavecchia A (1994) Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/ macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med 179:1109-1118
80. Sato N, Narita M, Takahashi M, Yagisawa K, Liu A, Abe T, Nikkuni K, Furukawa T, Toba K, Aizawa Y (2003) The effects of STI571 on antigen presentation of dendritic cells generated from patients with chronic myelogenous leukemia. Hematol Oncol 21:67-75
81. Sawyers CL (1999) Chronic myeloid leukemia. N Engl J Med 340:1330-1340
82. Sawyers CL, Hochhaus A, Feldman E, Goldman JM, Miller CB, Ottmann OG, Schiffer CA, Talpaz M, Guilhot F, Deininger MW, Fischer T, O'Brien SG, Stone RM, Gambacorti-Passerini CB, Russell NH, Reiffers JJ, Shea TC, Chapuis B, Coutre S, Tura S, Morra E, Larson RA, Saven A, Peschel C, Gratwohl A, Mandelli F, Ben-Am M, Gathmann I, Capdeville R, Paquette RL, Druker BJ (2002) Imatinib induces hematologic and cytogenetic responses in patients with chronic myelogenous leukemia in myeloid blast crisis: results of a phase II study. Blood 99:3530-3539
83. Shah NP, Nicoll JM, Nagar B, Gorre ME, Paquette RL, Kuriyan J, Sawyers CL (2002) Multiple BCR-ABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (STI571) in chronic phase and blast crisis chronic myeloid leukemia. Cancer Cell 2:117-125
84. Silver RT, Woolf SH, Hehlmann R, Appelbaum FR, Anderson J, Bennett C, Goldman JM, Guilhot F, Kantarjian HM, Lichtin AE, Talpaz M, Tura S (1999) An evidence-based analysis of the effect of busulfan, hydroxyurea, interferon, and allogeneic bone marrow transplantation in treating the chronic phase of chronic myeloid leukemia: developed for the American society of hematology. Blood 94:1517-1536
85. Slavin S, Nagler A, Naparstek E, Kapelushnik Y, Aker M, Cividalli G, Varadi G, Kirschbaum M, Ackerstein A, Samuel S, Amar A, Brautbar C, Ben-Tal O, Eldor A, Or R (1998) Non-myeloablative stem cell transplantation and cell therapy as an alternative to conventional bone marrow transplantation with lethal cytoreduction for the treatment of malignant and non-malignant hematologic diseases. Blood 91:756-763
86. Spierings E, Wieles B, Goulmy E (2004) Minor histocompatibility antigens - big in tumour therapy. Trends Immunol 25:56-60
87. Taieb J, Maruyama K, Borg C, Terme M, Zitvogel L (2004) Imatinib mesylate impairs Flt3L-mediated dendritic cell expansion and antitumor effects in vivo. Blood 103:1966-1967 (Author reply, 1967)
88. Takahashi T, Tanaka Y, Nieda M, Azuma T, Chiba S, Juji T, Shibata Y, Hirai H (2003) Dendritic cell vaccination for patients with chronic myelogenous leukemia. Leuk Res 27:795-802
89. Talpaz M, Silver RT, Druker BJ, Goldman JM, Gambacorti-Passerini C, Guilhot F, Schiffer CA, Fischer T, Deininger MW, Lennard AL, Hochhaus A, Ottmann OG, Gratwohl A, Baccarani M, Stone R, Tura S, Mahon FX, Fernandes-Reese S, Gathmann I, Capdeville R, Kantarjian HM, Sawyers CL (2002) Imatinib induces durable hematologic and cytogenetic responses in patients with accelerated phase chronic myeloid leukemia: results of a phase 2 study. Blood 99:1928-1937
90. Topaly J, Zeller WJ, Fruehauf S (2002) Combination therapy with imatinib mesylate (STI571): synopsis of in vitro studies. Br J Haematol 119:3-14
91. Turtle CJ, Hart DN (2004) Dendritic cells in tumor immunology and immunotherapy. Curr Drug Targets 5:17-39
92. Vey N, Blaise D, Lafage M, Olive D, Viens P, Baume D, Camerlo J, Stoppa AM, Gabus R, Brandely M, Hercend T, Maraninchi D (1999) Treatment of chronic myelogenous leukemia with interleukin-2: a phase II study in 21 patients. J Immunother 22:175-181
93. Vivancos P, Granena A Jr, Sarra J, Granena A (1999) Treatment with interleukin-2 (IL-2) and interferon (IFN (alpha 2b)) after autologous bone marrow or peripheral blood stem cell transplantation in onco-hematological malignancies with a high risk of relapse. Bone Marrow Transplant 23:169-172
94. Wang L, Butt NM, Atherton MG, Clark RE (2004) Dendritic cells become BCR-ABL negative in chronic myeloid leukaemia patients successfully treated with imatinib. Leukemia 18:1025-1027
95. Wieder ED, Kant S, Lu S, He Z, Molldrem JJ (2003) PR1 peptide vaccination of myeloid leukaemia patients induces PR1-specific CTL with high CCR7 expression. Blood 102:611a
96. Zeis M, Siegel S, Wagner A, Schmitz M, Marget M, Kuhl-Burmeister R, Adamzik I, Kabelitz D, Dreger P, Schmitz N, Heiser A (2003) Generation of cytotoxic responses in mice and human individuals against hemalological malignancies using survivin-RNA-transfected dendritic cells. J Immunol 170:5391-5397
97. Zeng Y, Graner MW, Feng H, Li G, Kalsanis E (2004) Imatinib mesylate effectively combines with chaperone-rich cell lysate-loaded dendritic cells to treat bcr-abl+ murine leukemia. Int J Cancer 110:251-259